Solar energy conversion: From natural to artificial

Journal of Photochemistry and Photobiology C: Photochemistry Reviews 31 (2017) 36–83

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Journal of Photochemistry and Photobiology C: Photochemistry Reviews journal homepage: www.elsevier.com/locate/jphotochemrev

Solar energy conversion: From natural to artificial photosynthesis Mohamed E. El-Khouly a,∗ , Eithar El-Mohsnawy b , Shunichi Fukuzumi c,d,∗∗ a

Department of Chemistry, Faculty of Science, Kafrelsheikh University, Kafrelsheikh, 33516, Egypt Department of Botany, Faculty of Science, Kafrelsheikh University, Kafrelsheikh 33516, Egypt c Department of Chemistry and Nano Science, Ewha Womans University, Seoul 120-750, Korea d Faculty of Science and Engineering, Meijo University, Nagoya, Aichi 468-8502, Japan b

a r t i c l e

i n f o

Article history: Received 13 October 2016 Received in revised form 5 February 2017 Accepted 9 February 2017 Available online 20 February 2017 Keywords: Natural photosynthesis Artificial photosynthesis Semi-artificial photosynthesis

a b s t r a c t Solar energy has a great potential as a clean, cheap, renewable and sustainable energy source, but it must be captured and transformed into useful forms of energy as plants do. An especially attractive approach is to store solar energy in the form of chemical bonds as performed in natural photosynthesis. Therefore, there is a challenge in the last decades to construct semi-artificial and artificial photosynthetic systems, which are able to efficiently capture and convert solar energy and then store it in the form of chemical bonds of solar fuels such as hydrogen or hydrogen peroxide, while at the time producing oxygen from water. Here, we review the molecular level details of the natural photosynthesis, particularly the mechanism of light dependent reactions in oxygen evolving organisms, absorption efficiency of solar energy and direct energy production. We then demonstrate the concept and examples of the semi-artificial photosynthesis in vitro. Finally we demonstrate the artificial photosynthesis, which is composed of light harvesting and charge-separation units together with catalytic units of water oxidation and reduction as well as CO2 reduction. The reported photosynthetic molecular and supramolecular systems have been designed and examined in order to mimic functions of the antenna-reaction center of the natural process. The relations between structures and photochemical behaviors of these artificial photosynthetic systems are discussed in relation to the rates and efficiencies of charge-separation and charge-recombination processes by utilizing the laser flash photolysis technique, as well as other complementary techniques. Finally the photocatalytic production of hydrogen peroxide as a more promising solar fuel is discussed in relation with the natural photosynthesis, which also produces hydrogen peroxide in addition to NADPH. © 2017 Elsevier B.V. All rights reserved.

Contents 1. 2.

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Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37 Natural photosynthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38 2.1. Efficiency of absorption solar energy (natural antenna system) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38 2.2. Photosystem II (PSII) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38 2.3. Photosystem I (PSI) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41 2.4. Photosynthetic electron transport chain in natural system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43 2.5. Biohydrogen production via photosynthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44 2.5.1. Hydrogenases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44 2.5.2. Insights to the hydrogenases mechanism of small molecule mimics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 46 2.5.3. Production of hydrogen in native system in vivo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 46 Hydrogenase-ferredoxin fusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47 Semi-artificial system in vitro . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47 4.1. Construction of PSI and NiFe-Hydrogenases via PsaE . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 48 4.2. Wiring PSI through nanoconstruction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49

∗ Corresponding author. ∗∗ Corresponding author at: Department of Chemistry and Nano Science, Ewha Womans University, Seoul, 120-750, Korea. E-mail addresses: [email protected] (M.E. El-Khouly), [email protected] (S. Fukuzumi). http://dx.doi.org/10.1016/j.jphotochemrev.2017.02.001 1389-5567/© 2017 Elsevier B.V. All rights reserved.

M.E. El-Khouly et al. / Journal of Photochemistry and Photobiology C: Photochemistry Reviews 31 (2017) 36–83

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4.3. Immobilized PSI layer(s) on nanocrystalline semiconductors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49 4.4. Coating PSI with platinum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 50 Artificial photosynthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 50 5.1. Covalently linked molecular systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 51 5.1.1. Porphyrin-based donor-acceptor molecular systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 51 5.1.2. Subphthalocyanines based light harvesting complexes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55 5.1.3. BODIPY-based light harvesting systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58 5.2. Supramolecular artificial photosynthetic systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61 5.2.1. Metal-ligand interactions of porphyrins/naphthalocyanines with electron acceptors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63 5.2.2. Supramolecular photosynthetic complexes via crown ether-ammonium cation interactions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69 5.2.3. Axial coordination in donor–acceptor ensembles of silicon phthalocyanines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70 5.2.4. Anion-complexation-induced stabilization of charge separation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73 5.3. Artificial photosynthetic systems for production of hydrogen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 74 5.4. Artificial photosynthetic systems for production of hydrogen peroxide . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 78 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 79 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 79

Mohamed E. El-Khouly was born in Egypt and earned his PhD degree in photochemistry from Tohoku University, Japan (2002). After that, he continued his research in Japan funded from Venture Business Laboratory (2003–2004), Center of Excellence (2004–2006), and Japan Society for the Promotion Science (2006–2008). In the period of 2008–2012, he joined the research group of Prof. Shunichi Fukuzumi at Osaka University as a specially appointed Associate Professor. Sine 2013, he has been a Full Professor at Kafrelsheikh University. His research interests are mainly focused on ultrafast laser photolysis of the molecular and supramolecular light harvesting systems, carbon nanostructures, artificial photosynthesis complexes, material science, and laser chemistry. Eithar El-Mohsnawy was born in Egypt and received his PhD degree in the Algal Biotechnology from Faculty of Biology and Biotechnology, Ruhr-University Bochum, Germany (2007). He was hired as a Lecturer at Suez Canal University, Egypt on 2007. Since 2014, he moved to Kafrelsheikh University as an Associate Professor. His research interests involved photosystem 1 structure and function, photosynthetic electron transport chain, native and semi-artificial photosynthesis, and biohydrogen production.

Shunichi Fukuzumi earned a bachelor’s degree and PhD degree in applied chemistry at Tokyo Institute of Technology in 1973 and 1978, respectively. After working as a postdoctoral fellow (1978–1981) at Indiana University in USA, he joined the Department of Applied Chemistry, Osaka University, as an Assistant Professor in 1981 and was promoted to a Full Professor in 1994. His research interests are artificial photosynthesis and electron transfer chemistry. He was the leader of an ALCA (Advanced Low Carbon Technology Research and Development) project that started in 2011. He is now a Distinguished Professor of Ewha Womans University, a Designated Professor of Meijo University, a Professor Emeritus of Osaka University.

1. Introduction There is unprecedented interest in renewable energies that are collected from natural resources as alternative to fossil fuels [1–6]. Among them, solar energy has an enormous potential as an abundant, cheap, clean and sustainable energy source [7,8], but it cannot be employed as such, so it must be captured and transformed into useful forms of energy as plants do. An especially attractive approach in the recent years is to convert this solar energy to chemical bonds and store it in stable organic molecules as performed in natural photosynthetic process [9–12]. Simply, natural photosynthesis is the process by which sunlight is absorbed, trans-

ferred and converted into the energy of chemical bonds of organic molecules that are used for building up the body of all living organisms [7–12]. Compared to the total arriving solar energy to the earth surface (about 24 × 1020 kJ/year), the amount of absorbed energy is considered to be very limited (0.1%) [13,14]. Beside the production of billion tons biomass per year, more than 10% of the total atmospheric CO2 are consumed and substituted by oxygen [13,14]. The idea of using the basic science underlying photosynthesis in the design of solar fuels has been discussed for over 100 years ago by an Italian scientist, Giacomo Ciamician [15], in a famous lecture entitled “The photochemistry of the future”, when he stated: “Photochemistry will artificially put solar energy to practical uses. To do this, it would be sufficient to be able to imitate the assimilating processes of plants”. Nowadays Ciamician’s idea for production of ‘solar fuel’ from inexpensive and abundant material such as water that could be split into oxygen and hydrogen has attracted increasing attention [16–19]. Hydrogen is often called a fuel of the future since its combustion generates water as the product. A highly attractive way for the light driven water splitting in newly designed devices would be to mimic the molecular and supramolecular organization and functions of the natural photosynthetic system, i.e., “artificial photosynthesis” [20–55]. In the last decades, the artificial photosynthesis has been fascinating scientists in chemistry and biology[w1], who hope to construct efficient photosynthetic systems that are able to capture solar energy efficiently and then, convert and store it in the form of chemical bonds of solar fuels such as hydrogen and hydrogen peroxide, while at the time producing oxygen from water [16–19]. This review summarizes the recent research trends of natural, semi-artificial and artificial photosynthesis in terms of concepts, design, and examples. We focus at the beginning on the molecular level details of the natural photosynthesis, particularly Photosystem I (PSI), Photosystem II (PSII), mechanism of light dependent reactions in oxygen evolving organisms, biohydrogen production via photosynthesis and direct energy production, and production of hydrogen in natural systems in vivo. In the second part, we describe the concept of the semi-artificial systems and the ways of producing biohydrogen in semi-artificial devices. At the third part, we demonstrate the concept of artificial photosynthesis and examples of the recently reported photosynthetic molecular and supramolecular systems, from our laboratories and others, in order to mimic functions of the antenna-reaction center of the natural process. The relations between structures and photoinduced reactivities of the reported artificial photosynthetic donor-acceptor systems are discussed in relation to the efficiency of the intramolecular electron-transfer/energy-transfer processes by utilizing the laser photolysis technique and other complementary techniques.

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Finally, the photocatalytic production of hydrogen peroxide as a more promising solar fuel than hydrogen is discussed in relation with the natural photosynthesis, which also produces hydrogen peroxide in addition to NADPH. 2. Natural photosynthesis Photosynthesis is considered to be an essential biological process by which photosynthetic organisms convert solar energy into ATP and NADPH required for carbon dioxide fixation [56]. This process is achieved through two separate reactions: Light reactions (Light dependent reactions) and dark reactions (light independent reactions). In the light dependent reactions, photons are absorbed by antenna chlorophyll systems leading to excitation of special chlorophyll pair followed by water splitting and charge separation to produce NAD(P)H and ATP. In the light independent reactions, the generated ATP and NADPH are consumed to synthesize sugar and other large organic molecules from carbon dioxide [57]. In natural photosynthesis, two different groups of photosynthetic organisms are distinguished based on evolving oxygen. The first group is oxygenic photosynthetic organisms such as purple bacteria, green bacteria, and heliobacteria, which contain only one photosystem and use inorganic reduced compounds as an electron donor [58]. The second group is oxygenic photosynthetic organisms like cyanobacteria, algae and higher plants, which have two different photosystems and use water as an electron donor and consequently molecular oxygen is evolved [59]. On the other hand, photosynthetic organisms are also classified according to the type of photochemical reaction center into type I reaction centers (RCs) that use iron-sulfur as the terminal electron acceptor, (heliobacteria and green sulfur bacteria), and type II RCs that use a quinone as the terminal electron acceptor (EA), such as the filamentous bacteria (Fig. 1) [60,61]. It should be noted that the higher plants, algae and cyanobacteria have both types of PSI and PSII, so these organisms can undergo photosynthetic oxygen evolution; while all other photosynthetic prokaryotes only conduct anoxygenic photosynthesis [60,61]. 2.1. Efficiency of absorption solar energy (natural antenna system) The effective absorption of solar light by antenna pigments is the critical initial step in photosynthesis. The studies done in the last decades have solved the crystal structure of Photosystem II (PSII) in higher plants and Cyanophyta (cyanobacteria), where it proved the existing of PSII in a dimeric form [62–64]. Each monomeric complex contains 19–20 protein subunits that carry a common core antenna pigment complement of about 35 chlorophylls a (Chl-a), 11 ß-carotenes, two pheophytins, about 20 lipid molecules, two plastoquinones, one non-heme iron, two heme irons, four manganese atoms, three or four calcium atoms (one of which is in the Mn4 Ca cluster), three chloride ions, one bicarbonate ion and more than 15 detergents oxygenic [64]. While Photosystem I (PSI) is present in a monomeric form in higher plants and algae [65], it is commonly present in a trimeric form in cyanobacteria [66]. Each monomeric PSI contains 12–14 protein subunits that carry 96 chlorophylls a (Chl-a), 22 ß-carotene, 3 (4Fe4S) clusters, two phylloquinone molecules and 4 lipid molecules [65–70]. Since the efficiency of the light dependent photosynthetic process mainly based on energy capture, both higher plants and algae have additional antenna systems through which a large quantity of solar energy can be absorbed and transferred to the reaction centers [64,65,69,71–74]. In higher plants, there are light harvesting complex (LHC) systems that absorb and transfer the solar energy to PSI and PSII complexes. LHC II is the common antenna system in PSII

of higher plants and chlorophytes [71–74]. As shown in Fig. 2, the X-ray image of LHC-II shows icosahedral shape of proteoliposome [74]. Each one contains 14 chlorophyll molecules that are distinguished as eight Chl-a and six Chl-b molecules. All Chl-b molecules are arranged around the interface between adjacent monomers. Four carotenoid molecules per monomer have been recognized. It is thought that xanthophyll molecules are involved in the nonradiative energy dissipation, beside the absorption properties [74]. Concerning the antenna system of PSI of higher plants and Chlorophyta (Fig. 3), there are four groups of light harvesting complexes (Lhca 1–4) that bind to the side of PSI. About 20 chlorophyll molecules are arranged in strategic locations in the cleft between Lhca and the core. The importance of these complexes is attested by not only providing the required solar energy, but also considering the evolutionary forces that developed the chloroplast of terrestrial plants [68,75–77]. In cyanobacteria (prokaryotes), the X-ray structure of PSII complex showed existence of PSII complex in a dimeric form and each monomer carries 36 chlorophyll a and 7 ß-carotene molecules [62,78–80], while PSI is mainly present in a trimeric form in addition to the monomeric form. Each monomer contains about 96 molecules of Chl-a and 22 molecules of ß-carotene [66,67,70]. Furthermore, cyanobacteria have additional light harvesting complex system that differs from those present in higher plants known as phycobilins. Studies of energy transfer on wild type and phycobilins mutant in cyanobacteria showed that energy was transferred directly to PSI as well as to PSII [81,82]. Phycobilins are water-soluble proteins containing pigments [83–85]. Existing phycobilins on the surface of thylakoid membrane enable them for short distance diffusion that consequently can control the distribution of relative energy transfer from phycobilisomes to PSII and PSI [83]. Studies using fluorescence recovery after photobleaching (FRAP) proved that the phycobilins are mobile protein complexes that diffuse rapidly on the surface of the thylakoid membrane according to incident energy [84,85]. By immersing cyanobacterial cells in high osmotic strength buffers, phycobilins diffusion is blocked [86]. Under these conditions, cells are ‘locked’ in either state 1 or state 2, according to the situation before immersing in the buffers [86]. Time-resolved fluorescence studies showed that about 50–60% of phycobilins are decoupled from PSII on transition to state 2 and energy storage studies indicate that these phycobilins are functionally coupled to PSI [87]. Therefore, it could be concluded that the association between phycobilisomes and reaction centers is transient and unstable [84,85,87]. Fig. 4 shows a model postulated by Kirilovski et al. [88], who suggested the transition of phycobilins from PSII to PSI when going from light to dark conditions. At dark period incubation, cyanobacteria adapt to be at state 2 and the antenna mainly binds to PSI (reduced PQ-pool, low fluorescence; the O level), while at continuous lighting regime, cyanobacteria adapt to be at state 1 where antenna moves to bind mainly to PSII (oxidized PQ-pool, high fluorescence, the M level). 2.2. Photosystem II (PSII) PSII is a one of the biggest membrane protein complexes that are located in the thylakoid membranes of oxygenic photosynthetic organisms. It performs series of light-induced electron-transfer reactions reaching the splitting of water to electrons, protons and molecular oxygen. The structure of PSII has been solved at resolutions from 3.8 to 2.9 Å in two thermophilic cyanobacterial species (Thermosynechococcus elongatus and Thermosynechococcus vulcanus) [63,64,89,90]. The molecular weight of PSII in higher plants is about 350 kDa and it is composed of 17 transmembrane protein subunits in addition to three peripheral proteins and a number of cofactors [64]. The Mn4 Ca cluster is located in the center


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Fig. 1. Diagram shows different types of reaction centers and the photosynthetic electron transport chains in purple bacteria, oxygenic phototrophs, and green sulfur bacteria. (Reprinted with permission from Ref. 61).

Fig. 2. Distribution of photosynthetic pigments in the LHC-II trimer and monomer. A) LHC-II trimer, Stereo view, shows pigments distribution. Monomers are labeled I–III. Color code; Chl-a; green, Chl-b; blue, lutein; yellow, neoxanthin; orange, xanthophyll; magenta, carotenoids; l-cycle. B and C) Pigments arrangement in a monomer at stromal and lumenal sides, respectively. (Reprinted with permission from Ref. 74). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.).

Fig. 3. A) A half ring Lhca arrangement around the monomeric PSI in higher plants with protein subunits. B) Energy pathway. Color code: reaction center chlorophylls unique for plants; Cyan, chlorophylls bound to the Lhca monomers; blue, Lhca linker chlorophylls; red, chlorophylls positioned in the cleft between Lhca and the reaction center; magenta. (Reprinted with permission from Ref. 77). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

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Fig. 4. State transition mechanism model of the photosynthetic energy conversion from phycobilins to photosystems in cyanobacteria. (Reprinted with permission from Ref. 88).

Fig. 5. Cyanobacterial PSII in dimeric form. The protein helices represent as cylinders. Color code: D1 is shown in yellow, D2 is shown in orange, CP43 is shown in green, CP47 is shown in red, cyt b559 is shown in wine red, PsbL, PsbM, and PsbT are shown in medium blue while PsbH, PsbI, PsbJ, PsbK, PsbX, PsbZ and PsbN are shown in gray. The extrinsic protein subunits are PsbO shown in blue, PsbU shown in magenta and PsbV shown in cyan. Regarding to Chl of the D1/D2 reaction center are shown in light green, pheophytins are shown in blue. Chl of the antenna complexes are shown in dark green, ß-carotenes are shown in orange, hemes are shown in red, nonheme Fe is shown in red, QA and QB are shown in purple. The oxygen-evolving complex (OEC) is shown in red. (Reprinted with permission from Ref. 63). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

where the water is splitting into electrons, protons, and molecular oxygen [64]. As shown in Fig. 5, the cyanobacterial PSII is found in dimeric form [63,64]. Each monomer has 19 protein subunits, 35 chlorophyll molecules, 11 ␤-carotenes, two pheophytins, two plastoquinones, two heme irons, one non-heme iron, four manganese atoms, three or four calcium atoms (one of which is in the Mn4 Ca cluster), three chloride ions (two of which are in the vicinity of the Mn4 Ca cluster), one bicarbonate ion, more than 20 lipids, more than 15 detergents and more than 1,300 water molecules were found, yielding a total of 2,795 water molecules in the dimer [63,64]. The electron densities of manganese and calcium atoms in the oxygen-evolving complex (OEC) were well-resolved using X-ray measurements of PSII crystal structure [64]. As seen from Fig. 6, the electron density of the four calcium atoms was found to be lower than those of the manganese atoms, while the five oxygen atoms act to serve as oxo bridges linking the five metal atoms [64]. As shown, the atoms of Mn4 CaO5 cluster build up a cubane-like structure in which the calcium and manganese atoms occupy four corners and the oxygen atoms occupy the other four. The bond distances between the oxygen atoms and the calcium atom in the cubane are generally in the range of 2.4–2.5 Å and those between the oxygen

atoms and manganese atoms are in the range of 1.8–2.1 Å. While the bond distance between one of the oxygen atoms at the corner of the cubane (O5) and the calcium is about 2.7 Å, and those between O5 and the manganese atoms are in the range of 2.4–2.6 Å. In addition to the five oxygen atoms, four water molecules (W1 to W4) are associated with the Mn4 CaO5 cluster, of which W1 and W2 molecules are coordinated to Mn4 with respective distances in the range of 2.1 and 2.2 Å. W3 and W4 molecules are coordinated to the calcium with a distance of about 2.4 Å [64]. Ultrafast kinetics measurements of cyanobacterial PSII showed the presence of two early radical pairs before the electron is transferred to the quinone QA [91,92]. Although PSII shows high activity, it is continuously turned over and this affects the long-term stability in vitro. For this reason, extensive works have been performed to solve this problem. Rögner and his coworkers isolated Psb27 subunit and investigated its role on the stability of PSII [93]. They found that Psb27 acts as an assembly and repairing factor of PSII after light induced [93]. So under light stress conditions, Psb27 played an important role in the activity and vitality of cyanobacterial [93]. The combination of high light intensity and cold stress on thermophilic cyanobacterium T. elon-


Fig. 6. Crystall structure of Mn4 CaO5 cluster, distances (in Angstrom) between the cluster metal atoms and oxygen bridges or water molecules. (Reprinted with permission from Ref. 64).

gatus (30 ◦ C and 1000 mol of photons mg−1 s−1 ) exhibited complete inhibitory effect in case of a Psb27 mutant strain, while wild type cells continued growing [93]. Moreover, Psb27-containing PSII complexes were the predominant PSII type in preparations from wild-type cells grown under cold stress [93]. These investigations showed existing of two different PSII-Psb27 complexes. The first complex is present in monomeric PSII-Psb27 species, which thought to be involved in the assembly of PSII, while the second is found in dimeric PSII-Psb27 complex, which may have a role on the PSII repairing cycle [93]. Electron transfer pathway within PSII mainly depends upon the redox potential of reaction center core P680+ /P680 (the primary oxidant) and other series intermediate electron carriers [94–98]. The recorded redox potential of PSII reaction center (P680+ /P680 ) was found to be +1.27 V [96,98], while the redox potentials of intermediate electron carriers were found to be −640 mV (for Pheo a/Pheo a− ), −30 mV (for QA− /QA ), +970 mV (for TyrZ • /TyrZ ), +930 mV (for O2 /H2 O), and +30 mV (for QB /QB − ) [94,95,97]. In addition to the redox potentials of PSII reaction center and intermediate electron carriers of PSII complex, the distances between these cofactors were found to be an effective parameter that controls the electrons flow. Through high resolution of PSII crystal structure, the distances between P680 and the electron carriers involved the electron transport chain were detected and the electron pathway were confirmed. As shown in Fig. 7, the close distances between P680 and other intermediate electron carriers facilitate the fast electron flow to QB as well as regains electrons from OEC (Oxygen evolving complex) to P680 . The estimated distance between P680 and Pheo a was found to be 14 Å, Pheo a and QA was 14 Å, Tyrz and P680 was 8.4 Å, OEC (Mn4 Ca) and Tyrz was 7 Å, and QA and QB was 14.3 Å [63,99–101]. The sequence and the rate of electron flow were monitored through very fast kinetics measurements of PSII (Fig. 7A). Fig. 7B shows that the electron transfer from P680 to Pheo a occurs in 3 ps, whereas water oxidation occurs in about 1.4 ms [94,95,102,103]. 2.3. Photosystem I (PSI) PSI is considered one of the biggest bio-solar energy converters, catalyzing one of the first photosynthetic steps in cyanobacteria, algae and higher plants [94]. It has an efficient large antenna system

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that absorbs and transfers the light energy to the reaction center (P700 ). PSI is responsible for catalyzing the light driven electron transfer from plastocyanin or cytochrome C6 (Cyt C6 ) on lumen side to ferredoxin on the stromal side [66–68,104–107]. The crystal structures of chlorophyll-a binding PSI core complexes from higher plants and cyanobacteria show great similarity, with minor differences in the outer protein subunits [85]. Specifically, the PSI subunits PsaG and PsaH are detected only in higher plants but missing in cyanobacteria; in contrast, the subunits PsaX and PsaM are detected only in cyanobacteria but not in higher plants (Fig. 8) [65–70,105,106]. Moreover, subunit PsaL has significant structural differences between plants and cyanobacteria. PSI in cyanobacteria is reported to form a trimer under certain physiological conditions, while PSI in higher plants was not observed in trimeric form up to now [69,105–107]. Although PsaM and PsaL subunits are involved in trimeric formation and stabilization of PSI in cyanobacteria [66,67], the absence of PsaM subunit leads to structural changes of PsaL that prevents the trimeric formation of PSI in higher plant in the presence of PsaH [65,69]. Another major structural difference between cyanobacteria and higher plants is recognized by the fact that the higher plants PSI are composed of the core complex and four peripheral chlorophyll a/b binding LHC complexes (Lhca1–Lhca4) that form external antenna. This external antenna is missing in cyanobacterial PSI [68,105,108]. Moreover, the supramolecular organization of the PSI complex shows additional difference between higher plants and cyanobacteria under iron-stress conditions, where cyanobacteria can develop a ring of iron-stress induced (IsiA) subunits surrounding a PSI [109,110]. The trimeric complex shows more stability in thermophilic than in mesophilic cyanobacteria and PSI trimers are the most abundant protein in the thylakoid membrane of T. elongatus and the formation of intact trimers is pivotal for the growth of the cells at low light intensity [108–110]. The molecular weight of trimeric PSI in cyanobacteria is about 1,068,000 Da [66,67,70]. Crystal structure of cyanobacterial PSI is composed of 12 proteins (PsaA, PsaB, PsaC, PsaD, PsaE, PsaF, PsaI, PsaJ, PsaK, PsaL, PsaM and PsaX) and 127 cofactors, which are non-covalently bound. These cofactors are 96 chlorophylls, 22 carotenoids, 3 (4Fe4S) clusters, two phylloquinone molecules, and 4 lipid molecules [67,70]. The large protein subunits PsaA and PsaB are the most important subunits; they are found in the center of the PSI monomers and harbor the majority of chlorophylls and carotenoids of the antenna system as well as most of the cofactors of the electron transport chain from P700 to the first FeS cluster FX [65–70,106–111]. Most protein subunits are immersed in the thylakoid membrane, while the subunits PsaC, PsaD and PsaE are extrinsic subunits that form a stromal hump, which extends beyond the membrane by 90 A◦ [67]. PsaC carries the two terminal FeS clusters, FA and FB . All three subunits together form the docking site for ferredoxin/flavodoxin; with PsaC carrying the terminal FeS clusters FA and FB [67,70]. The reaction center of PSI is composed of six chlorophylls, two phylloquinones and three 4Fe4S clusters [65–70,106–109]. The catalyzing role of PSI can be divided into the process of light capturing, excitation energy transfer and electron transfer. Although charge separation was thought to be initiated from P700 [87], Holzwarth et al. showed that the accessory Chl(s) act as the primary electron donor(s) and the A0 Chl(s) are the primary electron acceptor, while P700 is not oxidized at the first electron-transfer process, but at the second electron-transfer process [111]. As a result of capturing the solar energy and transfer to the reaction center, P700 is oxidized and the electron is transferred stepwise to A0 , A1 and from there subsequently to the three 4Fe4S clusters, named FX , FA and FB (Fig. 9) [65,67]. After the docking of ferredoxin, the electron is transferred from the terminal 4Fe4S cluster of PSI, FB , to the 2Fe2S cluster of ferredoxin or the flavin cofactor of flavodoxin, which acts as a mobile

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Fig. 7. Electron transfer chain in PSII. A) Steps of electron transfer from P680 to QB and from Mn4 Ca to P680 . Color code: Chl a are shown in green, Pheo a are shown in light blue, plastoquinones are shown in purple color, ß-Carotene is shown in orange, Ca2+ is shown in green and Mn atoms are shown in magenta. B) Summary of the distances and electron flow rates through P680 and other cofactors involved electron transfer chain. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 8. Illustration of PSI structures of cyanobacterial and higher plants and their corresponding energy transfer networks. (a) Cyanobacterial PSI (top view). The relative positions of two additional PSI monomers (in blue and red) in a trimer as well as the trimer axis (red disk) are shown. Subunits PsaM, PsaX and PsaL, present near the trimer axis, are highlighted. (b) Energy transfer pathways within the chlorophyll network of cyanobacterial PSI. (c) Top view of the higher plants PSI-LHCI supercomplex. Subunits PsaG and PsaH are highlighted, along with subunit PsaL. Lhca subunits and their associated chlorophylls are shown in blue (Lhca 1 and 2) and cyan (Lhca 3 and 4). (d) Energy transfer pathways in the chlorophyll network of the higher plants PSI-LHCI supercomplex. (Reprinted with permission from Ref. 106). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)


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Fig. 10. Diagram shows the kinetics of electron transfer and the existing distances between cofactors in PSI. Electrons flow from P700 to cofactors A0 , A1 , FX , FA , and FB . The lifetimes of forward electron transfer are shown (solid black arrows) and the lifetimes of backward electron transfer are shown (dashed arrow) from cofactors back to P700 . The distances between neighbor cofactors are shown in a blue color. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 9. Reaction center of PSI and electron-transfer pathway. Site of hybridization between the hydrogenase with PsaC and 3. Deletion of natural phylloquinone and replacement with artificial phylloquinone combined with the hydrogenase.

electron carrier to the ferredoxin-NADP oxidoreductase, which then finally reduces NADP+ to NADPH [65,67]. To complete the cycle, P700+ is re-reduced. The docking site for soluble electron carrier proteins, plastocyanin or cytochrome C6 , is present at the lumenal side of the complex near to P700 . The electron-transport chain is functionally the most important part of PSI [70]. Since the rate of hydrogen production depends upon the electron-transfer chain from PSI to hydrogenase, a direct interaction to hydrogenase is required. Examples of these devices (systems) technology can be modified leading to further improvement. The redox potentials of the primary electron donor (P700 ) and other intermediate electron carriers within PSI have pivotal role on the electron flow within PSI. The recorded redox potential of the primary electron donor of P700 was found to be +430 mV, while the potential of primary electron acceptor A0 was −1000 mV. The estimated redox potential of A1 , FX , FA and FB were recorded as −800, −705, −520 and −580 mV, respectively [67,100,112,113]. The kinetics of electron transfer within PSI complex has been deeply investigated by different research group [114–120]. Beside the redox potential of intermediates electron carriers, the distances among these cofactors have also important role on electron flow from P700 (primary electron donor) to FB (final electron acceptor). The estimated distances of P700 –A0 , A0 –A1 , A1 –FX , FX –FA and FA –FB were found to be 7, 9, 16, 15 and 7 Å, respectively [100,114–120]. As shown in Fig. 10, the lifetimes of forward electron transport from P700 to FB through intermediate electron carriers were 10 ps (from P700 to A0 ), 30 ps (form A0 to A1 ), 200 ns (from A1 to FX ), and 500 ns (from FX to FA /FB ). 2.4. Photosynthetic electron transport chain in natural system In the thylakoid membrane of oxygen evolving organisms, there are two main photosynthetic electron transport chains, the linear and the nonlinear (cyclic) electron transport chains [121–124]. Photosynthetic process is underpinned by the photocatalytic water-splitting reaction that is achieved by water splitting center of PSII in plants, algae and cyanobacteria. Electrons transfer

through a number of internal electron cofactors within PSII (pheophytin and quinones) and PSI (phylloquinone and 4Fe4S clusters) to reach final electron acceptors plastoquinone and ferredoxin, respectively [70,121]. The absorbed solar energy by chlorophylls and other accessory pigments is transferred efficiently and rapidly to the PSII and PSI reaction centers, where charge separation and water splitting take place in PSII (Fig. 11). The first initial energy conversion to electrochemical potential occurs in PSII with a maximum thermodynamic efficiency of about 70% that generates a radical pair • • state P680 + Pheo − [121]. The redox potential of P680•+ is quite highly oxidizing and estimated to be around +1.2 V, while that of • • Pheo − is about −0.5 V [121]. The P680 + generated in PSII regains the liberated electron through the splitting of water molecules at water oxidizing center. Two water molecules are dissociated into dioxygen, four protons and four electrons [64,121]. In oxygenic photosynthetic organisms, this reaction keeps going continuously since the QH2 molecules are oxidized by light absorbed in PSI, where the reducing equivalent is moved along an electron transport chain to PSI, because the absorbed solar energy by chlorophyll antenna molecules excite the reaction center, known as P700, to lift it to a reducing potential of about −1.0 V or more [121,122]. Liberated electrons pass through sequence of electron carriers reaching the final electron acceptor (Ferredoxin FD) allowing reducing equivalents to be transferred to NADPH. For this reason, PSII is considered a water-plastoquinone-oxidoreductase that catalyzes the water splitting to O2 , four protons and electrons:

As shown in Fig. 11, the plastoquinone is cycling electrons transfer between PSII and the cytochrome b6f (Cyt b6f) within the lipid phase in thylakoid membrane that consequently forwards these electrons onto mobile electron carrier protein plastocyanin (Pc) or cytochrome c6 (Cyt c6) bound on the lumenal side of Cyt b6f. These soluble mobile electron carriers in turn transfer the electrons to PSI [122]. Additionally, a proton concentration difference across the thylakoid membrane is generated leading to electrochemical transmembrane potential which in turn is used by the ATP synthase, embedded in the thylakoid membrane, to generate ATP from ADP

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Fig. 11. Diagram shows electrons flow during the light dependent reaction. In non-cyclic electron transport chain, FD transfers electrons to FNR (Ferredoxin-NADP-reductase) and consequently producing NADPH or orient to hydrogenase producing hydrogen. Controlling PSII:PSI ratio, anaerobic condition and induction hydrogenase enzyme enhance the production of hydrogen. In cyclic electron transport chain, FD transfers electron back to Cytb6f. ATP molecules are produced during the electrons flow gradient and the flow protons through ATPase. PSII: Photosystem II, PSI: Photosystem I, PQ: plastoquinone, TEA: terminal electron acceptor, Pc: plastocyanine, Cyclic ETC: cyclic electron transport chain, FD: ferredoxin, FNR: ferredoxin nicotinamide reductase and NADP: nicotinamide adenine dinucleotide phosphate, ATP: adenosine triphosphate.

and Pi [122–124]. The chemical free energy, in form of NADPH and ATP, is utilized during the light independent reactions, which are performed in the cytosol of cyanobacteria and other oxygenic photosynthetic organisms [123,124]. In the linear electron transport, all three transmembrane protein complexes (PSII, Cyt b6f and PSI) are connected in series [122–124]. In the overall process solar energy is used for transferring electrons from water to NADP+ , yielding protons, O2 , ATP and NADPH. In addition to the described linear electron-transfer pathway, an alternative pathway exists (cyclic electron transport). At low activity level of PSII or low NADP+ concentration in stromal side, the reduced electron carrier (ferredoxin, FD) is directed to Cytb6f and the electrons transferred back to plastocyanin or Cyt c6 via the Cyt b6f complex. This process does not require any input energy by PSII so PSII does not involve and consequently there is no evolving O2 [125]. As a result of difference in internal energy content of external electron carriers among PSII, Cyt b6f, PSI, and several ATP molecules are generated. The efficiency of this reaction is high being 55% when driven by red photons, while decreases to about 20% when light is absorbed across the whole solar spectrum [125].

2.5. Biohydrogen production via photosynthesis Autocompanies have already produced hydrogen-powered vehicles that emit water as the only byproduct [126]. Conventional carbon emitting power plants, natural gas and electricity are considered the traditional means for hydrogen manufacture [127]. The efficient process of photosynthesis in natural system paves the way for suggesting a direct production of biohydrogen via switching the electron transport to hydrogenase instead of FNR (FerredoxinNADP-reductase) [128–130]. In natural systems, some organisms are able to hydrogen production in combination with NADPH production [128]. At the beginning of life on the earth, hydrogen was thought to be the only/main energy resource for living of primitive organisms. Therefore, there was no strong evolutionary evidence for the presence of oxygen-resistant hydrogenases [126]. Based on theoretical calculations, the coupling the photosynthetic process with hydrogen production enhances the efficiency of hydrogen production that can reach 40% [129]. However, the actual realistic goal could be close to 10% efficiency [130]. Based on photosynthetic process, there are two known strategies used for hydrogen production:

• Production of hydrogen in native system in vivo • Production of hydrogen in Semi-artificial system in vitro. Both strategies act to enhance the hydrogen production through the combination between two or three main complexes (hydrogenase, PSI and PSII). The development of hydrogen production is obtained through several routes, e.g.) direct or indirect fusion between hydrogenase with synthetic electron carrier(s) or terminal electron acceptor of PSI, improvement of the surrounding conditions of hydrogenase and/or enhancement of the electron pumping to hydrogenase. The nature and structure of these complexes aid to build up the suitable designs for reaching this goal. 2.5.1. Hydrogenases Based on the linker of bimetallic active site cofactors, hydrogenases could be classified into NiFe, FeFe and Hmd-Fe hydrogenases (Fe hydrogenases) [131]. The main differences among these three types are observed in their active site (Figs. 12–14 [131–143]. Hydrogenases were isolated from bacteria, cyanobacteria and chlorophytes [131–133], and have ability to produce hydrogen during the nitrogen fixation [132]. Some unicellular non-heterocystous cyanobacteria are able to do photosynthesis and nitrogen fixation in the same cell, so it is believed that these organisms can hold a temporal partition between photosynthetic oxygen evolution and hydrogenase/nitrogenase mediated hydrogen production in Synechococcus PCC 7942 and Spirulina sp. [134]. FeFe-hydrogenases are commonly isolated from eukaryotic algal species and a few prokaryotes [131]. FeFe-hydrogenases are known to be highly oxygen sensitive, so they are highly turned over, while some other organisms produce oxygen-tolerant hydrogenases such as Aquifex aeolicus, which are able to produce hydrogen even in the presence of oxygen [135]. NiFe-hydrogenases are found mainly in prokaryotic organisms and more tolerance against air compared to FeFe-hydrogenases [134]. 2.5.1.1. NiFe-Hydrogenases. Based on phylogenetic analysis and function, six groups of (NiFe)-hydrogenases are detected [131,133,136,137]. X-ray crystallography and electron paramagnetic resonance (EPR) investigations showed that all (NiFe)-hydrogenases have the same conserved bimetallic active site architecture and also Ni is bound to the protein via four cysteine ligands, where two are terminally coordinated and two bridge the bimetallic centers (Fig. 12) [133,137]. During the catalytic cycle, the center and oxidation state change with the changes


Fig. 12. Structural diagram of NiFe-hydrogenase. A) Enzyme is composed of large protein subunit (dark grey ribbon) carrying bimetallic active site. The small protein subunit (light grey ribbon) is carrying the FeS relay. B) The detail of NiFe-metallic centers active site. Color code: Ni; green ball, oxygen; bright red, nitrogen; blue, sulfur; yellow, hydrocarbon; green sticks, iron; orange-red ball and sticks. (Reprinted with permission from Ref. 133). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

in the nature of the ligand bound in the fifth Ni coordination site [133,137]. The Ni3+ state of the enzymes is oxidatively inactivated, while under reductive activation, hydrogen can link to the Ni2+ state producing a Ni3+ -␮-hydrido complex [133,137]. The (NiFe) active site is immersed in a large protein subunit that has the minimal functional unit of this active site, while the FeS centers are bound to a small protein subunit that binds the hydrogen catalytic center to external redox partners (Fig. 12) [133,136,137]. NiFeSe-hydrogenases have a lot of attention in recent years due to their oxygen-tolerancy [138]. Structurally, they are considered a subgroup from NiFe-hydrogenases, where they are detected and isolated only from microorganisms that are cultivated on a selenium-containing medium [133,138]. Under this condition, some methanogenic or sulfate-reducing microorganisms are capable of constructing NiFeSe-hydrogenases instead of NiFe-hydrogenases, where the standard S-Cys is replaced by a selenocysteine (SeCys) that bound to the Ni in the active site of hydrogenases [138–140]. On the other hand, under selenocysteine limitation, the (NiFeSe)-producing microbes turned to produce only homologues NiFe-hydrogenases [138,139]. Since the H2 -producing activity is observed even in the presence of oxygen, the NiFeSe-hydrogenases are recommended to be used in solar hydrogen producing cells, but not in H2 /O2 fuel cells [133,139,140].

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Fig. 13. A) Structural diagram of FeFe-hydrogenase from Desulfovibrio desulfuricans. FeFe-hydrogenase contains 6 Fe atoms in their H-cluster that are required for their activity. All the metal centers are coordinated by the large (dark grey ribbon) protein subunit. B) The chemical structure of the H-cluster active site. (Reprinted with permission from Ref. 133).

2.5.1.2. FeFe-Hydrogenases. FeFe-Hydrogenases are commonly named as algal hydrogenases and/or diiron hydrogenases [133]. As shown in Fig. 13, there are six iron atoms located in the active site (catalytic H-cluster); four of them build up a (4Fe4S) cluster, where the S-Cys linkage connects the (FeFe) site while the separate iron atoms are labeled proximal or distal [133,137–141]. The H-cluster active site for an algal FeFe-hydrogenase is immersed in a single polypeptide chain. In contrast, the structures of most bacterial FeFe-hydrogenases strongly resemble to that of NiFe-hydrogenase types, with additional FeS clusters, which connect electrons between the active site and the protein surface [133,137]. FTIR and EPR spectroscopic investigations of different FeFe hydrogenases showed that the nature of H-cluster is highly conserved, so all these types of enzymes have the same spectroscopic properties and both (4Fe4S) and (FeFe) components of the H-active site-cluster are redox-active [133,137–141]. The hydrogen production measurements of Clostridium pasteurianum FeFe-hydrogenases exhibited high activity, where the recorded hydrogen production rate was about 3400 ␮mol min−1 mg−1 (in 1 min 1 g of enzyme would produce 83 L of atmospheric pressure hydrogen) [137]. It should be clarified that at oxygen atmosphere, the rate of hydrogen production is irreversibly inhibited due to the destruction effect of oxygen on the (4Fe4S) cluster within the active site rather than the (2Fe) center [141]. Although O2 binding can be blocked by CO inhibition, there is no documented mechanism explaining how FeFe-hydrogenases re-engineer to neutralize

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Fig. 15. Structures of catalytically active synthetic small molecule hydrogenase mimics.

Fig. 14. A) Structural diagram of Fe-hydrogenase from Methanocaldococcus jannaschii, PDB code 3DAG. The active site is immersed in monomeric protein subunit (grey). B) The chemical structure of the dihydrogen activating Fe guanylylpyridinol active site. (Reprinted with permission from Ref. 143).

inhibitory effect of oxygen and consequently remain active in the presence of oxygen [133,137]. 2.5.1.3. Fe-Hydrogenases. The Fe-hydrogenases were isolated and identified in 1990 [142]. These enzymes are commonly known as hydrogen forming methylenetetrahydromethanopterin dehydrogenases and also ‘iron-sulfur cluster-free’ hydrogenases [131,133,142,143]. The cytochrome-free hydrogenotrophic methanogens use it for catalyzing the reversible transfer of hydride to methylenetetrahydromethanopterin from hydrogen molecules (Fig. 14) [143]. This reaction takes place in one step only during the conversion of carbon dioxide to methane [133]. Additionally, the single iron atom is represented as the only metal center in each protein subunit, which is located at the hydrogen-activating Fe guanylylpyridinol catalytic site [143]. Two moles of iron are detected per mole of 76 kDa homodimer [133,143]. This class of hydrogenase is highly O2 sensitive [142]. 2.5.2. Insights to the hydrogenases mechanism of small molecule mimics Studying and understanding the properties of hydrogenases active site and the mechanism of hydrogen production paved the way synthesizing mimic compounds which both resemble hydrogenases and are active hydrogen catalysts [137]. It is obvious that the presence of CO is considered an essential requirement for the activity of hydrogenases, where it is needed for

the coordination of Fe-atom within the hydrogenases active site, so CO acts as a ligand in the active site [133,143]. On the other hand, the stability of iron at low oxidation states is established by aiding of CO ␲-acceptor bond, which makes iron atoms behave more like Pt [145]. The practical investigations have been performed on both active FeFe-hydrogenases and NiFe-hydrogenases enzyme analogues have shown the mechanistic importance of building a proton transport site near the hydrogen activating metal center in a hydrogen catalyst [133,143–146]. By moving three different active mimics from (FeFe) enzyme active sites, having a carbon-, oxygen-, or nitrogen-capped dithiolate, ligand to a [4Fe4S] cluster containing hydrogenase apo-protein, only the nitrogen-containing molecule yielded a catalytically active H-cluster-containing enzyme (Fig. 15) [133,144–146]. Also, in Ni model compounds, the engineering of a second coordination sphere that can function as a proton relay has dramatically enhanced and accelerated the rate of hydrogen evolution [133,145,146]. 2.5.3. Production of hydrogen in native system in vivo Although Chlamydomonas hydrogenase is one of the most known active hydrogenases (up to 2000H2 s−1 ), it is considered the most oxygen-sensitive species [147,148]. Despite a successful direct coupling of photosynthesis and hydrogen production (see Fig. 11), this coupling is highly inefficient because it requires an extremely reduced PSII water-splitting activity combined with anaerobic conditions and finally leads to degradation of the algal culture [149,150]. Compared to Chlamydomonas sp., cyanobacterial hydrogenases are considered more tolerant and able to continuous hydrogen production. By aid of photosynthesis, cyanobacteria can consume earth-abundant inorganic substrates and solar energy for biosynthesis and hydrogen production [127,147–159]. Several strategies have been performed to overcome or decrease these inhibitory effects of oxygen and enhance the hydrogen production within algal or cyanobacterial cell [130]. These strategies are summarized on the following points. 1) Culturing of Chlamydomonas on partially to extremely anaerobic condition [151]. 2) Inhibiting the cyclic electron-transport chain and enhancement the respiration to consume most of oxygen [152].


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Fig. 16. Electron transport competition between FNR and the fused Fd-HydA. The schematic shows that both Fd-HydA and Fd are directly reduced at PSI complex to support hydrogen production, or simultaneous NADPH and hydrogen production. (Reprinted with permission from Ref. 161).

3) Increasing the PSII: PSI ratio either by keeping the organisms under state 1 transition or by deleting the antenna genes [153,154]. 4) Random mutagenesis of Chlamydomonas hydrogenase to decrease its sensitivity toward oxygen [155]. 5) Overexpression of bacterial Fe-hydrogenase within Synechococcus PCC7942 [156] and induction an oxygen tolerant hydrogenase of Ralstonia eutropha that shows low activity but more tolerance [157]. 6) Overexpression a construction of one PSI-stromal-subunit or FD with hydrogenase, which oriented the electrons directly to hydrogenas enzyme [158]. 7) Designed photobioreactor through which some or all mentioned factors are controlled and the conditions were changed to keep the vitality of cells [159,160].

3. Hydrogenase-ferredoxin fusion It is clear that ferredoxin NADP reductase (FNR) is physically bound to the thylakoid membrane in plant and algae and cyanobacteria, so the presence of membrane PSI bound FNR is the main factor inhibiting efficient electron transfer to soluble HydA, which consequently leads to lowering the hydrogen production rates [130,158]. Fd-HydA fusion protein could functionally replace HydA [158]. The protein fusion strategy is a matured approach, being successfully applied to several electron donors and acceptors. Indeed, a fusion between a bacterial FeFe-hydrogenase and Fd enhanced the efficiency of hydrogen production from glucose, another potential source for hydrogen production, in cyanobacterial cells [158]. In contrast, the photocatalytic hydrogen production has much lower light conversion efficiency because additional photons are required to synthesize the sugar molecules supplied to the cyanobacteria [159–161]. Construction achieved by Yacoby et al., who proved that the replacing of ferredoxin with a ferredoxin-hydrogenase fusion changed the bias of electron transfer from FNR to hydrogenase and consequently, led to increasing rate of hydrogen photoproduction (Fig. 16) [161]. These results support the hypothesis of new direction for improvement the biological hydrogen production and a mean to elucidate the mechanisms that control partitioning of photosynthetic electron transport [158–161]. The presence of some copies of single Fd is important for the survival of cell beside hydro-

Fig. 17. Electron-transfer pathways in the Z-scheme of; A) Natural photosynthesis, B) Semiartificial system. All recorded potentials are given versus the standard hydrogen electrode (SHE) in volts. Cytb6f, Cyt c6 and Fd in natural photosystem are replaced by Os1, Os2 and MV in Semiartificial system. (Reprinted with permission from Ref. 164).

gen production [161]. For this, the relative amount of single Fd to Fd-hydrogenase fusion may control the rate of evolving hydrogen. 4. Semi-artificial system in vitro Galvanic cells based on photosynthetic complexes have been designed since 1970 [162]. The charge separation processes in the natural photosystem (Z-scheme) have inspired the design of semi-artificial photosynthesis systems based on organic and inorganic photosensitizers to convert solar energy into chemical energy [162,163]. So, exploiting the yield in light harvest by photosynthetic proteins may further increase the efficiency of solar to chemical energy conversion in semi-artificial systems [164]. Fig. 17 shows photobioelectrochemical half-cells based on PSI and PSII as well as suggesting artificial electron carriers for successful electron gradients in vitro. The electrons provided by PSII are insufficiently energetic, and PSI-based systems require sacrificial electron donors [165] or an externally applied potential [166] to achieve solar to chemical energy conversion. These limitations could be overcome through serial coupling of both light excitation steps of PSI and PSII in a semi-artificial photosynthesis system (Fig. 17B) [165]. In analogy to the natural Z-scheme, PSII would liberate electrons from water, which are then transferred to PSI. The charge separation at PSI would provide electrons, which are energetically high enough for hydrogen evolution. In order to obtain the maximum yields in solar energy conversion, the energy from the charge separation at PSII side needs to be recovered as well. This scheme could be the base that can be modified to reach a continuous hydrogen production [162–165]. A device model for biohydrogen production was suggested and developed by Rögner and his coworkers [168]. To develop the in vitro electron transport and to achieve high photocurrent, the system should exhibit high activity, high stability, immobilization

48


Fig. 18. Model for biohydrogen production in vitro. A) Complete device showing the position of photosystem complexes and suggesting electron carriers. B) Diagram showing water-splitting and electrons transfer through complexes and mediators required for H2 production. (Reprinted with permission from Ref. 168).

and appropriate orientation of PSI and PSII, and suitable artificial electron carriers (Fig. 18) [104,164–169]. In the way of producing biohydrogen by semi-artificial device, some success has been achieved of the following:

• PSI of Thermosynechococcus elongatus was purified in monomeric and trimeric active, photostable and thermostable forms [168]. • Immobilizing of PSI and PSII was developed to attain two redox hydrogels with − 396 mV and maximum power output of 1.91 ± 0.56 ␮W cm−2 [163,164,168,169]. • Construct PSI-Hydrogenase in photoactive, oxygen tolerant and stable form [159].

For this reason, the in vitro strategies of light-driven hydrogen production put the PSI in the priority. Enhancement the hydrogen production based on photosynthetic process should require an oxygen-tolerant and active hydrogenases. In addition to hydrogenases activity, under immobilization the close distance between hydrogenase and PSI should be required. Several attempts have been published that discuss the fusion between PSI and hydrogenase in vitro [158,169–175]. All strategies concerning the connection designs between PSI and hydrogenase are based on reduction of the distance between them, which lead to successful electrons pumping to hydrogenase active site [158,169–175]. These bindings may achieve through external native electron carrier (Fd) [158], one of stromal PSI subunits (PsaD, PsaE) or dithiol nanoparticles [170].

4.1. Construction of PSI and NiFe-Hydrogenases via PsaE Direct coupling of a hydrogenase to PSI is one important way to enhance the light-driven hydrogen production. This strategy has been constructed by Ihara et al. [170], who fused the PsaE subunit of PSI from Thermosynechococcus elongatus to the C-terminus of NiFehydrogenase from Ralstonia eutropha. This fusion was combined in vitro by mixing purified mutant PSI from Synechocystis sp. PCC 6803 PsaE and Hyd-PsaE [170]. The resulting PSI-hydrogenase hybrid complex was capable of light-driven hydrogen production using ascorbate as an artificial electron donor (Fig. 19) [170]. The hydrogen production rate was quite low and was not possible to be quantified due to the partial fusing of Hyd-PsaE with PsaE. To overcome this problem, Schwarze et al. developed a new purification strategy for the Hyd-PsaE fusion protein as well as PSI-PsaE [158]. This approach yielded the pure and active fusion protein, where this purification strategy allowed the efficient removal of contaminating premature MBH forms and yielded homogenous complexes. The Hyd-PsaE-PSI showed high hydrogen evolution activity that was comparable to the wild-type MBH protein purified from the membrane. PSI-His10-tag was attached to the N terminus of PsaF, which is exposed to the luminal side of thylakoid membranes. This strategy allowed an oriented immobilization of the PSI onto modified gold electrodes [158,167,168]. Also, purified PSI-wt and PSI-PsaE exhibited the same oxygen consumption activity of wild type PSI (700 ␮mol O2 /mg Chl/h) [158,170]. The 10-Histag-PSI enables oriented immobilization onto Ni-NTA-modified electrode surfaces, which allows the quantitative characterization of the structure, composition, and light-mediated hydrogen evolution activity of the respective protein monolayer by spectroelectrochemical methods [158].


49

Fig. 19. Models of the hydrogenase-PsaE-PSI complex. A) Membrane-bound hydrogenase of Ralstonia eutropha H16. B) Wild-type photosystem I of Synechocystis sp. PCC 6803. C) MBHstop protein lacking the C-terminal anchor of HoxK. D) MBHPsaE and PSI-PsaE. (Reprinted with permission from Ref. 158).

4.2. Wiring PSI through nanoconstruction The strategy of fusion is based on linking PSI with hydrogenase via short and effective linker. The protein−protein connections between PSI from thermophilic cyanobacterium Thermosynechococcus elongatus and high tolerant (FeFe)-hydrogenase from Clostridium pasteurianum are considered an effective complex capable of photocatalytic hydrogen [171,172]. This fusion of these active protein complexes occurred via dithiol linkers [171–173]. Lubner et al. have developed a biological organic nanoconstruct that directly binds the terminal [4Fe-4S] cluster within PSI from Synechococcus sp. PCC 7002, to the distal [4Fe-4S] cluster of the FeFe-hydrogenase from Clostridium acetobutylicum (Fig. 20) [171]. This construction saved an optimum electron transfer from PSI to hydrogenase where under enough illumination intensity; the PSI–½FeFe-H2 ase nanoconstruct evolves molecular hydrogen in a rate of 2,200 ± 460 ␮mol mg chlorophyll−1 h−1 , which is equivalent to 105 ± 22 e− PSI−1 s−1 [171]. Cyanobacteria can evolve oxygen in a rate of 400 ␮mol mg chlorophyll−1 h−1 , which is equivalent to 47 e− PSI−1 s−1 at a PSI to PSII ratio of 1.8 [171]. It is clear that greater than two fold electrons were obtained by the hybrid biological/organic nanoconstruct as compared to in vivo [171]. As linkers, several dithiol derivatives with various lengths (e.g., decanedithiol, octanedithiol and hexanedithiol) have been examined for fusing PSI and FeFe-Hydrogenase [172]. The crystal structures of PSI and FeFe-Hydrogenase confirmed the fusion and the stability of these constructions. Additionally, the protein mobility via root-mean-squared fluctuations (RMSFs) showed that tethering through the shortest hexanedithiol linker led to enhancement of the atomic fluctuations of both PSI and the hydrogenase in these fusion complexes [172]. On the other hand, evaluation of the internal electron-transfer distances in these complexes showed

structural changes in the FeFe hydrogenase arising from ligation to PSI via the shortest hexanedithiol linker that may hinder electron transport in the hydrogenase, which may explain why the mediumlength octanedithiol linker gives the highest hydrogen production rate [172]. The main observed problem of this construction was the unequal distance between PSI and hydrogenase, leaving a population of free PSI complexes. Since using dithiol linkers produces different distances between the coupling complexes, Applegate et al. developed and optimized PSI–Hydrogenase nanoconstruct, where they incubated Cyt c6 with octanedithiol, PSI and FeFehydrogenase [173]. They concluded that Cyt c6 enhanced the formation of PSIC13G–1,8-octanedithiol-[FeFe]-hydrogenaseC97G (PSI–hydrogenase) nanoconstruct (Fig. 21) [173]. Although the maximum quantum yield for the PSI–hydrogenase nanoconstruct by one photon absorbed is ½H2 , the practical applications showed that an average of 0.10–0.15 hydrogen molecules/photon are yielded by photoexcitation of the PSI–hydrogenase nanoconstruct with a visible light in the range of 400–700 nm [173]. A possible reason for this difference might be due to the presence of different conjugates such as (PSI–PSI) conjugates and Hyd–Hyd conjugates beside non-productive PSIC13G–1,8-octanedithiol–PSIC13G, which could absorb light without generating hydrogen [173]. 4.3. Immobilized PSI layer(s) on nanocrystalline semiconductors The biohybrid dye-sensitized solar cells (DSSC) have been fabricated via electronic coupling between a robust red algal PSI associated with its light harvesting antenna and nanocrystalline ntype semiconductors, TiO2 and hematite (␣-Fe2 O3 ) [174]. PSI-LHCI could be immobilized as structured multilayers over semiconductors nanocrystalline arrays, organized as highly ordered, as evidenced by FE-SEM and XRD spectroscopy. The observed results

50


Fig. 20. Schematic comparison of electron flow in A) in vivo photosynthesis and B) the photosynthetic nanoconstructs. (Reprinted with permission from Ref. 171).

showed that ␣-Fe2 O3 /PSI-LHCI biophotoanode operated at the highest quantum efficiency as well as generated the largest open circuit photocurrent compared to the tandem system based on TiO2 /PSI-LHCI material (Fig. 22) [174]. Immobilization of the PSI-LHCI complex was oriented to be the reducing side towards the hematite surface and nanostructuring of the PSI-LHCI multilayer in which the subsequent layers of this complex are organized in the head-to-tail orientation [174]. It could be concluded that the biohybrid PSI-LHCI-DSSC performed photoelectrochemical hydrogen production upon illumination with visible light above 590 nm. Although the solar energy conversion efficiency of the PSI-LHCI/hematite DSSC was below a practical use, the system could provide a blueprint for a genuinely green solar cell that can be used for H2 production at a rate of 744 ␮mol H2 mg Chl−1 h−1 , allowing this technique to work as one of the performing biohybrid solar-to-fuel nanodevices [174]. Through this system, the problem of long time stability of PSII was overcome, where the nanostructure semiconductors can feed back liberated electrons to the PSI complex [174].

4.4. Coating PSI with platinum An effective strategy for biohydrogen generation is covering a noble metal catalyst to the reducing side of PSI (stromal side). Gold and platinum are found to be suitable catalysts for hydrogen production. As a result of depositing protons to the metal surface, they combine with electrons generating hydrogen atoms, which combine with each other to produce hydrogen molecules. This activity is recognized in both bulk material and in nanoparticles made from these metals. For successful hydrogen production, the catalyst should be very close to the reducing side of PSI, where the time of electron transfer should not exceed 65 ms [175]. Colloidal Pt-nanoparticles have the ability to be deposited directly onto isolated PSI [176–180]. Illumination of either chloroplasts or isolated PSI in the presence of hexachloroplatinate ([PtCl6 ]2− leads to the reduction of Pt4+ ions, then it can be precipitated onto the protein surface (Fig. 23) [178,180]. This metal serves as an additional cofactor in the electron-transfer chain of PSI, which catalyzes the reduction of protons to H2 . Illumination of isolated PSI reaction centers in the presence of an artificial electron donor (sodium ascorbate) and the native electron donor of PSI, plastocyanine or cytochrome c6, results in production of 0.025 ␮mol H2 mg Chl−1 h−1 [180].

Enhancement the H2 production is connected with increasing the temperature that could be reached (5.5 ␮mol H2 mg Chl−1 h−1 ). The ability to produce H2 has been examined by using several nanoparticles derived from pentapyridine cobalt complex and hexachloroosmiate ([OsCl6 ]2− ) [181]. It could be concluded that the presented semi-artificial systems highlight the scientific progress in the terms of photocurrent and biohydrogen production via the combination between PSI (nature complex) with artificial cofactors. The lowest hydrogen production (5.5 ␮mol H2 /mg Chl/h) was obtained in case of depositing of Pt on the surface of PSI complex, while the highest hydrogen production (2200 ␮mol H2 /mg Chl/h) was recorded in case of using the nanoconstruction complex between PSI and hydrogenase. Since the rate of electron pumping by PSI is considered one the most limiting parameter affecting the rate of hydrogen production, several attempts have been done to enhance photocurrent production and electron flow. In general, a successful photocurrent production requires optimization of several factors especially that concerning electron donors, electron acceptors, electrode types, electrode surface area, electron capturing through mixing PSI with polymers-Os complex and immobilization on p-doped silicon surface layer. Promising results have been obtained in case of inducing the nanostructures (e.g., ZnO, TiO, Os). Table 1 summarizes the most common and producible results including the applicable, immobilized surfaces, different electrodes and different electron donors (mediators) [33,78,139,150,165,182–186].

5. Artificial photosynthesis As mentioned earlier, photosynthesis is one of the most effective solar energy conversion systems on earth, where the organisms harvest sunlight and convert it into useful electrochemical energy. In the marvelous artificial photosynthesis process, the antenna units harvest sunlight and the excitation energy is funneled to the reaction center where multistep electron-transfer reactions occur to generate potential that can drive chemical reactions to produce chemical energy that can be used and stored by the organism [20–55]. These steps are summarized in Fig. 24. In recent years, a great deal of progress has been made in the field of artificial photosynthesis by constructing chemical photosynthetic systems capable of fast energy- and electron-transfer reactions and slow charge recombination [20,22,24,32,36,38–41,187–199]. Some of this progress will be illustrated in this section with examples of the recent reported molecular photosynthetic systems


51

and have advantages of absorbing the light in a wide range of solar spectrum. In order to get clear evidences for occurrence the energy-transfer and electron-transfer reactions in these artificial photosynthetic systems and to determine their rates and efficiencies [20,22,24,32,36,38–41,200,201], the powerful laser flash photolysis techniques have been mainly utilized, in addition to other complementary techniques. 5.1. Covalently linked molecular systems

Fig. 21. Schematic of PSI–hydrogenase nanoconstruct, it shows the electrontransfer pathway in red color. Absorbed photons are transferred to PSI reaction center (P700) where the charge is separated and electrons are transferred to hydrogenase via the internal electron carriers of PSI. (Reprinted with permission from Ref. 173). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

(by covalent bonds) and supramolecular photosynthetic complexes (via non-covalent binding modes) from our laboratories and those of others. Such systems are composed mainly from organic materials (antenna, electron donor, electron acceptor) that are quite related to that in the natural photosynthetic processes

5.1.1. Porphyrin-based donor-acceptor molecular systems Porphyrins form a ubiquitous class of naturally occurring biomolecules. Because of their intense absorption in the visible region, extensively conjugated ␲-systems, long-lived singlet and triplet states, rich electrochemistry, high photo-stability, and good capability to mediate visible photon–electron conversion processes [200–205], the covalently linked systems based on porphyrins have been extensively investigated as artificial photosynthetic models. For constructing such efficient photosynthetic models, the electron-donating porphyrins were combined with various electron acceptors. Among them, one can find that fullerene C60 is the most frequently utilized as an electron acceptor because of its 3-dimensional ␲ system, multiple photoreduction process (accepting up to six electrons in electrochemical measurements), and small reorganization energy (which accelerates the charge-separation process and decelerate the charge-recombination process) [206–212]. From the simple schematic diagram of the artificial photosynthetic systems shown in Fig. 24, one can see that the photoinduced electron transfer is characteristic of the artificial reaction centers. The first published report in this field in 1994 by the Arizona State team headed by Gust, Moore, and Moore (hereafter designated GMM) concerned dyad 1 (Fig. 25) (MP-C60 ; where M = H2 and Zn) and established some of the important ground rules for this field [213]. Using the laser photolysis techniques, the photodynamic studies of H2 P-C60 in nonpolar toluene showed that; excitation of dyad 1a to give 1 H2 P*-C60 is followed by singlet–singlet energy transfer to give H2 P-1 C60 *, which in turn undergoes typically efficient intersystem crossing to populate H2 P-3 C60 *. The behavior of 1a in polar benzonitrile showed different features where the electron transfer takes place from the singlet state of H2 P to the electron • • accepting C60 yielding the charge-separated state H2 P + -C60 − . The corresponding dyad 1b in both toluene and benzonitrile undergoes only very rapid electron transfer (kCS = 1011 s−1 ) to give the

Fig. 22. Schematic diagram for fabrication of PSI/␣-Fe2 O3 /FTO electrode. Nanostructured mesoporous hematite was spread on FTO glass plate. At high acidic condition, pH 4, PSI multilayer was physisorbed onto the hematite film. A second multilayer of PSI in the head-to-tail orientation upon immobilization can establish by spreading additional coating of Agarose that provided an interface for chemical cross-linking with 1,1-carbonyldiimidazole (CDI) at pH 4. (Reprinted with permission from Ref. 174).

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Fig. 23. Deposit platinum metal catalysts evolving hydrogen. Electrons required for hydrogen production are driven from PSI under illumination. PSI-reaction center regains the liberated electron through either native electron carrier (plastocyanin [Pc] or cytochrome c6 [Cyt. c6]) or artificial electron carrier (ascorbate).

•

•

charge-separated state ZnP + -C60 − [213]. The differences in the photodynamics of dyads 1a and 1b were rationalized in terms of energies of the various intermediates, namely 1 MP*-C60 , MP-1 C60 *, • • MP-3 C60 *, and MP + -C60 − [213]. Similar results were reported by GMM and coworkers for dyad 2 (Fig. 26) [214]. Specifically, it was shown that for the free base dyad (2a) in toluene, charge separation is not observed from either 1 MP*-C 1 60 or MP- C60 *, while in benzonitrile photoinduced electron transfer competes with photoinduced energy transfer, just as with 1a. For the corresponding Zn dyad (2b), photoinduced electron transfer is seen in toluene as well as benzonitrile. The lifetime of the charge-separated state (␶CS ) was 290 ps in the case of 2a and 50 ps in the case of 2b [214], which is considerably slower than the rate of charge separation. According to molecular modeling studies, dyad 2 adopts a folded conformation in which Dcc , the distance from the center of the porphyrin moiety to the center of the C60 , is • • 9.9 Å [192]. The free energy changes for formation of H2 P + -C60 − •+ •− and ZnP - C60 were estimated at 0.58 and 0.37 eV, respectively [214]. Another examples of porphyrin-fullerene conjugates with flexible linkers have been shown in dyads 3(a,b), where fullerene C60 is covalently linked with zinc porphyrin and magnesium porphyrin to examine the effect of the central metal ion of the porphyrin cavity on the photoinduced electron charge separation and charge recombination in these dyads (Fig. 27) [215,216]. The molecular orbital (MO) and electrochemical studies showed the electron transfer from the electron-donating porphyrin to the electron-accepting • • fullerene forming the charge-separated states ZnP + -C60 − and •+ •− MgP -C60 for 3a and 3b, respectively. The time-resolved emission technique revealed efficient quenching of the singlet-excited state of ZnP and MgP. While the quenching pathway of the singlet ZnP moiety involved electron transfer to the attached C60 moiety with a rate constant of 2.2 × 109 s−1 [215], the quenching pathway of the singlet MgP shows different features where the energy transfer from the singlet MgP to C60 moiety, generating the singlet excited C60 , from which subsequent charge-separation occurred with a rate constant of 1.7 × 109 s−1 [216]. By utilizing the nanosecond transient absorption technique, the transient absorption band of the C60 radical anion in the near IR region (∼1000 nm) serving as diagnostic probe for the electron-transfer reactions, from which the rate constants of charge recombination (lifetimes of charge-separated state) were found to be 1.8 × 106 s−1 (560 ns) and 3.3 × 106 s−1 (300 ns) for 3a and 3b, respectively [215,216]. By borrowing a concept of the multistep electron transfer from natural photosynthesis, triad 4 (Fig. 28) composed of diarylporphyrin (H2 P), carotenoid polyene (C), and fullerene (C60 ) entities

Fig. 24. Schematic representation of an artificial photosynthetic system for water splitting (solar fuel production).

Fig. 25. Structure of MP-C60 dyad 1 (where M = H2 and Zn).

Fig. 26. Structure of MP-C60 dyad 2 (where M = H2 and Zn).

has been designed by Gust and coworkers aiming to slow down the rate of charge recombination, and consequently to increase the lifetime of the charge-separated state [217]. In this triad, the porphyrin unit acts as the primary electron or energy donor, the carotene unit acts as a secondary electron donor, while the fullerene unit as an electron acceptor. In 2-methyltetrahydrofuran, the singlet-excited state of porphyrin in 4 decays by photoinduced electron transfer to • fullerene to give an intermediate charge-separated state (C H2 P + -


53

Table 1 Different photocurrent production by PSI complex extracted from different organisms. Different parameters have been applied (e.g. immobilized surface electrodes, electron donors, electron acceptor, light intensity and different wavelengths). Produced photocurrents are expressed as (␮A/cm) and current density (␮A/cm/mW). Applicable electron donors and immobilized materials were sodium ascorbate (NaAs), 2,6-dichlorophenolindophenol (DCIP/DCPIP), reduced ferricyanide [K4 Fe(CN)6 ], osmium[Os(bpy)2 Cl2 ]/Ospolymer, Z813 electrolytes, and ruthenium hexamine (RuHex). Methyl viologen (MV) was used as an electron acceptor. Photocurrent (␮A/cm)

Current density (␮A/cm/mW)

PSI Source

Immobilization surface electrode

Electron donor

Electron acceptor

Incident light intensity and wavelength

Ref.

1.6 0.9 120 875 29 362

0.48 0.5 3 4.6 16.1 4469.1

Thermosynechococcus elongatus Thermosynechococcus elongatus Synechocystis 6803 Spinach Thermosynechococcus elongatus Thermosynechococcus elongatus

Au nanoparticles/SAM/MPS/PSI MPS-SAM Au-PSI-Pt-PSI-Pt-PSI PSI films/p-doped silicon Os complex modified polymer TiO/ZnO-PsaD/E-PSI

NaAs/DCIP DCIP NaAs/DCIP – Os complexes –

– MV – MV MV –

3.3 mW/cm2 –680 nm 1.8 mW/cm2 –680 nm 40 mW/cm2 760 nm 190 mW/cm2 –633 nm 1.8 mW/cm2 –680 nm 0.081 mW/cm2 – sun light

[153,182] [165] [150,183] [139,184] [78,185] [33,186]

Fig. 27. Structure of MP-C60 dyad 3 (where M = Zn and Mg), and the proposed modulation of photoinduced electron transfer processes. •

C60 − ), followed by hole transfer from porphyrin to carotenoid to • give the final charge-separated state (C + -H2 P-C60 • −) with a quantum yield of 0.14 [217]. Based on the rates of charge-recombination processes, the lifetimes of charge-separated states were determined to be 170 ns (in solution) and 1.5 ␮s (in a glass matrix at 77 K). Although the triad 4 was regarded as a mimic of several aspects of photosynthetic electron transfer, the quantum yield of long• lived charge-separated state (C + -H2 P-C60 • −) was much lower than unity observed in the natural photosynthetic reaction center [217]. By using the same concept of the multistep electron transfer, Sakata et al. reported the photodynamics of zinc porphyrin-free base porphyrin- fullerene triad 5 (Fig. 29) [218]. By exciting the zinc porphyrin entity, as an energy-transferring antenna, an energy transfer from the first-excited state of zinc porphyrin (ZnP) to the energetically low-lying free base porphyrin (H2 P) was observed in polar benzonitrile. This energy transfer was followed by a sequential electron transfer to yield the final charge-separated • state (ZnP + -H2 P-C60 • −) with a quantum yield of ∼0.4 and a lifetime of 21 ␮s [218]. Based on molecule 5, the authors extended this idea by adding ferrocene (Fc) unit, as third electron donor, to construct tetrad 6 (Fc-ZnP-H2 P-C60 ) (Fig. 29) [219]. The photodynamic studies confirmed the following intramolecular events: (i) energy transfer from the singlet excited zinc porphyrin (1 ZnP*) to the linked free base porphyrin, (ii) electron transfer from the sin-

glet excited free base porphyrin (1 H2 P*) to fullerene generating • • the initial charge-separated state (Fc-ZnP-H2 P + -C60 − ), (iii) hole •+ migration from H2 P to ZnP yielding the intermediate charge• • separated state (Fc-ZnP + -H2 P-C60 − ), (iii) hole migration from •+ ZnP to Fc yielding an extremely long-lived charge-separated state • (Fc+ -ZnP-H2 P-C60 − ) with a lifetime of 380 ␮s in frozen benzonitrile [219]. Such extremely long-lived charge-separated state is comparable to that observed for the bacterial photosynthetic reaction center [219]. Pentad 7 has been designed by GMM aiming to slow down the rate of charge recombination by the concepts of multistep electron transfer and charge delocalization over the zinc porphyrin entities (Fig. 30) [220]. As seen, pentad 7 composed free base porphyrin (H2 P), fullerene (C60 ), in addition to three units of zinc porphyrin (ZnP). The photodynamic studies of 7 in 2-methyltetrahydrofuran showed the electron transfer from the singlet-excited state of H2 P to the covalently linked C60 , generating the charge-separated state • • (ZnP)3 H2 P + -C60 − with a time constant of 25 ps and a quantum • • yield 98% [220]. Prior to recombination of (ZnP)3 H2 P + -C60 − , the positive charge migrates from H2 P to the ZnP entities yielding the • • final charge-separated state (ZnP)3 + -H2 P-C60 − with a time constant of 380 ps [220]. The greater separation of charges in the final • • charge-separated state (ZnP)3 + -H2 P-C60 − increases the lifetime to 240 ns [220], which is nearly 100 times longer compared to the • initial electron transfer product (ZnP)3 H2 P + -C60 • −. To construct a simple working model of the antenna-reaction center complex, Fukuzumi et al. reported pentad 8 (Fig. 31) [189,221]. As seen, pentad 8 is composed of three boron dipyrromethene (BODIPY) units (as antennae), zinc porphyrin (as an energy acceptor as well as an electron donor), and C60 (as an electron acceptor) [189,221]. The optical absorption of 8 has advantage of absorbing the light over a broad range in the visible region (300–700 nm). Because of the spectral overlap between the BODIPY emission and ZnP absorption, the energy transfer was observed from the singlet-excited state of BODIPY (2.42 eV) to populate the singlet ZnP (2.08 eV) with a considerably large rate constant of 2.7 × 1010 s−1 [221]. This process is followed by the electron transfer from the formed singlet ZnP to the covalently • • linked C60 yielding the (BODIPY)3 -ZnP + -C60 − with a rate con-

Fig. 28. Structure of carotenoid polyene (C)-diarylporphyrin (H2 P)-fullerene (C60 ) dyad 4.

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Fig. 29. Structure of ZnP-H2 P-C60 triad (5) and Fc-ZnP-H2 P-C60 tetrad (6).

Fig. 30. Structure of (ZnP)4

H2 P-C60 7 and the proposed modulation of photoinduced electron transfer processes.

stant of 1.7 × 1011 s−1 [221]. Based on the rate constant of charge recombination (1.0 × 109 s−1 ), the lifetime of charge-separated • • state (BODIPY)3 -ZnP + -C60 – was found to be 1 ns [221]. Surprisingly, the nanosecond transient absorption measurements revealed

the formation of the triplet character of the charge-separated state • • (BODIPY)3 -ZnP + -C60 − via the triplet-excited state of ZnP with a quantum yield of 0.27 and a lifetime of 385 ns [221], which is 385 times longer as compared to that via the singlet excited ZnP.


55

Fig. 31. Structure of (BODIPY)3 -ZnP-C60 pentad 8 and the proposed modulation of photoinduced energy and electron transfer processes.

Fig. 32. Structures of Fc-ZnP(TPA)2

C60 (9) and ZnP(TPA)3

C60 (10), and the proposed modulation of photoinduced energy and electron transfer processes.

Fig. 33. Molecular structure of subphthalocyanine (SubPc) 11, and its characteristic absorption and emission spectra in the visible region.

Another example of antenna-reaction center with multistep electron transfer is shown in molecule 9 (Fig. 32) [222], which composed of two entities of triphenylamine (as antennae and electron donors), and porphyrin moiety (as energy acceptor and electron donor), and C60 (as well-known electron acceptor). The electrochemical measurements showed that the first oxidation potential of ZnP(TPA)2 was cathodically shifted over 100 mV as compared to unsubstituted ZnP because of the delocalization of porphyrin ␲-system to the closely linked triphenylamine entities. Upon shining the polyad 9 with UV light, the singlet–singlet energy transfer was clearly observed from the triphenylamine units to populate the singlet-excited state of zinc porphyrin, from which the electron transfer takes place to the covalently linked C60 [222]. The resulting • • transient (Fc-ZnP(TPA)2 + -C60 − ) state undergoes hole migration from ZnP entity to Fc generating the final charge-separated state

•

•

(Fc-ZnP(TPA)2 + -C60 − ) with a lifetime of 8.5 ␮s [222], which is much longer than that of its reference ZnP(TPA)3 C60 10 (1.2 ␮s) [223].

5.1.2. Subphthalocyanines based light harvesting complexes The basic structure of subphthalocyanine (SubPc) 11 shown in Fig. 33, consists of three N-fused diiminoisoindoline units arranged around a central boron atom and ␲-electron aromatic core associated with their curved structures, which make it different from their higher homologues, phthalocyanines [224–232]. In recent years there is a considerable interest in utilizing subphthalocyanines in constructing novel donor-acceptor photosynthetic systems [233–239] because of their strong absorption in the visible region, high fluorescence quantum yields, ability to tune their optoelectronic features by varying axial ligands and by function-

56


Fig. 34. Structure of SubPc-diazobenzene-C60 (12), and the proposed modulation of photoinduced energy transfer processes. (Adapted from Ref. 240).

Fig. 35. Structure of SubPc-TPA-ZnP (13), and the proposed modulation of photoinduced energy and electron transfer processes.

alizing the various peripheral positions, and low reorganization energy [233–239]. Taking these unique properties in concert, the ability of subphthalocyanine to act as antenna unit in the artificial photosynthetic system was examined by constructing molecule 12 (Fig. 34), where the subphthalocyanine unit is linked with fullerene through diazobenzene linkage [240]. The time-resolved emission technique showed an efficient energy transfer from the singlet-excited state of subphthalocyanine to the low-lying singlet C60 with a quantum yield of 97% and a rate constant of 1.3 × 1010 s−1 [240]. The formed singlet C60 decayed to the triplet state of fullerene C60 as confirmed by nanosecond transient absorption technique. Similar behavior of subphthalocyanine was observed in the covalently linked subphthalocyanine-triphenylamine-zinc porphyrin triad 13 (Fig. 35), where subphthalocyanine acts as an energy transferring moiety to covalently linked ZnP because of the good overlap between the subphthalocyanine emission and porphyrin absorption [241]. The optical emission studies of 13 in toluene showed a clear evidence of the fast energy transfer from the singlet-excited state of SubPc (2.16 eV) to zinc porphyrin (2.06 eV) by recording the quenching of the singlet subphthalocyanine accompanied with formation of the singlet state of zinc porphyrin, which in turn, donate its electron to the electron-accepting subphthalocyanine entity with a rate of 8.9 × 1010 s−1 generating the • charge-separated state (SubPc•–−-TPA-ZnP + ) [241]. The rate constant of charge recombination and lifetime of charge-separated state in toluene were determined to be 8.9 × 1010 s−1 and 140 ps, respectively [241]. The ability of subphthalocyanine to act as an electron acceptor was seen in molecule 14 (Fig. 36), where subphthalocyanine is covalently attached with ferrocene through the axial position of the macrocycle [242]. To increase its electron-accepting

properties, subphthalocyanine unit was substituted with electronwithdrawing fluorine (a), nitro (b) and alkylsulfonyl groups (c). In all cases, efficient electron transfer was clearly recorded from ferrocene to the singlet-excited state of SubPc. Interestingly, the laser flash photolysis studies in polar benzonitrile showed an • extremely long-lived Fc+ -SubPc − for 14a (43 ␮s), 14b (61 ␮s), and 14c (231 ␮s) [242]. The authors rationalized this great stabilization of this simple charge-separated state Fc+ -SubPc• − by the donoracceptor topology and the particular characteristics of the axial polar bond, which increases its length and ionic character upon SubPc reduction [242]. In a similar fashion, the electron-accepting character of subphthalocyanine has been examined by linking it with the electron-donating triphenylamine through axial ligand approach 15 (Fig. 37) [243]. The photodynamic studies of 15 showed electron transfer from triphenylamine to the singlet excited SubPc, gener• ating the charge-separated state SubPc − -TPA•+ . To achieve charge stabilization via multistep electron-transfer reactions, the triphenylamine unit was substituted with one and two units of fullerene C60 forming SubPc-TPA-C60 (molecule 16) and SubPc-TPA-(C60 )2 (molecule 17), as donor-acceptor1-acceptor2 model [243]. The computational and electrochemical studies of 16 and 17 predicted • • the formation of SubPc-TPA + -C60 − as a stable charge-separated state. Fast charge-separation processes via the singlet-excited SubPc were observed with the rate constants of ∼1010 s−1 [243]. Compared with SubPc-TPA dyad, a long-lived charge-separated sate was observed for 16 with the lifetime of 670 ns in benzonitrile. Interestingly, further charge stabilization was achieved in 17, in which the lifetime was found to be 1050 ns [243] that was • rationalized by the electron shift from SubPc − to C60 , and charge delocalization over the two fullerene units. Recently, El-Khouly et al. reported the electron-accepting and electron-donating properties of subphthalocyanine by linking it with ferrocenophane (18), and naphthalenediimide (19) (Fig. 38) [244]. Upon photoexcitation of SubPc, the electron-transfer behavior of 18 was recorded from ferrocenophane to the singlet excited SubPc, generating charge-separated state SubPc• −–Fc+ with a rate constant of 8.2 × 1010 s−1 as observed from the femtosecond transient absorption technique [244]. On the other hand, the photochemical events of molecule 19 showed quite different features. The femtosecond transient absorption studies revealed an electron transfer from the singlet-excited state of SubPc to NDI of 19 with a rate constant of ∼1012 s−1 [244]. From the kinetic studies, the rate constant of charge recombination and the lifetime of charge• • separated state (SubPc + –NDI − ) were found to be 2.9 × 109 s−1 and 345 ps, respectively [244]. To mimic the behavior of the reaction center, a multimodular system 20 (Fig. 39)was constructed by linking the zinc porphyrin-(triphenylamine)3 entities with the dodecafluorosubphthalocyanine SubPc(F)12 at its axial position with B-O bond [245]. Compared with the zinc porphyrin, the electrochemical measurements and MO calculations showed a higher donor ability of ZnP(TPA)3 because of the electronic interaction between the TPA entities and ZnP -system. Based on the first oxidation potential of ZnP(TPA)3 (256 mV vs Ag/AgNO3 ) and the first reduction potential of SubPc(F)12 (−930 mV vs Ag/AgNO3 ), the driving forces for the charge separation via the singlet and triplet zinc porphyrin were found to be −0.84 and −0.40 eV, suggesting an exothermic charge separation processes via both states [245]. A fast electron transfer from the singlet excited ZnP(TPA)3 to the axially linked SubPc(F)12 was observed by detecting the transient absorption bands of the radical ion-pair species • • (ZnP(TPA)3 + and SubPc(F)12 − ) in the picosecond time scale in both polar benzonitrile (kCS = 1.0 × 1012 s−1 ) and non-polar toluene (kCS = 9.0 × 1011 s−1 ). Since the kCS values are almost independent from solvent polarities, it is suggested that the charge-separation


57

Fig. 36. Structure of subphthalocyanine-Fc conjugates (14), along with the lifetimes of charge-separated states.

Fig. 37. Structures of SubPc-TPA dyad (15), SubPc-TPA-C60 triad (16), and SubPc-TPA-(C60 )2 (17), and the proposed modulation of photoinduced energy and electron transfer processes.

process occurred near the top region of the Marcus parabola [246]. The kCR and ␶CS were found to be 5.9 × 109 s−1 and 170 ps (in toluene), and 5.0 × 1010 s−1 and 20 ps (in benzonitrile). Such fast charge-recombination processes suggest that the radical-ion pair keeps the singlet-spin character. The observation that the kCR values increase with the increasing the solvent polarity (i.e., the lifetime of the charge-separated state is longer in nonpolar solvents compared to that in polar solvents) can be understood, if charge recombination is occurring in the Marcus inverted region [246]. Indeed, compared with the reorganization energy ranging 0.5–1.0 eV estimated above, the driving forces for charge recombination in toluene (GCR = −1.41 eV) are sufficiently large, whereas

the GCR value in benzonitrile (−1.16 eV) is closer to the reorganization energy. Interestingly, the nanosecond transient absorption spectra in polar benzonitrile showed the formation of long-lived • • charge-separated state (ZnP(TPA)3 + –SubPc(F)12 − ) with a lifetime of 370 ␮s and a quantum yield of 0.29 [245]. Such long-lived CS state was rationalized by the delocalization of the positive charge over the ZnP(TPA)3 entities, the particular characteristics of the axial B O bond, and the triplet character of the generated radical-ion pair [245]. Such an unusually large ratio of charge separation rate to charge recombination rate is highly desired for converting the solar energy into chemical energy, as plants do.

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Fig. 38. (Left) Structure of SubPc-Fc (18) and SubPc-NDI (19), and the proposed modulation of photoinduced electron transfer processes. (Right) Femtosecond transient absorption spectra observed by 390 nm laser irradiation of dyad 19 in N2 -saturated benzonitrile. Inset: Absorption time profile of the singlet excited state of SubPc at 597 nm.

Fig. 39. (Left) Structure of SubPc(F)12 -ZnP(TPA)3 (20), and the proposed modulation of photoinduced electron transfer processes. (Right) Nanosecond transient absorption spectra observed by 430 nm laser irradiation of SubPc(F)12 -ZnP(TPA)3 in N2 -saturated benzonitrile. Inset: Absorption time profile of the ZnP(TPA)3 radical cation at 660 nm.

5.1.3. BODIPY-based light harvesting systems Since the first reports related with BF2 -chelated dipyrromethene compounds (abbreviated as BODIPY) [247–250], these dyes have attracted great attention in the recent years as promising materials for constructing efficient artificial photosynthetic models [189]. As seen from Fig. 40, the basic structure of BODIPY (21) consists of two pyrrole rings linked by methene and BF2 groups. The major absorption of BODIPYs is observed in the visible region (∼500 nm) corresponds to (S0 → S1 transition) with high molar absorption coefficient (␧ ∼ 105 M−1 cm−1 ) [251–262]. In addition, the BODIPYs are highly fluorescent materials with a maximum emission around 520 nm [251–262]. One of the interesting features of BODIPYs is the red shift of absorption and emission maxima by increasing substituents at the pyrrole carbons of the BODIPY [263]. By replacing the 8-position carbon atom of BODIPY by a nitrogen atom, BF2 -chelated tetraarylazadipyrromethanes (azaBODIPY) macrocycle 21 was synthesized and examined as photoactive species in the artificial photosynthetic systems (Fig. 40) [189,264–275]. This small modification of the azaBODIPY ring results in: (i) a red shift of both the absorption and emission maxima for about 100 nm, (ii) lower the energy of the singlet state of

azaBODIPY for about 500 mV compared to that of BODIPY, (iii) a negative shift of the first reduction potential as compared to that of BODIPY [240–251]. All these novel features shown in Fig. 40 render BODIPYs and azaBODIPYs as promising materials for constructing artificial photosynthetic systems. Because of the similarity of their structures, the combination between BODIPY and the covalently linked porphyrin unit(s) has received a great attention in the recent years as building blocks for efficient light harvesting systems. An example is shown in dyad 22 (Fig. 41), where BODIPY has been linked to antimony tetraphenylporphyrin (SbTPP) via an alkyl chain [276]. The strong absorption band of the BODIPY entity (at 500 nm) is located in the unabsorbed region of porphyrins between the Soret (420 nm) and Q-bands (530–600 nm), indicating that dyad 22 absorb light over a wide range of the visible region. Fluorescence measurements showed the energy transfer from the singlet excited BODIPY (energy of 1 BODIPY* = ∼2.4 eV) to the attached porphyrin (∼2.1 eV) with quantum yields of 13–40% [276]. The efficiency of energy transfer decreased with increasing the length of the alkyl chain spacer unit. By exciting the porphyrin unit, the energy transfer from the singlet-excited state of porphyrin to BODIPY was excluded because of unfavorable energetics [276].


59

Fig. 40. Molecular structures of BODIPY and azaBODIPY (21), in addition to their absorption, fluorescence, and electrochemical spectra in benzonitrile.

Fig. 42. Structure of ZnPc-(BODIPY)4 (23), and the proposed modulation of photoinduced energy transfer processes.

Fig. 41. Structure of SbP-(BODIPY)2 (22), and the proposed modulation of photoinduced energy transfer processes.

An efficient energy transfer was also observed when zinc phthalocyanine (ZnPc) is covalently linked with four BODIPY units to afford ZnPc-(BODIPY)4 pentad 23 (Fig. 42) [277]. The absorption studies of 23 cover most of the visible and NIR region (ca. 300–750 nm), which render it as a promising model for capturing solar spectrum. Because of the good spectral overlap of the BODIPY emission and ZnPc absorption spectra, an efficient energy trans-

fer from the singlet-excited state of BODIPY to ZnPc was clearly recorded from the femtosecond laser flash photolysis measurements in tetrahydrofuran with the rate constant of 5.9 × 1010 s−1 [277]. These findings indicate the useful potential of the examined ZnPc-BODIPY pentad to be efficient photosynthetic antenna in the artificial photosynthetic systems. A similar example was reported for molecule 24 (Fig. 43), which is composed of four BODIPYS units (as energy donors) attached to a central perylenediimide (PDI) unit (as energy acceptors) [278]. As seen, both entities are linked though the highly flexible arms, which favors attainment of multiple conformations of molecule 24 [278]. An even more complex light-harvesting system was reported for molecule 25 (Fig. 44) [279], which exhibits many energy transfer steps, according to which chromophore absorbs the excitation light of the solar spectrum. As seen, there are a total of 21 chromophoric units accreted into a single unit, including three disparate BODIPY-based dyes. At low light densities, a wide spectral range is harvested by the array where the overall probability of absorbed photons reaching the terminal BODIPY dye is greater than 75%.

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Fig. 43. Structure of PDI-(BODIPY)4 (24).

At high photon intensities, excitons are shuttled across the array via through-space interactions [279], which delay the arrival of an absorbed photon at the terminal BODIPY. Recently, azaBODIPY (a structural analogue of BODIPY) has also attracted a considerable attention as a promising energy/electron acceptor unit in constructing novel photosynthetic systems. Based on such great difference between BODIPY and its analogue azaBODIPY, dyad 26 and triad 27 have been constructed by linking azaBODIPY with one and two units from BODIPY, respectively (Fig. 45) [280]. The photochemical studies showed that the two systems absorb the light in the wide range of the solar spectrum with intense absorption bands for BODIPY and azaBODIPY at 503 and 670 nm, respectively. Because of the good spectral overlap of the BODIPY emission and azaBODIPY absorption, an efficient energy transfer from the singlet-excited state of BODIPY to azaBODIPY was suggested. Such behavior was confirmed by exciting the BODIPY unit in the less polar toluene and polar benzonitrile, where the emission from 1 BODIPY* at 517 nm was heavily quenched, accompanied by the appearance of the emission band of the singlet azaBODIPY at 674 nm. The rate constant of the singlet–singlet energy transfer was found to be 1.1 × 1011 s−1 in both solvents [280]. While the formed 1 azaBODIPY* in toluene decayed to the ground state, it was found that the 1 azaBODIPY* accepts an electron from BODIPY yielding the charge-separated • • state (BODIPY + -azaBODIPY − ) with a rate constant of 1.4 × 109 s−1 [280]. These examples demonstrate utilization of a near-IR emitting sensitizer, azaBODIPY, as a suitable candidate to build new light harvesting photosynthetic donor-acceptor models. As an extension to the triad 27, zinc porphyrin was connected with one of the two BODIPY units to construct BODIPY-azaBODIPYzinc porphyrin triad 28 as antenna-reaction center complex (Fig. 46) [281]. Triad 28 exhibited a broadband capturing and emitting light (300–800 nm) that is quite useful for solar energy harvesting systems [281]. The femtosecond transient absorption studies confirmed the occurrence of the efficient energy transfer from the singlet-excited state of BODIPY to populate the singlet azaBODIPY, which in turn accepts one electron from ZnP yield• • ing the charge-separated state (BODIPY-azaBODIPY − -ZnP + ) with

Fig. 44. Structure of light harvesting EXBODIPY-(TMBODIPY)2 -(TMBODIPY)4 -(pyrene)8 (25).


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Fig. 45. (Left) Structure of azaBODIPY-BODIPY dyad (26) and azaBODIPY-(BODIPY)2 triad (27), and the proposed modulation of photoinduced energy and electron transfer processes. (Right) Femtosecond transient absorption spectra observed by 390 nm laser irradiation of 26 in N2 -saturated benzonitrile. Inset: Absorption time profile of the singlet states of BODIPY (at 580 nm) and azaBODIPY (at 690 nm). •

Fig. 46. Structure of BODIPY-azaBODIPY-ZnP triad (28), and the proposed modulation of photoinduced energy and electron transfer processes.

a lifetime of 1.3 ns [281]. Upon excitation of the ZnP at 420 nm, an energy transfer from the singlet-excited state of ZnP to azaBODIPY occurs to produce 1 azaBODIPY*, followed by electron transfer from ZnP to 1 azaBODIPY* generating the charge-separated state • (BODIPY-azaBODIPY − -ZnP•+ ). Furthermore, triad 28 has advantage to absorb the light in the NIR region by the azaBODIPY unit to populate its singlet-excited state, which then accepts an electron from ZnP to form the charge-separated state (BODIPY• azaBODIPY − -ZnP•+ ) [281]. In a similar fashion, a light harvesting photosynthetic antennareaction center model 29 (Fig. 47) has been designed and characterized [282] by covalently linking the near-infraredabsorbing azaBODIPY with monostyryl BODIPY and fullerene (C60 ). In the resulting BODIPY-azaBODIPY-C60 triad 29, the monostyryl BODIPY acts as antennae, azaBODIPY acts as electron donor, and C60 acts as electron acceptor. From molecules 28 and 29, one can see that azaBODIPY can utilize as an electron acceptor and donor, respectively. Upon excitation, the emission of 1 BODIPY* was heavily quenched by energy transfer to the azaBODIPY core, which in turn transfers an electron to the fullerene • • unit generating (BODIPY-azaBODIPY + -C60 − ). The rate constant of energy transfer was determined to be ∼1011 s−1 by monitoring the rise of azaBODIPY emission [282]. In addition, a fast chargeseparation process from 1 azaBODIPY* to C60 has been detected, which afforded the relatively long-lived charge-separated state

•

(BODIPY-azaBODIPY + -C60 − ) with a lifetime of 1.47 ns [282]. These findings show that the light harvesting BODIPY-azaBODIPY-C60 triad 29 is an interesting artificial model that can mimic the antenna and reaction center of the natural photosynthetic systems. In contrast to 22 and 23 where the energy transfer occurs from the singlet excited BODIPY to the attached porphyrin unit, the fluorescent blue BODIPY-porphyrin tweezers linked by triazole rings (30) showed different features (Fig. 48) [283]. In 30, two styryl groups are introduced at the 3- and 5- positions of the BODIPY core [283] yielding the light harvesting distyryl BODIPY, which absorb and emit the light at longer wavelengths (ca. 650 nm) than porphyrin [165,260]. Thus, distyryl BODIPY acts as an energy acceptor when combined with porphyrin. Upon photoexcitation of ZnP, an efficient energy transfer occurred from the singlet excited ZnP to the linked distyryl BODIPY to populate the singlet distyryl BODIPY with a rate constant of 1.3 × 1011 s−1 [283]. The efficiency of energy transfer from the singlet-excited ZnP to distyryl BODIPY was much changed by the conformation change due to coordination of the nitrogen atoms of triazole rings to the zinc atom of porphyrin entity at low temperature. When changing the solvent from toluene to polar benzonitrile, photoinduced electron transfer from the ZnP unit to the singlet-excited state of BODIPY occurred to • • generate the charge-separated state (distyryl BODIPY − –(ZnP)2 + ) [283]. This model provides a new strategy for the design toward photo-switching devices, which can be controlled by the conformation change depending on temperature and type of solvents. 5.2. Supramolecular artificial photosynthetic systems Although covalent donor-acceptor systems exhibited excellent ground and excited state properties with appreciable lifetimes of the charge-separated states, they substantially differ from natural systems, especially in the mode of binding between donor and acceptor units where the photo- and redox-active components in the bacterial photosynthetic reaction centers are arranged via non-covalent interactions into a protein matrix [284]. In principle, non-covalent bonds, such as hydrogen bond, anion binding, crown ether-ammonium cation binding, metal-ligand coordination, electrostatic interactions and ␲-␲ stacking, guarantee the control over modulating the composition and thus provide the opportunity to achieve well-defined and rigid structures with high directionality and selectivity [189,193,285–288]. Thus, exploration of non-covalently linked electron donor-acceptor systems appears to be more promising to construct mimics for natural photosynthetic systems [189,193,284,288]. In recent years, several non-covalently supramolecular systems were designed and syn-

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Fig. 47. (Left) Structure of BODIPY-azaBODIPY-C60 triad (29), and the proposed modulation of photoinduced energy and electron transfer processes. (Right) Femtosecond transient absorption spectra observed by 390 nm laser irradiation of 29 in N2 -saturated benzonitrile. Inset: Absorption time profile of the C60 radical anion at 1000 nm.

Fig. 48. (Left) Structure of distyryl BODIPY–(porphyrin)2 tweezers (30). (Right) Femtosecond transient absorption spectra observed by 390 nm laser irradiation of 30 in N2 -saturated benzonitrile. Inset: Absorption time profiles of the singlet states of ZnP (at 460 nm) and distyryl BODIPY (670 nm). (Lower) Energy-level diagram showing the different photochemical events of 30.

thesized employing different modes of binding to copy functions of biological systems, and to understand the basic concepts of photoinduced energy-transfer and electron-transfer reactions in the antenna-reaction centers [284,288]. In this section, we will focus

mainly on the designed supramolecular systems formed by the axial ligation via a nitrogen-based ligand to the metal center of the porphyrins/naphthalocyanines, anion binding, and crown etherammonium cation interactions. Such complexes have advantage of ease of construction compared with the covalent systems.


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Fig. 50. Supramolecular Fc-ZnP:ImC60 triad (33), and the proposed modulation of photoinduced electron transfer processes.

Fig. 49. Supramolecular dyads 31 and 32 featuring ZnP axially coordinated with C60 py and C60 Im, respectively.

5.2.1. Metal-ligand interactions of porphyrins/naphthalocyanines with electron acceptors 5.2.1.1. Porphyrins-based supramolecular systems. Porphyrins have highly tunable photochemical and electrochemical activity as well as the potential for forming complexes [200–205]. For this, a number of studies have been reported regarding porphyrins with covalently linked axial ligands as model compounds to understand the mechanisms of various biological redox reactions [189,284,288]. Various spectroscopic studies have revealed the existence of stable five coordinate metalloporphyrins, thus mimicking the active sites of various heme proteins in which axial ligands are provided to the heme by side chains of the protein entity. This concept of penta-coordination of porphyrins has been extended in designing novel artificial photosynthetic systems [189,193,284,288]. D‘Souza et al. reported supramolecular dyads 31 and 32 by coordinating to zinc porphyrin with C60 -pyridine and C60 -imidazole, respectively (Fig. 49) [289]. In these complexes, the reversible coordination of a pyridine or imidazole appended fullerene ligand to the square planar zinc center of the porphyrin constituents a labile but measureable binding motif. As seen from the steady-state absorption studies, increasing additions of fullerene derivatives resulted in appreciable bathochromic and hypochromic shifts in the Soret band and visible bands [289]. Efficient quenching of the singlet excited porphyrin emission was also observed from the steadystate fluorescence measurements. These measurements reveal the complex formation with binding constants of 7.0 × 103 M−1 and 1.1 × 104 M−1 in case of C60 -pyridine and C60 -imidazole, respectively [289]. The higher binding constant of 32 is consistent well with the higher basicity of imidazole ring. From the time resolved fluorescence studies, the rate constants of charge-separation processes from the singlet-excited state of ZnP to C60 py and C60 Im were found to 107 and 1010 s−1 , respectively [289]. This work has been extended by linking imidazole C60 (C60 Im) with the covalently linked porphyrin-ferrocene dyad for gen-

erating C60 Im:ZnP-Fc triad 33 (Fig. 50) [290]. Upon forming the supramolecular triad by axial coordination C60 Im:ZnP-Fc, electron transfer takes place from 1 ZnP* to C60 generating • charge-separated state Fc-ZnP + -C60 • −with a rate of 2.8 × 1010 s−1 , • followed by hole migration from ZnP + to Fc, generating the + final charge-separated state (Fc -ZnP-C60 •– ) with relatively slow rate of charge recombination (1.2 × 108 s−1 ) [290]. Because of the multistep electron-transfer mechanism, the ratio of chargeseparation/charge-recombination was found to be ∼100, which indicates the charge stabilization in 33 [290]. Inspired by the importance and ease of axial ligation in forming donor-acceptor dyads, D’souza and co-workers attempted a new approach of probing proximity effects in porphyrin-fullerene dyad (34) by using an axial ligand coordination, which is controlled by “tail-on” and “tail-off” binding mechanism [291]. In the reported porphyrin-fullerene dyad 34 (Fig. 51), the donor-acceptor proximity is controlled either by temperature variation or by an axial ligand replacement method. The steady-state fluorescence and time-resolved emission studies showed that the efficiency of charge-separation of “tail-off” form changes to some extent in comparison with the results obtained for the “tail-on” form, implying the existence of some through-space interactions between C60 and zinc porphyrin in the “tail-off” form [291]. Nanosecond transient absorption studies of 34 showed clear evidence for occurrence of the electron transfer from the singlet-excited state of porphyrin to C60 generating the charge-separated state with a lifetime of 1000 ns [291]. Like zinc porphyrin, magnesium tetraphenylporphyrin (MgTPP) was also utilized in constructing self-assembled donor-acceptor systems by coordinating with fulleropyrrolidine appended with an imidazole coordinating ligand (C60 Im) [292]. Spectroscopic studies revealed the formation of 1:1C60 Im:MgTPP supramolecular complex (35) (Fig. 52) with the formation constant of 1.5 × 104 M−1 , suggesting fairly stable complex formation [292]. The computational and electrochemical studies suggested the formation of the charge-separated state (C60 Im− :MgTPP+ ). In non-coordinating dichlorobenzene, upon coordination of C60 Im to MgTPP, the main quenching pathway involved electron transfer from 1 MgTPP* to the C60 Im moiety. From the picosecond time-resolved emission studies, the rate constant and quantum yield of the charge-separation process were found to be 1.1 × 1010 s−1 and 0.99, respectively, indicating fast and efficient charge separation [292]. The nanosecond laser photolysis showed a clear evidence of the electron transfer from porphyrin to C60 Im by recording the characteristic absorption

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Fig. 51. Rigid zinc porphyrin-C60 dyad 34 via ‘two-point‘ binding strategy.

Fig. 53. Supramolecular zinc porphyrin-stilbazole pyromellitic diimide conjugate 36.

Fig. 52. Supramolecular dyad 35 featuring MgP axially coordinated with C60 Im.

band of C60 radical anion at 1000 nm, from which the rate constant of charge recombination and the lifetime of C60 − : MgTPP+ were determined to be 8.3 × 107 s−1 and 12 ns, respectively [292]. The finding that the lifetime of the charge-separated state of C60 :ZnTPP (32) [289] is longer than that of C60 :MgTPP (34) [292] agrees well with the covalently linked systems 1 and 2 [215,216]. Otsuki et al. reported supramolecular dyad 36 (Fig. 53) where the stilbazole derivative containing a pyromellitic diimide unit was axially connected to the porphyrin [293]. The former unit acts an electron acceptor, while the latter acts as an electron donor. The zinc porphyrin can then transfer electrons through the bridge unit. The beauty of this system is that fluorescence quenching was only observed with the cis isomer and not with the trans isomer. The electron transfer rate and efficiency in the case of the cis isomer were found to be 1.83 × 109 s−1 and 0.77, respectively, whereas in trans isomer it was negligible. Such system exhibited photoswitchable photoinduced electron transfer based on geometric change [293]. The concept of axial ligation was extended to construct a simple working model of the antenna-reaction center complex by using the supramolecular approach. An example is shown in triad 37 (Fig. 54), where C60 Im is coordinated to the zinc atom of a covalently

Fig. 54. BODIPY-zinc porphyrin-fullerene based energy and electron transfer donoracceptor triad 37.

linked zinc porphyrin–BODIPY dyad to form the supramolecular triad (37: C60 Im → ZnP-BODIPY) [294]. This combination of BODIPY, porphyrin, and fullerene absorb the light in the broad range


Fig. 55. BODIPY-zinc phthalocyanine (ZnPc)-fullerene (C60 py) based energy and electron transfer donor-acceptor supramolecular triad 38.

of the visible spectrum. A good spectral overlap was observed between the BODIPY emission and the porphyrin absorption suggesting the occurrence of efficient intramolecular energy transfer [294]. This behavior was confirmed by recording the picosecond time-resolved emission studies in o-dichlorobenzene, where the rate constant and efficiency of the energy transfer from the singletexcited state of BODIPY to ZnP were found to be 9.2 × 109 s−1 and 0.83, respectively [294]. The formed singlet-excited state of ZnP donates an electron to the coordinated C60 , generating the rela• • tively stabilized charge-separated state (C60 Im − → ZnP + -BODIPY) with a lifetime of 5.0 ns [294]. The same type of coordination-covalent binding has been employed to construct supramolecular triad 38 (Fig. 55) [295]. The BODIPY unit is tethered to the peripheral position of a zinc phthalocyanine (ZnPc). The pyridine appended fulleropyrrolidine (C60 py) is utilized to coordinate to the zinc atom of ZnPc [295] to form the supramolecular triad C60 py:ZnPc-BODIPY. The advantage of such system stems from the complementary absorption of the UV/Vis part of the solar spectrum of the Pc (␭max = 680 nm) and BODIPY (␭max = 525 nm). The photochemical events in the noncoordinating toluene showed the energy transfer from the antenna BODIPY to the covalently linked zinc phthalocyanine, followed by electron transfer from the formed singlet-excited state of zinc phthalocyanine to C60 py generating the charge-separated state C60 py:ZnPc-BODIPY with a relatively long lifetime of 39.9 ns [295]. Supramolecular tetrad 39 (Fig. 56)shows another type of coordination-covalent binding complex [241], where the fullerene functionalized with an imidazole group is axially coordinated to the zinc center of the zinc porphyrintriphenylamine-subphthalocyanine (SubPc-TPA-ZnP) triad forming the supramolecular tetrad SubPc-TPA-ZnP:ImC60 . The subphthalocyanine acted here as an antenna unit, TPA-ZnP as a charge stabilizing moiety, and C60 Im as an electron acceptor. Optical absorption studies revealed a red-shift of the Soret absorption band of the zinc porphyrin entity with an addition of C60 Im indicating formation of SubPc-TPA-ZnP:ImC60 complex via metalligand axial coordination with a rate constant of 1.1 × 104 M−1 [241]. Similarly, the fluorescence studies revealed fluorescence quenching of the singlet-excited state of ZnP, which is likely due to electron transfer process from the singlet-excited porphyrin • • to the C60 Im moiety generating (C60 Im − :ZnP + -TPA-SubPc). The femtosecond transient absorption measurements showed a clear

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evidence of the electron transfer from the singlet-excited zinc porphyrin to the coordinated C60 Im by recording the characteristic • transient absorption bands of TPA-ZnP + (at 650 and 800 nm) • and C60 −(at 1000 nm). From the rise and decay of the C60 − , the rate constants of charge separation and charge recombination via the 1 ZnP* were determined to be 8.0 × 1011 and 6.3 × 108 s−1 , • • respectively [241]. The lifetime of C60 Im − :ZnP + -TPA-SubPc was determined to be 1.1 ns, as calculated from the inverse of the rate of charge recombination [241]. By utilizing the complementary nanosecond transient absorption spectroscopy, it was interesting to see the triplet character of the charge-separated state • • (C60 Im − :ZnP + -TPA-SubPc) with a lifetime of 6.6 ␮s by recording the radical species in the microsecond time domain [241]. By taking the unique properties of azaBODIPY and zinc porphyrin into account, supramolecular systems of covalently linked azaBODIPY-(zinc porphyrin)2 hosting bis-pyridine functionalized fullerene C60 (py)2 were recently reported by D’souza et al. [296]. As seen, the azaBODIPY was functionalized with two zinc porphyrin entities forming (ZnP)2 -azaBODIPY (40) (Fig. 57) . The two zinc porphyrin entities of 40 were arranged to accommodate the C60 (py)2 via a ‘two-point’ metal-ligand axial coordination to form the supramolecular tetrad (41: C60 (py)2 :(ZnP)2 -azaBODIPY) [296]. Spectroscopic studies of 40 showed the efficient energy transfer from the 1 ZnP* units to the attached azaBODIPY in toluene with a rate of 6.6 × 1011 s−1 , which was expected to occur from the good spectral overlap between the ZnP emission and azaBODIPY absorption [296]. Changing the solvent from the less polar toluene to polar benzonitrile revealed further quenching of the singlet ZnP emission with no emission corresponding to azaBODIPY indicating additional electron transfer from zinc porphyrin to the formed singlet-excited state of azaBODIPY producing the elec• • tron transfer product (ZnP)2 + -azaBODIPY − with a rate constant 10 −1 of 4.5 × 10 s as seen from the femtosecond transient absorption measurements [296]. The ‘molecular clip’ like structure of 40 was utilized to construct supramolecular tetrad using fullerene functionalized with two pyridine entities suitable for accommodating both the ZnP entities of C60 (py)2 :(ZnP)2 -azaBODIPY 41 by a ‘two-point’ axial coordination approach (Fig. 57) . The binding constant of 41 was determined to be 1.8 × 105 M−1 [296], based on the absorption and fluorescence measurements. Unlike the observed energy transfer from ZnP to azaBODIPY of 40, both the steady-state fluorescence and femtosecond transient absorption measurements showed the occurrence of electron transfer from the singlet ZnP to coordinated C60 (py)2 forming the charge-separated • • state C60 (py)2 − :(ZnP)2 + -azaBODIPY with a lifetime of 5.5 ns [296]. In a similar fashion, Gust et al. reported the photodynamic studies of a molecular hexad 42 composed of two zinc porphyrin moieties and four coumarin antenna entities, all organized by a central hexaphenylbenzene core (Fig. 58) [297]. The picosecond transient absorption studies showed fast and efficient energy transfer from the singlet-excited state of coumarin chromophores to zinc porphyrin on the 1–10 ps time scale, depending on the site of initial excitation. Such rates of energy transfer are consistent with the Förster dipole–dipole mechanism [297]. To utilize it as an antenna–reaction center complex, the bis-pyridine functionalized fullerene C60 (py)2 moiety self-assembles to the form of the hexad containing zinc porphyrins by a ‘two-point’ axial coordination approach. In the resulting heptad, the photochemical events involved the energy transfer from the singlet-excited state of coumarin chromophores to populate the singlet zinc porphyrin, which in turn donate an electron to the fullerene unit with a time • • constant of 3 ps to generate the charge-separated state (P + –C60 − ) with an overall quantum yield of 1.0 [297]. Finally, the chargeseparated state decays to populate the ground state with a time constant of 230 ps in o-difluorobenzene [297].

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Fig. 56. (Left) Subphthalocyanine-triphenylamine-zinc porphyrin-fullerene based energy and electron transfer donor-acceptor tetrad 39. (Right) Nanosecond transient absorption spectra observed by 430 nm laser irradiation of supramolecular tetrad 39 in N2 -saturated toluene. Inset: Absorption time profile of the C60 radical anion at 1000 nm.

Fig. 57. (Left) Structure of azaBODIPY-(ZnP)2 triad 40, and azaBODIPY-(ZnP)2 :py2 C60 supramolecular tetrad 41. (Right) Energy-level diagram showing the photochemical events of triad 40 (left) and self-assembled tetrad 41 (right).


Fig. 58. Structure of (coumarin)4 -(ZnP)2 -py2 C60 supramolecular heptad 42, and the proposed modulation of photoinduced electron transfer processes.

5.2.1.2. Naphthalocyanines-based supramolecular systems. Design of novel artificial photosynthetic systems capable of collecting and harvesting light from the visible and near-IR regions of the electromagnetic spectrum is challenging. For this, our group paid much attention in the recent years to construct supramolecular photosynthetic systems based on naphthalocyanine chromophores. As seen from Fig. 59, a more extended ␲-electron conjugated system going from porphyrin to phthalocyanine, macrocycles brings about a shift of absorption maxima to longer wavelengths, which results in a light harvesting better matched with the solar spectrum. To sensitize in the near infrared region (700–900 nm), a further benzoannelation is introduced into phthalocyanine rings, which results in naphthalocyanine (Nc) derivatives [298]. Naphthalocyanines emerge as attractive molecular building blocks for the artificial photosynthetic systems for their higher chemical and thermal stability, rich redox chemistry, which is suitable for effi-

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cient electron-transfer processes, and also ability to form metal complexes with almost all the metal ions, and semi-conducting properties when appropriately self-assembled via ␲ − ␲ stacking interactions [299–308]. A first example is shown in the supramolecular zinc naphthalocyanine-fullerene dyad (43), in which an imidazoleappended fullerene (C60 Im) axially coordinates via the imidazole nitrogen to the central metal of zinc naphthalocyanine (ZnNc) in non-coordinating toluene (Fig. 60) [309]. The binding constant was determined to be 6.2 × 104 M−1 , which is considerably larger than that of the zinc porphyrin analogous 32 [289]. Based on the time-resolved fluorescence measurements in toluene, the electron transfer occurs from the electron rich zinc naphthalocyanine to • • the electron deficient C60 Im generating the C60 Im − :ZnNc + with 10 −1 a quantum yield of 97% and rate constant of 1.4 × 10 s [309]. The picosecond transient absorption studies confirmed the electron transfer character by recoding the characteristic absorption bands of zinc naphthalocyanine radical cation at 985 nm [286]. From the rise and decay of this band, the rate constant of chargeseparation and charge-recombination processes were found to be 1.4 × 1010 and 8.5 × 108 s−1 , respectively [309]. The photochemical events in the coordinating benzonitrile showed quite different features, where the binding constant was found to be quite small compared to that in the non-coordinating toluene, in addition the electron transfer takes place from the triplet zinc phthalocyanine, but not from singlet state. This work has been extended by self-assembling two zinc naphthalocyanines to a fulleropyrrolidine bearing two pyridine entities using axial coordination approach to form C60 (py)2 :ZnPc supramolecular triad 44 (Fig. 60) [310]. The optimized structure of 44 showed that the two naphthalocyanine rings were nearly coplanar separated by 15.5 Å (Zn-to-Zn distance), while fullerene entity is located at the top of the center of the two rings. Compared with 43, the optical absorption and emission studies of 44 revealed more stable complex formation with a formation constant of 1.1 × 105 M−1 [310]. Upon exciting the ZnNc entity, an efficient electron transfer occurs from the singlet ZnNc to its coordinated • • C60 (py)2 generating the charge-separated ZnNc + −C60 (py)2 − with a quantum yield of 93% and a lifetime of 30 ns. The longer life-

Fig. 59. Absorption spectra of porphryin derivatives, phthalocyanines, and naphthalocyanine.

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Fig. 60. Structure of ZnNc:C60 Im supramolecular dyad 43 and (ZnNc)2 :C60 (py)2 supramolecular triad 44. •

Fig. 61. Structure of Fc-C60 py:ZnNc supramolecular triad 45, and the proposed electron transfer processes.

time of 44 compared to 43 (18 ns) was rationalized by the charge delocalization among the two zinc naphthalocyanine entities [310]. The concept of multistep electron transfer was utilized here to construct supramolecular triad 45 by coordinating zinc naphthalocyanine to the covalently linked pyridylfullerene-ferrocene dyad via metal-ligand axial coordination (Fig. 61) . Here, zinc naphthalocyanine entity acts as a primary electron donor, ferrocene as a second electron donor, pyridylfullerene as an electron acceptor [311]. Although the optimized structure indicates the second electron donor (Fc) away from the primary electron donor (ZnNc), the obtained photochemical data reflect the important role of the second donor in the generation of the charge-separated state in the triad. Upon excitation the ZnNc entity, the electron transfer takes place from the singlet ZnNc to the coordinated C60 py generating the • • charge-separated state Fc-C60 − py:ZnNc + with a quantum yield of 9 −1 0.83 and rate constant of 2.4 × 10 s [311]. Considering the lower

•

energy level of Fc-C60 − py:ZnNc + compared to the final charge• • separated state Fc+ -C60 − py:ZnNc, a hole transfer from the ZnNc + to the Fc entity is energetically favorable. The lifetime of charge• separated state of Fc+ -C60 − py:ZnNc was determined to be 15 ns • • [311], which is much longer than that of Fc-C60 − py:ZnNc + . These findings reflect the role of the second donor moiety in prolonging the lifetime of the charge-separated state in 45. In the previous examples, we discussed various photosynthetic supramolecular complexes based on C60 derivatives, as electron acceptor entities. A literature survey shows that zinc naphthalocyanine was coordinated with other electron acceptors including subphthalocyanine [312], perylenediimide [313], and naphthalenediimide [314] to construct novel supramolecular systems with good light harvesting properties in a wide range of the solar spectrum. The combination of zinc naphthalocyanine and subphthalocyanine shown in molecule 46 has been done in order to construct photosynthetic supramolecular system capable of collecting and harvesting light in a wide range of solar spectrum (300–900 nm) (Fig. 62) [312]. For it, the electron accepting pyridine-appended subphthalocyanine is linked to the zinc atom of zinc naphthalocyanine via metal-ligand coordination [290]. Both optical and emission studies in o-dichlorobenzene suggested stable complex formation with binding constant of 1.2 × 105 M−1 [312]. Upon exciting the ZnNc or SubPc(py), the quenching pathway involved charge separation from the ZnNc to the electron deficient SubPc(py). The energy-transfer process was excluded because of the lack of overlap between the SubPc(py) emission and ZnNc absorption. The electron transfer character from ZnNc to SubPc(py) was confirmed by recording the transient absorption band of the ZnNc radical cation at 960 nm, from which the rate constant of electron transfer from ZnNc to SubPc(py) was found to be 1.3 × 1010 s−1 [312]. The lifetime of the generated • charge-separated state ZnNc + -SubPc(py)− was found to be 1 ns.


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Fig. 62. (Left) Structure of SubPc(py):ZnNc supramolecular dyad 46. (Right) HOMO and LUMO for the self-assembled SubPc(py):ZnNc dyad.

The high charge-separation/charge-recombination ratio suggests the usefulness of self-assembled ZnNc: SubPc(Py) as an effective photosynthetic reaction center model. To examine the relation between the photochemical reactivities of the designed light harvesting supramolecular systems with their structures, we examined the photodynamic studies of molecules 47 and 48 that formed by linking zinc naphthalocyanine with pyridine-appended perylenediimide (PDIpy) and imidazoleappended perylenediimide (PDIim), respectively (Fig. 63) [313]. The perylenediimide entity of 47 was substituted with tertoctylphenoxy groups at the bay positions (PDIpy). The optical absorption studies for 47 and 48 showed a strong absorption in the visible and near-IR region, and stable complex formation (K = 2.4 × 104 and 1.1 × 105 M−1 for 47 and 48, respectively) [313]. Optical emission studies showed the electron transfer character from ZnNc to the perylene entity generating the charge-separated states. However, the kinetic studies performed by the femtosecond transient absorption technique showed clear difference between both systems in terms of rates of charge separation and charge recombination. It was clearly observed that the rates of both charge separation and charge recombination of 47 (4.1 × 1010 and 2.3 × 108 s−1 , respectively) are much larger than that of 48 (1.2 × 109 and 2.2 × 107 s−1 ) [313]. From the rates of charge recombination, it was interesting to see the much longer lifetime of charge-separated state of 48 (45 ns) compared with that of 47 (4.3 ns) [313]. Such a long-lived charge-separated state of 48 was rationalized by: (i) the steric effect caused by the substituted tertoctylphenyloxy groups at the bay positions of the PDI ring, and (ii) the longer center-to-center distance between the PDIim and ZnNc entities. In a similar way, the relation between structures and photochemical reactivities of two self-assembled dyads 49 and 50 has been examined. These two dyads have been constructed by coordinating pyridine-appended naphthalenediimide (NDIpy) with the zinc atom of naphthalocyanine chromophore (Fig. 64) [314]. In 49, NDI core and pyridine moiety were separated by two methylene units to modify its coupling with ZnNc. In order to improve their solubility, ethylhexyl and tert-butyl groups were installed in the naphthalenediimide and zinc naphthalocyanine, respectively. From optical absorption studies, the formation constants for 49 and 50 in toluene were to be 2.5 × 104 and 2.2 × 104 M−1 , respectively, suggesting moderately stable complex formation [314]. The electron transfer character from the singlet excited ZnPc to NDIpy and NDI(CH2 )2 py was observed from the steady-state emission and femtosecond transient absorption techniques. From the transient absorption band of ZnNc radical cation at the near-IR, the rate constants of charge separation of 49 and 50 were found to be 2.2 × 1010 and 4.4 × 109 s−1 , respectively, indicating fast charge separation [314]. The rate constants of charge recombination (lifetimes of the charge-separated states) were determined to be 8.5 × 108 s−1

(1.2 ns) for 49 and 1.9 × 108 s−1 (5.3 ns) for 50 [314], indicating the effect of long spacer in increasing the lifetime of the chargeseparated states. 5.2.2. Supramolecular photosynthetic complexes via crown ether-ammonium cation interactions Since Pederson’s invention of crown ethers [315], they have been treated as one of effective groups for selective binding to cationic, anionic and also neural analyst [316–318]. Among these, benzo 18-crown-6 received much attention because of their ease to form hydrogen-bonding complexes with quaternary alkyl ammonium cations [284,319]. Owing to its importance, non-covalently linked donor-acceptor systems have been systematically studied to mimic the natural photosynthetic antenna-reaction center. Unlike the metal-ligand coordination where the photochemical studies should perform only in the non-coordinating solvents, crown etherammonium cation binding mode allows the researchers to perform the photochemical studies in different media [284,288,320,321]. Because of its importance and ease of construction, D’souza et al. utilized the crown ether-ammonium cation binding mode to build an artificial photosynthetic triad 51 to mimic the antenna-reaction center complex in a supramolecular fashion (Fig. 65) [322]. For the construction, first, BODIPY was covalently attached to a zinc porphyrin entity bearing a benzo-18-crown-6 host segment at the opposite end of the porphyrin ring. Next, an alkyl ammonium functionalized fullerene was used to self-assemble the crown ether entity via ion-dipole interactions to form the moderately stable supramolecular triad 51 (K = 4.6 × 104 M−1 ) in polar benzonitrile [322]. The optical emission and time-resolved emission studies showed the occurrence of energy transfer from the antenna BODIPY to the energy acceptor zinc porphyrin with a quantum efficiency of ∼97%. This was followed by charge separation from the 1 ZnP* to the linked C60 , via the crown ether-ammonium cation interactions, to populate a short-lived charge-separated state [322]. By utilizing the nanosecond transient absorption spectroscopy, it was interesting to see the formation of the triplet character of the charge-separated state with a lifetime of 23 ␮s, indicating charge stabilization in the supramolecular triad [322]. A notable weakness of 51 [322], however, stems from the arrangement of the donor ZnP and acceptor C60 entities close to each other. Although charge stabilization to some extent was observed, a long-lived charge stabilized state was difficult to attain. This approach was extended by designing a new supramolecular triad 52 [323], which composed of the same subunits BODIPY, ZnP and C60 but with different spatial arrangement (Fig. 66) . The authors intentionally placed the BODIPY antenna unit between the electron donor ZnP and C60 to increase the distance between them [323]. Similar to 51, the photodynamic behavior of C60 :crownBODIPY-ZnP showed the energy transfer from the singlet-excited BODIPY to ZnP, followed by electron transfer from

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Fig. 63. (Upper panel) Structure of ZnNc axially coordinated with PDIpy and PDIim to form dyads 47 and 48, respectively. (Lower panel) Femtosecond transient absorption spectra observed by 390 nm laser irradiation of 47 in N2 -saturated toluene (left Figure) and nanosecond transient absorption spectra observed by 430 nm laser irradiation of 48 in N2 -saturated toluene (right Figure). Inset: Absorption time profiles of the ZnNc radical cation at 960 nm.

the singlet ZnP to C60 . The nanosecond transient absorption measurements of 52 in polar benzonitrile showed a clear evidence of • • formation of the long-lived C60 − :crownBODIPY-ZnP + with a lifetime of the order of 100 ␮s [323], which was nearly four times longer compared to that of 51 [322]. Such interesting finding revealed the importance of the spatial arrangements for the donor and acceptor units in constructing efficient artificial photosynthetic systems. The cation–crown ether binding was combined with another metal-ligand coordination mode to form a well-defined distance and orientation supramolecular porphyrin-fullerene dyad 53 (Fig. 67) [324]. The optical absorption studies in polar benzonitrile showed the formation of stable supramolecular complex with a binding constant of 4.4 × 104 s−1 [324], which is much higher than that of the supramolecular ZnP:PyC60 dyad 31 [264] via only the metal-ligand binding mode (7.0 × 103 M−1 ). The photochemical studies showed a fast charge separation from the singlet-excited state of ZnP to C60 with a quantum yield of 0.86 and a rate constant of (3.1 × 109 s−1 ) [324]. The charge recombination between the radical-ion pairs was found to be 2.1 × 107 s−1 . The higher ratio of charge-separation/charge-recombination rates of 53 compared to that of 31, suggesting the effect of “two-point” binding strategy in forming stable and efficient artificial light harvesting supramolecular complexes compared to “one-point” binding mode [324].

5.2.3. Axial coordination in donor–acceptor ensembles of silicon phthalocyanines Silicon phthalocyanines (SiPcs) with their low tendency to aggregate, high solubilities, longer fluorescence lifetimes, longlived and low-lying triplet excited state, and the ease of chemical modification at the axial positions [325] have been employed in photodynamic therapy [326–330], organic photovoltaic devices [331,332], and hydrogen production [333]. Recently, SiPcs have been utilizing as building blocks for constructing artificial photosynthetic systems [334–339]. In such complexes, the electron-donating SiPcs can form strong Si–O bonds by axial coordination of carboxylates with various electron acceptors. Utilization of silicon phthalocyanine as energy acceptor in the energy-transfer reactions was shown in molecule 54 (Fig. 68), where the silicon phthalocyanine is axially linked with two zinc porphyrin entities SiPc–(ZnP)2 ) [340]. In this model, SiPc acts as a promising electron/energy acceptor unit. Upon photoexcitation of the zinc porphyrin moieties, the electron transfer occurs from the singlet excited ZnP to the electron deficient SiPc generating • • the charge-separated state (SiPc − -(ZnP)2 + ) with a rate constant of 2.4 × 1012 s−1 in dimethylformamide [340]. The observation of the singlet SiPc emission after the photoexcitation of zinc porphyrin moieties gives evidence for energy transfer from the singlet excited ZnP with a rate of 7.3 × 1011 s−1 [340]. In addition, the direct photoexcitation of the SiPc moiety also results in electron transfer from the porphyrin moieties to the singlet-excited state of SiPc to afford


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Fig. 64. (Upper panel) Structure of ZnNc axially coordinated with NDI-py and NDI-(CH2 )2 -py to form supramolecular dyads 49 and 50, respectively. (Lower panel) Femtosecond transient absorption spectra observed by 390 nm laser irradiation of 50 (right figure) and 49 (left figure) in N2 -saturated toluene. Inset: Absorption time profile of the ZnNc radical cation at 960 nm.

Fig. 65. Structure o supramolecular triad 51 where BODIPY-zinc porphyrin entity bearing benzo-18-crown-6 is linked with alkyl ammonium functionalized fullerene, and the proposed energy and electron transfer processes. •

•

the same charge-separated state (SiPc − -(ZnP)2 + ) with a lifetime of 20 ps [340]. Silicon phthalocyanine can be also utilized as electron donor in the photosynthetic donor-acceptor complexes. Examples of these models are shown in molecules 55-57 (Fig. 69) [341,342]. In triad 55, SiPc is axially linked with two units of fullerene C60 forming SiPc-(C60 )2 [341]. Similarly, triads 56 and 57 have been constructed by axially linking the SiPc with two units of trinitrofluorenone (TNF) and trinitrodicyano-methylenefluorene (TNDCF) to afford TNFSiPcTNF (56) and TNDCF-SiPc-TNDCF (57) [342]. These triads exhibit no aggregation phenomena in solution due to the presence of electron acceptor units in the axial position and the tert-butyl groups

in the equatorial positions of the phthalocyanine. The occurrence of photoinduced electron transfer from the singlet-excited state of SiPc to the electron acceptor moieties was confirmed by femtosecond laser flash photolysis measurements. The photoexcitation of SiPc-(C60 )2 (55) in benzonitrile with a 400 nm femtosecond laser pulse affords transient absorption bands of the SiPc radical cation (at 880 nm), and C60 radical anion (1000 nm) as an evidence for occurrence of electron transfer from the singlet-excited state of • SiPc to C60 generating SiPc + -(C60 )2 • − with a lifetime of 5.0 ns [341]. When turning to 56 and 57, it was found that the rate constants of charge separation were determined as 2.0 × 1011 and 2.9 × 1012 s−1 , respectively. The rate constants of charge recombination (lifetimes of the charge-separated states) for 56 and 57 were found to be

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Fig. 66. (Left) Structure o supramolecular triad 52 where alkyl ammonium functionalized fullerene is linked with BODIPY-zinc porphyrin entity bearing a benzo-18-crown-6, and the proposed energy and electron transfer processes. (Right) Nanosecond transient absorption spectra observed by 430 nm laser irradiation of supramolecular triad 52 in N2 -saturated benzonitrile. Inset: Absorption time profile of the C60 radical anion at 1000 nm.

Fig. 67. Structure of supramolecular zinc porphyrin-fullerene dyad 53 via cationcrown ether and metal-ligand coordination binding modes.

2.0 × 1011 s−1 (22 ps) and 2.9 × 1012 s−1 (2.2 ps), respectively [342]. Compared with SiPc-(TNF)2 56 and SiPc-(TNDCF)2 57, the slow rate of charge recombination for SiPc-(C60 )2 55 was recorded because of the effect of the spherical C60 in decelerating the charge recombination process [341,342]. SiPc triads have been extended to a SiPc-(azobenzene)2 -(C60 )2 pentad (58) composed of silicon phthalocyanine (SiPc) that is connected with two fullerene C60 and two azobenzene units (Fig. 70) [343]. This combination between SiPc, azobenzene and C60 in the examined SiPc-(azobenzene)2 -(C60 )2 allows exhibiting strong light absorption over the whole visible spectrum. Photoexcitation of the pentad results in rapid formation of the charge-separated state (2.0 × 1011 s−1 ) by photoinduced electron transfer from the singletexcited state of SiPc to C60 [343]. Such electron transfer character

was supported by observing the fluorescence quenching of the singlet SiPc by the attached two C60 units, and the negative driving force for charge separation as obtained from the electrochemical measurements. From the recombination between the SiPc radical cation and C60 radical anion, the charge-separated state has a lifetime of 2.50 ns in benzonitrile [343], which is rationalized by the long center-to-center distance between SiPc and C60 (17 Å). This work has been further extended by replacing two azobenzene units with two 1,4,5,8-naphthalenediimide to form C60 NDI-SiPc-NDI-C60 pentad (59) as (acceptor2-acceptor1donor-acceptor1-acceptor2) model (Fig. 71) [344]. Pentad 59 has been compared with the SiPc-(NDI)2 triad to examine the effect of multistep electron transfer from the singlet excited state of SiPc to the attached planar NDI (first electron acceptor) and spherical C60 (second electron acceptor) on increasing the lifetime of chargeseparated state of the pentad. The lifetime of charge-separated state • • (SiPc + -(NDI)2 -(C60 )2 − ) was determined to be 1000 ps [344], which • • is four time longer that of SiPc + -(NDI)2 − triad (60) (Fig. 71). This interesting finding indicates the effect of electron-shift between the electron-accepting NDI and C60 entities on prolonging the lifetime • of the charge-separated state (SiPc + -(NDI)2 -(C60 )2 • −) [344]. For constructing an efficient light harvesting systems based on silicon phthalocyanine, we designed and examined the photodynamic properties of the highly soluble dendrimers 61 (Fig. 72), where silicon phthalocyanine was linked with two, four and eight fullerene entities to form SiPc-nC60 dendrimers (where n = 2 (G1), 4 (G2) and 8 (G3) with relatively high yields [345]. The structures of G1-G3 were confirmed by using 1 H NMR, and MALDI-TOF massspectroscopic analysis. The optical absorption studies showed strong absorption bands in the visible region with maxima at 685 and 340 nm. The fluorescence measurements showed significant fluorescence quenching of the singlet excited SiPc by the attached C60 entities. Based on the fluorescence time profiles of the singlet

Fig. 68. Structure of SiPc-(ZnP)2 dyad 54.


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Fig. 69. Structure of triads SiPc-(C60 )2 (55), SiPc-(TNF)2 (56) and SiPc-(TNDCF)2 (57), and the proposed electron transfer processes.

Fig. 70. Structure of SiPc-(C60 )2 triad 58 and the proposed modulation of photoinduced electron transfer processes.

excited SiPc, the rate constants of charge separation were found to 3.6 × 108 , 2.7 × 108 and 2.4 × 108 s−1 for G1, G2 and G3, respectively [345]. By employing the nanosecond transient absorption studies, the electron transfer takes place from the singlet excited SiPc to the linked C60 units generating the charge-separated states • • SiPc + -nC60 − with lifetimes of 33, 149, and 200 ns for G1, G2 and G3, respectively [345]. The elongation of the charge-separated lifetimes of G3 compared to that of G1 and G2 was rationalized by the electron migration among the eight C60 subunits. The high ratio of charge recombination/charge separation rates, in addition to their strong absorption in a wide range of the solar spectrum; suggest the usefulness of dendrimers 61 in the light-harvesting systems [345]. 5.2.4. Anion-complexation-induced stabilization of charge separation In certain cases, the activity of naturally occurring systems is optimum only in the presence of an ionic cofactor either due to resulting structural stabilization [346–348] or because of charge balancing by the ion [349–351]. This situation is observed in many enzyme systems using organic or inorganic ions. For example,

nature uses chloride anions as a cofactor of the oxygen-evolving complex (OEC) [352–360]. Inspired by the above concept, a supramolecular oligochromophoric model system (62) is an example of the concept of dual binding mode (Fig. 73) [361], where the bis-porphyrin-substituted oxoporphyrinogen OxP-(ZnP)2 has two different binding sites, as required. One site (composed of twisted two-faced zinc porphyrin units) is capable of binding bis(4-pyridyl)-substituted guests through coordination to the central zinc cations [361], while the other site (composed of two pyrrole-type amine groups of the oxoporphyrinogen unit) interacts with anionic species through hydrogen bonding [361]. The optical absorption spectra of OxP(ZnP)2 exhibited the absorption bands of ZnP and OxP at 430 and 510 nm, respectively [361]. Compared to tetraarylporphyrins, it was found that the Soret band of ZnP entity of OxP-(ZnP)2 is ∼15 nm red-shifted because of the higher ␲-conjugated porphyrin macrocycle [361]. Steady-state fluorescence studies revealed an efficient fluorescence quenching of the singlet excited ZnP (at 612 and 667 nm) by the attached OxP entity, which was rationalized by the electron transfer from the singlet excited ZnP to the attached

74


Fig. 71. Structure of SiPc-(NDI)2 -(C60 )2 pentad (59) and SiPc-(NDI)2 triad (60), and the proposed modulation of photoinduced electron transfer processes. •

OxP forming the charge-separated state OxP•− -(ZnP)2 + with a rate of 1.4 × 1010 s−1 and a quantum yield of 0.96 [361]. Upon coordination of ZnP-(OxP)2 with C60 (py)2 using the two-point binding approach to form supramolecular tetrad OxP-(ZnP)2 :C60 (py)2 , the electron transfer takes place from the singlet-excited state of ZnP to the axially coordinated C60 (py)2 forming the charge-separated • • OxP-(ZnP)2 + :C60 (py)2 − with a rate of 1.7 × 1010 s−1 and a quantum yield of 0.97 [361]. The charges of C60 radical anion and ZnP radical cation were recombined with a rate of 5.7 × 106 s−1 , from which the lifetime of the charge-separated state was determined to be 160 ns [361]. Complexation of F− anion to the oxoporphyrinogen center of OxP-(ZnP)2: C60 (py)2 formed two-bound supramolecular host complex (OxP-(ZnP)2 :C60 (py)2 + F− ) with a binding constant of 7.4 × 104 M−1 as recorded from the steady–steady absorption and fluorescence emission measurements [362]. As demonstrated from the electrochemical measurements, complexation of F− anion to the oxoporphyrinogen center lowers its first oxidation potential by nearly 600 mV, allowing an intermediate energy state for charge • migration from the ZnP + to the oxoporphyrinogen:anion complex [361]. A decrease in charge recombination driving force caused by F− anion binding, in addition to the increase in the reorganization energy of electron-transfer process, results in the desired increase in the lifetime of the charge-separated state from 0.16 ␮s (for OxP(ZnP)2 :py2 C60 ) [341] to 14 ␮s (for OXP-(ZnP)2 :py2 C60 + F− ) [362] as indicated by the nanosecond transient absorption studies. Such interesting finding provides valuable insight into the role of anion binding on the control of the photodynamics of both photoinduced electron-transfer and charge-recombination reactions. Another example to control the electron-transfer processes by adding external ionic cofactors was shown in molecule 63 (Fig. 74) [363]. As seen, the chemical structure contains two fulleropyrrolidine (C60 ) units substituted through 4,4 -biphenylmethylene groups at the nitrogen atoms of an oxoporphyrinogen (OxP) unit forming OxP(C60 )2 [363]. From the optical absorption studies in polar benzonitrile, the binding constant of F− with OxP(C60 )2 was

found to be 5.8 × 104 M−1 , suggesting moderately stable complex formation [363]. The emission of the singlet-excited state of OxP was heavily quenched by adding F− due to formation of an almost non-emitting complex (> 98% quenching) [363]. Interestingly, addition of F− revealed drastic changes in the oxidation potentials of OxP entity. As seen from the electrochemical measurements, addition of 1 equivalent of F− to the solution of OxP(C60 )2 resulted in a cathodic shift of nearly 510 mV (E1/2 = −0.14 V) [364]. From the redox values of OxP and C60 entities, the driving forces for charge separation for OxP(C60 )2 in the absence and presence of F− were found to be 0.1 and 0.61 eV, respectively. By utilizing the nanosecond transient absorption spectroscopy, the lifetime of the charge-separated state in the presence of F− was determined as 6.3 ␮s [363], which is much longer than that of OxP(C60 )2 (15 ps), reflecting the great effect of F− anion-complexation on charge stabilization of the electron-transfer products.

5.3. Artificial photosynthetic systems for production of hydrogen The sustainable production of solar fuels, such as H2 from water, by artificial photosynthesis is a promising means to replace fossil fuels for long-term global energy requirements. There has been much effort for development of artificial photosynthesis where the hydrogenase enzymes have been replaced by Pt nanoclusters. The reaction center protein has also been replaced by synthetic organic compounds, which undergo efficient charge separation with slow charge recombination. A variety of photocatalytic hydrogen-evolution systems have been developed and studied for many years [365–377]. Such systems normally consist of an electron donor, a photosensitizer, an electron mediator such as methyl viologen (MV2+ ), and a hydrogen-evolution catalyst such as Pt nanoclusters (Scheme 1). Photosensitizers have also been linked covalently or noncovalently with MV2+ in order to improve the charge separation efficiency in the hydrogen-evolution photocatalytic systems [373–377]. However, it took a long time (e.g. h) to obtain an appreciable amount


75

Fig. 72. Structure of SiPc-(C60 )n dendrimers 61 (where n = 2, 4 and 8).

of hydrogen because the lifetime of the charge-separated state is relatively short, and the catalytic activity of hydrogen production • with MV + is also low [377]. As an example, the previously mentioned triad 5 (ZnP-H2 PC60 ) [218] has been reported to act as an efficient photocatalysts for the uphill oxidation of an NADH analogue, 1-benzyl-1,4dihydronicotineamide (BNAH), [377,378] by hexyl viologen (HV2+ ), as shown in Scheme 2. Electron transfer from BNAH (Eox = 0.57 V vs. • SCE) to ZnP + (Eox = 0.71 V vs. SCE) is exothermic. Electron transfer •– from C60 (Ered = –0.67 V vs. SCE) to HV2+ (Ered = −0.42 V vs. SCE) is also exothermic [377,379]. Thus, once the charge-separated state is produced by photoirradiation of 5, the electron-transfer oxidation of BNAH and the electron-transfer reduction of HV2+ are accom-

•

•

plished by electron transfer with ZnP + and C60 − , respectively (Scheme 2). The occurrence of such electron transfer reactions was studied by laser flash photolysis measurements, confirming that triad 5 indeed acts as an efficient photocatalyst for the uphill oxidation of NADH analogues by HV2+ in benzonitrile [377,379]. The quantum yield of the photocatalytic reaction increases with increasing concentration of HV2+ or BNAH, to reach a limiting value • • of 0.99. The longer lifetime of the ZnP + -spacer- C60 − state in the triad 5 (8.3 ␮s) relative to that of the ZnP-C60 dyad (0.8 ␮s) results in enhanced redox reactions involving the charge-separated state, BNAH and HV2+ [377,379]. The photocatalytic efficiency of H2 evolution has been much improved by using organic donor–acceptor linked molecules with

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Fig. 73. Structure of supramolecular OxP-(ZnP)2: C60 (py)2 pentad (62) via two binding sites (metal-ligand coordination and anion binding).

Fig. 74. (Left) Structure of OxP(C60 )2 triad (63). (Right) Nanosecond transient absorption spectra observed by 430 nm laser irradiation of triad 63 in the presence of F− anion in dichlorobenzene.

Fig. 75. Time dependence of hydrogen evolution under steady-state irradiation (␭ > 390 nm) of a deaerated phthalic acid buffer and MeCN [1:1 (v/v)] mixed solution containing Acr+ –Mes, NADH and Pt-PVP in the absence (red) and in the presence (blue) of MV2+ at room temperature. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

a long-lived electron-transfer state [380,381], which can inject electrons directly to hydrogen-evolution catalysts without an electron mediator upon photoexcitation of the donor–acceptor linked dyads instead of using inorganic photocatalysts [382,383]. A very high quantum yield (52%) and a high yield (95%) of H2 based on

an electron donor NADH (␤-nicotinamide adenine dinucleotide, reduced form) was achieved under photoirradiation of a deaerated phthalic acid buffer (pH 4.5, 50 mM) and acetonitrile (MeCN) [1:1, v/v] mixed solution containing 9-mesityl-10-methylacridinium ion (Acr+ -Mes) (0.10 mM), NADH (1.0 mM) and poly(N-vinyl-2-


77

Scheme 1. Conventional photocatalytic system for hydrogen evolution with an electron mediator (methyl viologen).

Scheme 2. Photocatalytic reduction of hexyl viologen (HV2+ ) by an NADH analogue (BNAH) with an electron donor–acceptor triad 5 (ZnP-H2 P-C60 ).

Scheme 3. Photocatalytic hydrogen evolution with Acr+ –Mes and NADH.

pyrrolidone)-protected platinum nanocluster (Pt-PVP) (0.20 mg) at 298 K [383]. The photocatalyst (Acr+ -Mes) undergoes electron transfer from the Mes entity to the singlet-excited state of the Acr+ unit generating an extremely long-lived charge-separated state, which is capable of oxidizing NADH and reducing Pt-PVP, leading to efficient hydrogen evolution. The efficiency of hydrogen evolution is around 300 times higher than that in the presence of MV2+ (Fig. 75). This interesting finding was rationalized by the faster reduction rate of Pt-PVP by Acr• -Mes as compared with that by MV+ . The electron donor (NADH) is replaced by ethanol in the presence of an alcohol dehydrogenase (ADH) with which NADH is reproduced in the photocatalytic hydrogen evolution (Scheme 3) [383]. Thus, the overall catalytic reaction shows the formation hydrogen from ethanol using enzymatic, photochemical, and metal catalysts. 5.4. Artificial photosynthetic systems for production of hydrogen peroxide Although hydrogen can produce electricity using hydrogen fuel cells and electricity can produce hydrogen by electrolysis, being renewable and harmless to the environment, high-pressure tanks (350–700 bar) are necessary to store gaseous hydrogen

[377,384,385]. Industrial production processes of hydrogen are still expensive and energy consuming, and often produced from fossil fuels [377]. In addition, an effective infrastructure for supplying hydrogen has yet to be established. In contrast to hydrogen, hydrogen peroxide (H2 O2 ), a liquid with high energy density, is a promising energy carrier for portable devices in the next generation, because safety of H2 O2 is guaranteed not only in an aqueous solution but also in solid by forming adducts with urea or carbonate, in which H2 O2 concentration reaches higher than ∼30 wt% [386–389]. When H2 O2 , which contains two atoms of hydrogen and two atoms of oxygen, is used as a fuel, the only byproducts are steam, oxygen and heat with zero emissions of greenhouse gases. In contrast to gaseous hydrogen, hydrogen peroxide is a liquid, with low concentration (up to 10%) aqueous solutions used for bleaching hair, teeth, wood pulp and other products. H2 O2 is produced even in natural photosynthesis, in which the reducing power released from PSI via PSII by water oxidation is normally used for the reduction of NADP+ to NADPH by which CO2 is reduced in the well-known Calvin–Benson cycle, but PSI can also reduce O2 in the Mehler reaction to produce hydrogen peroxide via disproportionation of superoxide anion [390].

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Scheme 4. H2 O2 production under photoirradiation of [RuII (Me2 phen)3 ]2+ in the presence of Ir(OH)3 in H2 O.

Photocatalytic production of H2 O2 occurred under photoirradiation of [RuII (Me2 phen)3 ]2+ (Me2-phen = 4,7-dimethyl-1,10phenanthroline) used as a photocatalyst with visible light in the presence of Ir(OH)3 acting as a water-oxidation catalyst in an O2 -saturated water [391]. This is the combination of the photocatalytic two-electron reduction of O2 with the four-electron oxidation of H2 O by four equivalents of [RuIII (Me2 phen)3 ]3+ as shown in Scheme 4 [391]. Photoinduced electron transfer from the excited state of [RuII (Me2 phen)3 ]2+ to O2 results in the for• mation of [RuIII (Me2 phen)3 ]3+ and superoxide radical anion (O2 − ) which is protonated to produce H2 O2 in competition with back • electron transfer (BET) from O2 − to [RuIII (Me2 phen)3 ]3+ . Four III 3+ equivalents of [Ru (Me2 phen)3 ] can oxidize water with the aid of catalysis of Ir(OH)3 nanoparticles to produce O2 . Metal ions par• ticularly Sc3+ inhibit by strong coordination to O2 − to accelerate the production of H2 O2 [391]. The photocatalytic reactivity of H2 O2 production was improved by replacing Ir(OH)3 nanoparticles by [CoIII (Cp*)(bpy)(H2 O)]2+ (Cp* = ␩5 -pentamethylcyclopentadienyl, bpy = 2,2-bipyridine) and other water oxidation catalysts in presence of Sc(NO3 )3 in water [391–394]. The optimized quantum yield of the photocatalytic H2 O2 production at ␭ = 450 nm was determined using ferrioxalate actinometer to be 37% [391]. The value of conversion efficiency from solar energy to chemical energy was also determined to be 0.25% [391]. More efficient photocatalytic production of H2 O2 has been achieved using the most earth abundant seawater as an electron source instead of precious pure water and O2 in the air in a two-compartment photoelectrochemical cell with WO3 as a photocatalyst for water oxidation and a cobalt chlorin complex supported on a glassy-carbon substrate for the selective two-electron reduction of O2 [395]. The concentration of H2 O2 produced in seawater reached 48 mM, which was high enough to operate H2 O2 fuel cells [396–399]. The solar energy conversion efficiency for the photocatalytic production of H2 O2 in seawater was determined to be 0.55% under simulated 1 sun illumination. The highest solar energy conversion efficiency was determined to be 6.6% under simulated solar illumination adjusted to 0.05 sun after 1 h photocatalytic reaction (0.89% under the sun illumination), when surface modified BiVO4 with iron(III) oxide(hydroxide) (FeO(OH)) and CoII (Ch) were employed as a water oxidation catalyst in the photoanode and as an O2 reduction catalyst in the cathode, respectively [400]. The production of a high concentration of H2 O2 and its conversion to electrical energy can provides practical solution to the construction of the perfect recycling and sustainable society. 6. Conclusion Biohydrogen is considered the key of development and civilization, where it is one of the most effective solutions for double crisis

(pollution and energy). Studies on natural, semi-artificial, and artificial systems introduced the possibility of continuous hydrogen production even in low rate. Two main factors affect the successful production of hydrogen during the photosynthetic process; the rate of electrons flow and the absence of molecular oxygen. The rate of electrons flow from PSI to hydrogenase is enhanced by direct fusion of FD and Hydrogenase [158,161], while decreasing the evolving oxygen rate occurs by decreasing the activity of PSII [142,151,155–157]. Understanding the mechanism of photosynthetic process paves the way for enhancement the biohydrogen production either in vivo or in vitro [56–125]. Adjusting cultivation conditions and/or inducing Fd-Hyd construction are considered the 1st step for successful hydrogen production. In contrast, studies on biohydrogen production in vitro showed the efficient role of nanoparticles either as monolayers or as deposit agent on the surface donor side of PSI like platinum [156–181]. Although several attempts have been done to enhance the hydrogen production by native system, several problems have been observed under practical applications, where exposing algal cells to long time inactivation of PSII or sulfur-deficiency led to death of algal cells [108]. Moreover, incubation of isolated photosystems with highly oxygen tolerant [FeFe]-hydrogenase in the presence of suitable electrical catalysis generates high hydrogen production rate [126–154,156,167–173]. The structure Semi-artificial system is based on both isolated biological complexes and artificial components that facilitate the electrons flow between complexes. For example; MV (methyl viologen) have almost the same redox potential as FD, so it could be an excellent electron carrier between PSI and hydrogenases [164]. Also in Semi-artificial system, it is possible to use high tolerant [FeFe]-hydrogenase [156]. Moreover, the distance between PSI and hydrogenases could be reduced via dithiol linker [171–173], overexpression of PsaC or PsaE subunit with hydrogenase or any genetically engineering protein linker [156], immobilizing PSI complex on nanocrystalline semiconductors [174], or coating PSI complex with platinum nanoparticles [176–180]. So the main advantages of semi-artificial system are saving the flexibility to use the best electron carriers (natural or artificial), the hydrogenases (highly active or more tolerant) and the best photosystem complexes (stable and active). When turning to the artificial photosynthesis, one can see a rapid progress in the last years by constructing efficient molecular and supramolecular artificial photosynthetic systems. All of these examples of artificial photosynthetic owe their basic design parameters to processes found in natural systems. The relations between structures and photochemical reactivities are discussed in relation to the rates of the photoinduced intramolecular electron-transfer/energy-transfer reactions. The quantum yields and lifetimes of charge-separated state following the electron transfer processes are measures of achievements in artificial photosynthesis systems. The longer the lifetime of charge-separated states, the greater the chance that a subsequent process can convert the potential energy of the charge-separated state into some “usable” form of energy. As seen from the reported examples, one of the important ways to achieve the long lived chargeseparated states of the artificial photosynthetic antenna-reaction center systems is to promote multistep electron-transfer reactions along well-define redox gradients [217–220,222,290]. In addition, the rates and efficiencies of the energy and electron transfers are greatly varied by changing the distance and orientation of the donor and acceptor entities [270,300,301], the solvents, and the linkers between the photoactive species [199–202,291,292]. In the supramolecular systems, different kind of non-covalent binding approaches were utilized including metal-ligand coordination [289–297], crown ether-cation complexation [321–324], and anion binding [361–363]. Compared with the “one-point” binding self-assembly [309,312,313], the “two point” binding


[296,310,324,361,363] can construct more stable supramolecular complexes with defined distance and orientation, and subsequent manipulation of the rates of energy-transfer and electron-transfer reactions by controlling the donor-acceptor interactions in different media. Despite such rapid progress in the semi-artificial and artificial photosynthetic systems in the last decade, it remains a significant challenge to construct more efficient artificial photosynthetic systems and devices capable of producing molecular fuels such as hydrogen and hydrogen peroxide at a scale and cost that can compete with fossil fuels. Acknowledgements This project was supported financially by the Science and Technology Development Fund (STDF, Egypt, Grant Nos. 5537 and 12436). S. Fukuzumi thanks JSPS KAKENHI (Grant no. 16H02268). S. Fukuzumi and M. E. El-Khouly would like to acknowledge Francis D’souza for a long term and fruitful collaboration. E. El-Mohsnawy also acknowledges M. Rögner for the long-term collaboration. References [1] R. Service, Science 309 (2005) 548–551. [2] N.S. Lewis, D.G. Nocera, Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 15729–15735. [3] V. Smil, Energy, Oxford, 2006. [4] N.S. Lewis, Science 315 (2007) 798–801. [5] Special section of sustainability and energy, Science 315 (2007) 781–813. [6] N.S. Lewis, MRS Bull. 32 (2007) 808–820. [7] N. Armaroli, V. Balzani, Angew. Chem. Int. Ed. 46 (2007) 52. [8] N. Armaroli, V. Balzani, Chem. Eur. J. 22 (2016) 32–57. [9] J. Deisenhofer, H. Michel, EMBO J. 8 (1989) 2149–2170. [10] Molecular Mechanisms of Photosynthesis, in: R.E. Blankenship (Ed.), Blackwell Science Ltd, Malden, MA, 2002. [11] J. Barber, Chem. Soc. Rev. 38 (2009) 185–196. [12] D.R. Ort, X. Zhu, A. Melis, Plant Physiol. 155 (2011) 79–85. [13] B. Ke, Photosynth. Res. 73 (2002) 207–214. [14] J. Whitmarsh, J. Govindjee, Concepts in Photobiology: Photosynthesis and Photomorphogenesis, Narosa Publishing House, New Dehli, India, 1999, pp. 11–51. [15] G. Ciamician, Science 36 (1912) 385–394. [16] Photochemical Conversion and Storage of Solar Energy, in: J.S. Connolly (Ed.), Academic, New York, 1981. [17] K. Maeda, K. Teramura, D.L. Lu, T. Takata, N. Saito, Y. Inoue, K. Domen, Energy Environ. Sci. 1 (2008) 15–31. [18] M. Hambourger, G.F. Moore, D.M. Kramer, D. Gust, A.L. Moore, T.A. Moore, Chem. Soc. Rev. 38 (2009) 25–35. [19] E. Fujita, J.T. Muckerman, Bull. Jpn. Soc. Coord. Chem. 51 (2008) 41–54. [20] D. Gust, T.A. Moore, Science 244 (1989) 35–41. [21] T.J. Meyer, Acc. Chem. Res. 22 (1989) 163–170. [22] M.R. Wasielewski, Chem. Rev. 92 (1992) 435–461. [23] M.A. Steffen, K. Lao, S.G. Boxer, Science 264 (1994) 810–816. [24] G.R. Fleming, R. van Grondelle, Curr. Opin. Struct. Biol. 7 (1997) 738–748. [25] A.J. Hoff, J. Deisenhofer, Phys. Rep. 287 (1997) 1–247. [26] L. Sun, L. Hammarström, B. A∀kermark, S. Styring, Chem. Soc. Rev. 30 (2001) 36–49. [27] Advances in photosynthesis, in: B. Ke (Ed.), Photosynthesis: Photochemistry and Photobiophysics, vol. 10, Kluwer Academic Publishers, UK, 2003. [28] W. Zinth, J. Wachtveitl, ChemPhysChem 6 (2005) 871–880. [29] G.J. Meyer, Inorg. Chem. 44 (2005) 6852–6864. [30] M.H.V. Huynh, D.M. Dattelbaum, T.J. Meyer, Coord. Chem. Rev. 249 (2005) 457–483. [31] R. Lomoth, A. Magnuson, M. Sjoedin, P. Huang, S. Styring, L. Hammarström, Photosynth. Res. 87 (2006) 25–40. [32] M.R. Wasielewski, J. Org. Chem. 71 (2006) 5051–5066. [33] C. Röger, M.G. Müller, M. Lysetska, Y. Miloslavina, A.R. Holzwarth, F. Würthner, J. Am. Chem. Soc. 128 (2006) 6542–6543. [34] A. Nantalaksakul, D.R. Reddy, C.J. Bardeen, S. Thayumanavan, Photosynth. Res. 87 (2006) 133–150. [35] W. Lubitz, E.J. Reijerse, J. Messinger, Energy Environ. Sci. 1 (2008) 15–31. [36] V. Balzani, A. Credi, M. Venturi, ChemSusChem 1 (2008) 26–58. [37] C.S. Mullins, V.L. Pecoraro, Coord. Chem. Rev. 252 (2008) 416–443. [38] L. Hammarström, S. Styring, R. Soc, Lond. B: Biol. Sci. 363 (2008) 1283–1291. [39] A.C. Benniston, A. Harriman, Mater. Today 11 (2008) 26–34. [40] M.R. Wasielewski, Acc. Chem. Res. 42 (2009) 1910–1921. [41] D. Gust, T.A. Moore, A.L. Moore, Acc. Chem. Res. 42 (2009) 1890–1898. [42] R. Berera, R. van Grondelle, J.T.M. Kennis, Photosynth. Res. 101 (2009) 105–118.

79

[43] P.E.M. Siegbahn, Acc. Chem. Res. 42 (2009) 1871–1880. [44] H. Dau, I. Zaharieva, Acc. Chem. Soc. 42 (2009) 1861–1870. [45] H. Dau, C. Limberg, T. Reier, M. Risch, S. Roggan, P. Strasser, ChemCatChem 2 (2010) 724–761. [46] I. McConnell, G. Li, G.W. Brudvig, Chem. Biol. Rev. 17 (2010) 434–447. [47] K. Kalyanasundaram, M. Grätzel, Curr. Opinion Biotech. 21 (2010) 298–310. [48] Y. Tachibana, L. Vayssieres, J.R. Durrant, Nat. Photonics 5 (2012) 511–518. [49] J.J. Concepcio, R.L. House, J.M. Papanikolas, T.J. Meyer, Proc. Natl. Acad. Sci. U.S.A. 109 (2012) 15560–15564. [50] D.G. Nocera, Acc. Chem. Res. 45 (2012) 767–776. [51] M. Wiechen, H.-M. Berends, P. Kurz, Dalton Trans. 41 (2012) 21–31. [52] Y. Tachibana, L. Vayssieres, J.R. Durrant, Nat. Photonics 6 (2012) 511–518. [53] S. Fukuzumi, K. Ohkubo, T. Suenobu, Acc. Chem. Res. 47 (2014) 1455–1464. [54] D. Kim, K.K. Sakimoto, D. Hong, P. Yang, Angew. Chem. Int. Ed. 54 (2015) 2–10. [55] M. Yamamoto, K. Tanaka, ChemPlusChem 81 (2016) 1028–1044. [56] N. Nelsen, Biochim. Biophys. Acta 1807 (2011) 856–863. [57] M.R. Jones, P.K. Fyfe, Curr. Biol. 17 (2001) R318–321. [58] G. Drews, J.F. Imhoff, Variations in Autotrophic Life, in: J.M. Shively, L.L. Barton (Eds.), Academic Press, London, San Diego, New York, Boston, Sydney, Tokyo, Toronto, 1991, pp. 51–97. [59] M. Teuber, M. Rögner, S. Berry, Biochim. Biophys. Acta 1506 (2001) 31–46. [60] J.M. Olson, Photosynth. Res. 68 (2001) 95–112. [61] M. Hohmann, R. Blankenship, Annu. Rev. Plant Biol. 62 (2011) 515–548. [62] A. Zouni, H.T. Witt, J. Kern, P. Fromme, N. Krauß, W. Saenger, P. Orth, Nature 409 (2001) 739–743. [63] K.N. Ferreira, T.M. Iverson, K. Maghlaoui, J. Barber, S. Iwata, Science 303 (2004) 1831–1838. [64] Y. Umena, K. Kawakami, J.-R. Shen, N. Kamiya, Nature 473 (2011) 55–60. [65] A. Ben-Shem, F. Frolow, N. Nelson, Nature 426 (2003) 630–635. [66] P. Fromme, P. Jordan, N. Krauß, Biochim. Biophys. Acta 1507 (2001) 5–31. [67] P. Jordan, P. Fromme, O. Klukas, H.T. Witt, W. Saenger, N. Krauß, Nature 411 (2001) 909–917. [68] P.R. Chitnis, Annu. Rev. Plant Physiol. Plant Mol. Biol. 52 (2001) 593–626. [69] N. Nelson, A. Ben-Shem, Nat. Rev. Mol. Cell. Biol. 5 (2004) 971–982. [70] I. Grotjohann, P. Fromme, Photosynth. Res. 85 (2005) 51–72. [71] C.C. Gradinaru, I.H.M. van Stokkum, A.A. Pascal, R. van Grondelle, J. Phys. Chem. B 104 (2000) 9330–9342. [72] R. Croce, M.G. Müller, R. Bassi, A.R. Holzwarth, Biophys. J. 80 (2001) 901–915. [73] D. Elard, K.K. Niyogi, A. Grossman, Plant Cell 14 (2002) 1801–1816. [74] Z. Liu, H. Yan, K. Wang, T. Kuang, J. Zhang, L. Gui, X. An, W. Chang, Nature 428 (2004) 287–292. [75] H.V. Scheller, P.E. Jensen, A. Haldrup, C. Lunde, J. Knoetzel, Biochim. Biophys. Acta 1507 (2001) 41–60. [76] A. Ben-Shem, F. Frolow, N. Nelson, FEBS Lett. 564 (2004) 274–280. [77] Y. Mazor, A. Borovikova, N. Nelson, eLife 4 (2015) e07433. [78] J. Biesiadka, B. Loll, J. Kern, K.D. Irrgang, A. Zouni, Phys. Chem. Chem. Phys. 6 (2004) 4733–4736. [79] A. Remy, J. Niklas, H. Kuhl, P. Kellers, T. Schott, M. Rögner, K. Gerwert, Eur. J. Biochem. 271 (2004) 563–567. [80] J. Kern, J. Biesiadka, B. Loll, W. Saenger, A. Zouni, Photosynth. Res. 92 (2007) 389–405. [81] C.W. Mullineaux, Biochim. Biophys. Acta 1184 (1994) 71–77. [82] M.G. Rakhimberdieva, V.A. Boichenko, N.V. Karapetyan, I.N. Stadnichuk, Biochemistry 40 (2001) 15780–15788. [83] J.J. van Thor, C.W. Mullineaux, H.C.P. Matthijs, K. Hellingwert, J. Botanica Acta 111 (1998) 430–443. [84] C.W. Mullineaux, M.J. Tobin, G.R. Jones, Nature 390 (1997) 421–424. [85] M. Sarcina, M. Tobin, C. Mullineaux, J. Biol. Chem. 276 (2001) 46830–46834. [86] S. Joshua, C. Mullineaux, Plant Physiol. 135 (2004) 2112–2119. [87] C. Mullineaux, J. Allen, Photosynth. Res. 22 (1990) 157–166. [88] D. Kirilovsky, R. Kana, O. Prasil, Dissipation In Plants, Algae and Cyanobacteria, vol. 40, Springer Netherlands, Dordrecht, 2014. [89] A. Guskov, J. Kern, A. Gabdulkhakov, M. Broser, A. Zouni, W. Saenger, Nat. Struct. Mol. Biol. 16 (2009) 334–342. [90] N. Kamiya, J.R. Shen, Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 98–103. [91] A.R. Holzwarth, M.G. Müller, M. Reus, M. Nowaczyk, J. Sander, M. Rögner, Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 6895–6900. [92] Y. Miloslavina, M. Szczepaniak, G. Müller, J. Sander, M. Nowaczyk, M. Rögner, A. Holzwarth, Biochemistry 45 (2006) 2436–2442. [93] M.M. Nowaczyk, R. Hebeler, E. Schlodder, H.E. Meyer, B. Warscheid, M. Rögner, Plant Cell 18 (2006) 3121–3131. [94] B.A. Diner, G.T. Babcock, Structure, dynamic and energy conversion efficiency in photosystem II, in: D. Ort, C.F. Yocum (Eds.), Oxygenic Photosynthesis: The Light Reactions, Kluwer, Dordrecht, The Netherlands, 1996, p. 213. [95] B.A. Diner, F. Rappaport, Annu. Rev. Plant Biol. 53 (2002) 551–580. [96] A. Cuni, L. Xiong, R. Sayre, F. Rappaport, J. Lavergne, Phys. Chem. Chem. Phys. 6 (2004) 4825–4831. [97] C. Tommos, G.T. Babcock, Biochim. Biophys. Acta 1458 (2000) 199–219. [98] J. Nield, K. Redding, M. Hippler, Eukaryot. Cell 3 (2004) 1370–1380. [99] A. Cuni, L. Xiong, R. Sayre, F. Rappaport, J. Lavergne, Phys. Chem. Chem. Phys. 6 (2004) 4825–4831. [100] N. Nelson, F.C. Yocum, Annu. Rev. Plant Biol. 57 (2006) 521–565. [101] C.M. Christopher, C.P. Christopher, P.D. Leslie, Photochem. Photobiol. Sci. 4 (2005) 933–939.

80


[102] M. Szczepaniak, J. Sander, M. Nowaczyk, M.G. Müller, M. Rögner, A.R. Holzwarth, Biophys. J. 96 (2009) 621–631. [103] X.M. Gong, R. Agalarov, K. Brettel, C. Carmeli, J. Biol. Chem. 278 (2003) 19141–19150. [104] E. El-Mohsnawy, M.J. Kopczak, E. Schlodder, M. Nowaczyk, H.E. Meyer, B. Warscheid, N.V. Karapetyan, M. Rögner, Biochemistry 49 (2010) 4740–4751. [105] M.K. S¸ener, S. Park, D. Lu, A. Damjanovic, T. Ritz, P. Fromme, K. Schulten, J. Chem. Phys. 120 (2004) 11183–11195. [106] M.K. S¸ener, C. Jolley, A. Ben-Shem, P. Fromme, N. Nelson, R. Croce, K. Schulten, Biophys. J. 89 (2005) 1630–1642. [107] P. Fromme, A. Melkozernov, P. Jordan, N. Krauß, FEBS Lett. 555 (2003) 40–44. [108] F. Klimmek, U. Ganeteg, J.A. Ihalainen, H. van Roon, P.E. Jensen, H.V. Scheller, J.P. Dekker, S. Jansson, Biochemistry 44 (2005) 3065–3073. [109] E.J. Boekema, A. Hifney, A.E. Yakushevska, M. Piotrowski, W. Keegstra, S. Berry, K.P. Michel, E.K. Pistorius, J. Kruip, Nature 412 (2001) 745–748. [110] R. Kouril, N. van Oosterwijk, A.E. Yakushevska, E.J. Boekema, Photochem. Photobiol. Sci. 4 (2005) 1091–1094. [111] A.R. Holzwarth, M.G. Müller, J. Niklas, W. Lubitz, J. Phys. Chem. B 109 (2005) 5903–5911. [112] M.T. Zeng, X.M. Gong, M.C. Evans, N. Nelson, C. Carmeli, Biochim. Biophys. Acta 1556 (2002) 254–264. [113] N.V. Karapetyan, Biofizika 49 (2004) 212–226. [114] N.V. Karapetyan, A.R. Holzwarth, M. Rogner, FEBS Lett. 460 (1999) 395–400. [115] B. Ke, Biochim. Bio. Phys. Acta 301 (1973) 1–33. [116] M. Medina, FEBS J. 276 (2009) 3942–3958. [117] S. Santabarbara, P. Heathcote, M.C.W. Evans, Biochim. Biophys. Acta Bioenerg. 1708 (2005) 283–310. [118] A.Y. Semenov, S.K. Chamorovsky, M.D. Mamedov, Biofizika 49 (2004) 227–238. [119] P. Setif, Biochim. Biophys. Acta Bioenerg. 1507 (2001) 161–179. [120] K. Nguyen, B.D. Bruce, Biochim. Biophys. Acta Bioenerg. 1837 (2014) 1553–1566. [121] J. Barber, D. Phong, J.R. Tran, Soc. Interface 10 (2013) 98410. [122] R.E. Blankenship, Molecular Mechanism of Photosynthesis, Blackwell Science, Oxford, UK, 2002. [123] J.W. Lengeler, G. Drews, H.G. Schlegel, Biology of the Prokaryotes, Thieme-Verlag, Stuttgart, Distributed in the USA by Blackwell Science, 1999. [124] D. Heinecke, Encyclopedia of Life Sciences, Nature Publishing group, London, 2001, pp. 1–4. [125] K.P. Michel, Habilitation, Universität Bielefeld, 2003. [126] U. Eberle, B. Mueller, R. von Helmolt, Energy Environ. Sci. 5 (2012) 8780–8798. [127] N. Khanna, P. Lindblad, Int. J. Mol. Sci. 16 (2015) 10537–10561. [128] D.S. Horner, B. Heil, T. Happe, T.M. Embley, Trends Biochem. Sci. 27 (2002) 148–153. [129] R.C. Prince, H.S. Kheshgi, Critical Rev. Microbiol. 31 (2005) 19–31. [130] B. Esper, A. Badura, M. Rögner, Trends Plant Sci. 11 (2006) 543–547. [131] J. Appel, R. Schulz, J. Photochem. Photobiol. B 47 (1998) 1–11. [132] K. Schutz, T. Happe, O. Troshina, P. Lindblad, E. Leitao, P. Oliveira, P. Tamagnini, Planta 218 (2004) 350–359. [133] A. Parkin, in: P.M.H. Kroneck, M.E.S. Torres (Eds.), Understanding and Harnessing Hydrogenases, Biological Dihydrogen Catalysts, vol. 14, Met. Ions Life Sci., 2014, pp. 99–124. [134] H. Bothe, O. Schmitz, M.G. Yates, W.E. Newton, Mol. Biol. Rev. 74 (2010) 529–551. [135] A. Volbeda, L. Martin, P.P. Liebgott, A.L. de Lacey, J.C. Fontecilla-Camps, Metallomics 7 (2015) 710–718. [136] P. Constant, S. Chowdhury, L. Hesse, J. Pratscher, R. Conrad, Appl. Environ. Microbiol. 77 (2011) 6027–6035. [137] W. Lubitz, H. Ogata, O. Rüdiger, E. Reijerse, Chem. Rev. 114 (2014) 4081–4148. [138] C.S.A. Baltazar, M.C. Marques, C.M. Soares, A.M. DeLacey, I.A.C. Pereira, P.M. Matias, Chem.2011, Eur. J. Inorg. Chem. (2011) 948–962. [139] A. Parkin, G. Goldet, C. Cavazza, J.C. Fontecilla-Camps, F.A. Armstrong, J. Am. Chem. Soc. 130 (2008) 13410–13416. [140] T. Sakai, D. Mersch, E. Reisner, Angew. Chem. Int. Ed. 52 (2013) 12313–12316. [141] S.T. Stripp, G. Goldet, C. Brandmayr, O. Sanganas, K.A. Vincent, M. Haumann, F.A. Armstrong, T. Happe, Proc. Natl. Acad. Sci. U.S.A. 106 (2009) 17331–17336. [142] R.K. Thauer, A.K. Kaster, M. Goenrich, M. Schick, T. Hiromoto, S. Shima, Annu. Rev. Biochem. 79 (2010) 507–536. [143] H. Tamura, M. Salomone-Stagni, T. Fujishiro, E. Warkentin, E. Meyer-Klaucke, U. Ermler, S. Shima, Angew. Chem. Int. Ed. 52 (2013) 9656–9659. [144] G.J. Kubas, Chem. Rev. 107 (2007) 4152–4205. [145] Y.A. Small, D.L. DuBois, E. Fujita, J.T. Muckerman, Energy Environ. Sci. 4 (2011) 3008–3020. [146] R.M. Bullock, A.M. Appel, M.L. Helm, Chem. Commun. 50 (2014) 3125–3143. [147] G. Berggren, A. Adamska, C. Lambertz, T.R. Simmons, J. Esselborn, M. Atta, S. Gambarelli, J.M. Mouesca, E. Reijerse, W. Lubitz, T. Happe, V. Artero, M. Fontecave, Nature 499 (2013) 66–69. [148] A. Melis, Int. J. Hydrogen Energy 27 (2002) 1217–1228. [149] T. Happe, A. Kaminski, Eur. J. Biochem. 269 (2002) 1022–1032. [150] L. Girbal, G. von Abendroth, M. Winkler, P.M.C. Benton, I. Meynial-Salles, C. Croux, I.W. Peters, T. Happe, P. Soucaille, Appl. Environ. Microbiol. 71 (2005) 2777–2781.

[151] A. Melis, Int. J. Hydrogen Energy 27 (2002) 1217–1228. [152] O. Kruse, J. Rupprecht, J.H. Mussgnug, G.C. Dismukes, B. Hankamer, Photochem. Photobiol. Sci. 12 (2005) 957–970. [153] A. Melis, A. Murakami, J.A. Nemson, K. Aizawa, K. Ohki, Y. Fujita, Photosynth. Res. 47 (1996) 253–265. [154] J.E.W. Polle, S. Kanakagiri, E. Jin, T. Masuda, A. Melis, Int. J. Hydrogen Energy 27 (2002) 1257–1264. [155] M. Seibert, T. Flynn, M.L. Ghirardi, Biohydrogen II, in: J. Miyake (Ed.), Elsevier Science, 2001, pp. 67–77. [156] Y. Asada, Y. Koike, J. Schnackenberg, M. Miyake, L. Uemura, J. Miyake, Biochim. Biophys. Acta 1490 (2000) 269–278. [157] K.A. Vincent, J.A. Cracknell, O. Lenz, I. Zebger, B. Friedrich, F.A. Armstrong, Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 16951–16954. [158] A. Schwarze, M. Kopczak, M. Rögner, O. Lenz, Appl. Environ. Microbiol. 76 (2010) 2641–2651. [159] J.R.J. Benemann, Appl. Phycol. 12 (2000) 291–300. [160] A. Melis, M. Seibert, T. Happe, Photosynth. Res. 82 (2004) 277–288. [161] I. Yacoby, S. Pochekailov, H. Toporik, M.L. Ghirardi, P.W. King, S. Zhang, Proc. Natl. Acad. Sci. U.S.A. 108 (2011) 9396–9401. [162] W. Haehnel, H.J. Hochheimer, Bioelectrochem. Bioenerg. 6 (1979) 563–574. [163] W. Schuhmann, H.P. Josel, H. Parlar, Angew. Chem. 99 (1987) 264–266, Angew. Chem. Int. Ed. 26 (1987) 241–243. [164] T. Kothe, N. Plumer, A. Badura, M.M. Nowaczyk, D.A. Guschin, M. Rögner, W. Schuhmann, Angew. Chem. Int. Ed. 52 (2013) 14233–14236. [165] A. Badura, D. Guschin, T. Kothe, M. Kopczak, W. Schuhmann, M. Rögner, Energy. Environ. Sci. 4 (2011) 2435–2440. [166] N. Terasaki, N. Yamamoto, T. Hiraga, Y. Yamanoi, T. Yonezawa, H. Nishihara, T. Ohmori, M. Sakai, M. Fujii, A. Tohri, M. Iwai, I. Enami, Y. Inoue, S. Yoneyama, M. Minakata, Angew. Chem. Int. Ed. 48 (2009) 1585–1587. [167] A. Prodöh, M. Ambill, E. El-Mohsnawy, J. Lax, M. Nowaczyk, R. Oworah-Nkruma, T. Volkmer, S.-O. Wenk, M. Rögner, Biohydrogen III, in: J. Miyake, Y. Igarashi, M. Roegner (Eds.), Elsevier, Oxford, 2004, pp. 171–179. [168] E. El-Mohsnawy, PhD. Thesis, Ruhr University Bochum, 2007, pp. 112–115. [169] V. Hartmann, T. Kothe, S. Pöller, E. El-Mohsnawy, M. Nowaczyk, N. Plumeré, W. Schuhmann, M. Rögner, Phys. Chem. Chem. Phys. 16 (2014) 11936–11941. [170] M. Ihara, H. Nishihara, K.-S. Yoon, O. Lenz, B. Friedrich, H. Nakamoto, K. Kojima, D. Honma, T. Kamachi, I. Okura, Photochem. Photobiol. 82 (2006) 676–682. [171] C.E. Lubner, A.M. Applegate, P. Knörzer, A. Ganago, D.A. Bryant, T. Happe, J.H. Golbecka, Proc. Natl. Acad. Sci. U. S. A. 108 (2011) 20988–20991. [172] B.J. Harris, X.L. Cheng, P. Frymier, J. Phys. Chem. B 120 (2016) 599–609. [173] A.M. Applegate, C.E. Lubner, P. Knorzer, T. Happe, J.H. Golbeck, Photosynth. Res. 127 (2016) 5–11. [174] K. Ocakoglu, T. Krupnik, B. van den Bosch, E. Harputlu, M. Pia Gullo, J.D.J. Olmos, S. Yildirimcan, R.K. Gupta, F. Yakuphanoglu, A. Barbieri, J.N.H. Reek, J. Kargul, Adv. Funct. Mater. 24 (2014) 7467–7477. [175] J.H. Golbeck, Photosynthetic Reaction Centers, Biophysical Society, Bethesda MD, 2004. [176] C.C. Moser, C.C. Page, R.J. Cogdell, J. Barber, C.A. Wraight, Adv. Protein Chem., in: C.R. Douglas (Ed.), Academic Press, 2003, pp. 71–109. [177] A. Fujishima, K. Honda, Nature 238 (1972) 37–38. [178] G.R. Bamwenda, S. Tsubota, T. Nakamura, M. Haruta, J. Photochem. Photobiol. A 89 (1995) 177–189. [179] E. Greenbaum, Science 230 (1985) 1373–1375. [180] E. Greenbaum, J. Phys. Chem. 92 (1988) 4571–4574. [181] S. Fukuzumi, Curr. Opin. Chem. Biol. 25 (2015) 18–26. [182] N. Terasaki, N. Yamamoto, T. Hiraga, I. Sato, Y. Inoue, S. Yamada, Thin Solid Films 499 (2006) 153–156. [183] N. Terasaki, N. Yamamoto, M. Hattori, N. Tanigaki, T. Hiraga, K. Ito, M. Konno, M. Iwai, Y. Inoue, S. Uno, K. Nakazato, Langmuir 25 (2009) 11969–11974. [184] G. Le Blanc, G. Chen, E.A. Gizzie, G.K. Jennings, D.E. Cliffel, Adv. Mater. 24 (2012) 5959–5962. [185] L. Frolov, Y. Rosenwaks, C. Carmeli, I. Carmeli, Adv. Mater. 17 (2005) 2434–2437. [186] A. Mershin, K. Matsumoto, L. Kaiser, D. Yu, M. Vaughn, M.K. Nazeeruddin, B.D. Bruce, M. Graetzel, S.G. Zhang, Sci. Rep. 2 (2012) 234–241. [187] V. Balzani, A. Juris, M. Venturi, S. Campagna, S. Serroni, Chem. Rev. 96 (1996) 759–834. [188] Y. Terazono, G. Kodis, K. Bhushan, J. Zaks, C. Madden, A.L. Moore, T.A. Moore, G.R. Fleming, D. Gust, J. Am. Chem. Soc. 133 (2011) 2916–2922. [189] M.E. El-Khouly, S. Fukuzumi, F. D’souza, ChemPhysChem 15 (2014) 30–47. [190] S. Fukuzumi, Bull. Chem. Soc. Jpn. 79 (2006) 177–195. [191] S. Fukuzumi, T. Kojima, J. Mater. Chem. 18 (2008) 1427–1439. [192] S. Fukuzumi, Phys. Chem. Chem. Phys. 10 (2008) 2283–2297. [193] F. D’souza, O. Ito, Chem. Soc. Rev. 41 (2012) 86–96. [194] S. Fukuzumi, T. Honda, K. Ohkubo, T. Kojima, Dalton Trans. (2009) 3880–3889. [195] M.E. El-Khouly, Y. Chen, X. Zhuang, S. Fukuzumi, J. Am. Chem. Soc. 131 (2009) 6370–6371. [196] S. Fukuzumi, K. Ohkubo, Dalton Trans. 42 (2013) 15846–15858. [197] S.-H. Lee, I.M. Blake, A.G. Larsen, J.A. McDonald, K. Ohkubo, S. Fukuzumi, J.R. Reimers, M.J. Crossley, Chem. Sci. 7 (2016) 6534–6550. [198] H. Imahori, S. Fukuzumi, Adv. Funct. Mater. 14 (2004) 525–536. [199] M. Rudolf, S.V. Kirner, D.M. Guldi, Chem. Soc. Rev. 45 (2016) 612–630.

M.E. El-Khouly et al. / Journal of Photochemistry and Photobiology C: Photochemistry Reviews 31 (2017) 36–83 [200] Multiporphyrin Arrays: Fundamentals and Applications, in: D. Kim (Ed.), CRC Press, NW, 2012. [201] Y. Ding, W.-H. Zhu, Y. Xie, Chem. Rev. (2016), http://dx.doi.org/10.1021/acs. chemrev.6b00021. [202] T. Tanaka, A. Osuka, Chem. Soc. Rev. 44 (2015) 943–969. [203] A. Tsuda, A. Osuka, Science 293 (2001) 79–82. [204] M. Urban, M. Grätzel, M.K. Nazeeruddin, T. Torres, Chem. Rev. 114 (2014) 12330–12396. [205] M.K. Panda, K. Labomenou, A.G. Coutsolelos, Coord. Chem. Rev. 256 (2012) 2601–2627. [206] H.W. Kroto, J.R. Heath, S.C. O‘Brien, R.F. Curl, R.E. Smalley, Nature 318 (1985) 162–163. [207] S. Fukuzumi, H. Imahori, H. Yamada, M.E. El-Khouly, M. Fujitsuka, O. Ito, D.M. Guldi, J. Am. Chem. Soc. 123 (2001) 2571–2575. [208] H. Imahori, M.E. El-Khouly, M. Fujitsuka, O. Ito, Y. Sakata, S. Fukuzumi, J. Phys. Chem. A 105 (2001) 325–332. [209] Fullerenes: From Synthesis to Optical Properties, in: D.M. Guldi, N. Martin (Eds.), Kluwer Academic Publishers, 2002. [210] H. Imahori, Y. Mori, J. Matano, J. Photochem. Photobiol. C 4 (2003) 51–83. [211] M.E. El-Khouly, O. Ito, P.M. Smith, F. D’souza, J. Photochem. Photobiol. C 5 (2004) 79–104. [212] Fullerenes and Other Carbon Rich Nanostructures, in: J.-F. Nierengarten (Ed.), Springer-Verlag, Berlin Heidelberg, 2014. [213] P.A. Liddell, J.P. Sumida, A.N. Macpherson, L. Noss, G.R. Seely, K.N. Clark, A.L. Moore, T.A. Moore, D. Gust, Photochem. Photobiol. 60 (1994) 537–541. [214] D. Kuciauskas, S. Lin, G.R. Seely, A.L. Moore, T.A. Moore, D. Gust, T. Drovetskaya, C.A. Reed, P.D.W. Boyd, J. Phys. Chem. 100 (1996) 15926–15932. [215] F. D’souza, S. Gadde, M.E. Zandler, K. Arkady, M.E. El-Khouly, M. Fujitsuka, J. Phys. Chem. A 106 (2002) 12393–12404. [216] M.E. El-Khouly, Y. Araki, O. Ito, S. Gadde, A.L. McCarty, P.A. Karr, M.E. Zandler, F. D’souza, Phys. Chem. Chem. Phys. 7 (2005) 3163–3171. [217] P.A. Liddell, D. Kuciauskas, J.P. Sumida, B. Nash, D. Nguyen, A.L. Moore, T.A. Moore, D. Gust, J. Am. Chem. Soc. 119 (1997) 1400–1405. [218] C. Luo, D.M. Guldi, H. Imahori, K. Tamaki, Y. Sakata, J. Am. Chem. Soc. 122 (2000) 6535–6551. [219] H. Imahori, D.M. Guldi, K. Tamaki, Y. Yoshida, C. Luo, Y. Sakata, S. Fukuzumi, J. Am. Chem. Soc. 123 (2001) 6617–6628. [220] G. Kodis, P.A. Liddell, L. de la Garza, P.C. Clausen, J.S. Lindsey, A.L. Moore, T.A. Moore, D. Gust, J. Phys. Chem. A 106 (2002) 2036–2048. [221] J.-Y. Liu, M.E. El-Khouly, S. Fukuzumi, D.K.P. Ng, Chem. Eur. J. 17 (2011) 1605–1613. [222] C.A. Wijesinghe, M.E. El-Khouly, M.E. Zandler, S. Fukuzumi, F. D’souza, Chem. Eur. J. 19 (2013) 9629–9638. [223] F. D’souza, S. Gadde, D.-M.S. Islam, C.A. Wijesinghe, A.L. Schumacher, M.E. Zandler, Y. Araki, O. Ito, J. Phys. Chem. A 111 (2007) 8552–8560. [224] G. De la Torre, T. Torres, F. Agulló-López, Adv. Mater. 9 (1997) 265–269. [225] M. Hanack, H. Heckman, R. Polley, in: E. Schauman (Ed.), Methods in Organic Chemistry, vol. E 94, Georg Thieme Verlag, Stuttgart, 1998, p. 717. [226] R.A. Kipp, J.A. Simon, M. Beggs, H.E. Ensley, R.H. Schmehl, J. Phys. Chem. A 102 (1998) 5659–5664. [227] N. Kobayashi, T. Ishizaki, K. Ishii, H. Konami, J. Am. Chem. Soc. 121 (1999) 9096–9110. [228] S.H. Kang, Y.S. Kang, W.C. Zin, G. Olbrechts, K. Wostyn, K. Clays, A. Persoons, K. Kim, Chem. Commun (1999) 1661–1662. [229] C.G. Claessens, T. Torres, Tetrahedron Lett. 41 (2000) 6361–6365. [230] N. Kobayashi, Bull. Chem. Soc. Jpn. 75 (2002) 1–19. [231] T. Torres, Angew. Chem. Int. Ed. 45 (2006) 2834–2837. ˜ [232] J. Guilleme, L.M. Fernández, D. Gonzalez-Rodríguez, I. Corral, M. Yánez, T. Torres, J. Am. Chem. Soc. 136 (2014) 14289–14298. [233] Á. Sastre-Santos, T. Torres, M.A. Diaz-Garcia, F. Agulló-López, C. Dhenaut, S. Brasselet, I. Ledoux, J. Zyss, J. Am. Chem. Soc. 118 (1996) 2746–2747. [234] B. del Rey, U. Keller, T. Torres, G. Rojo, F. Agulló-López, S. Nonell, C. Martín, S. Brasselet, I. Ledoux, J. Zyss, J. Am. Chem. Soc. 120 (1998) 12808–12817. [235] M. Trelka, A. Medina, D. Écija, C. Urban, O. Gröning, R. Fasel, J.M. Gallego, C.G. Claessens, R. Otero, T. Torres, R. Miranda, Chem. Commun. 47 (2011) 9986–9988. [236] C.G. Claessens, D. Gonzalez-Rodríguez, M.S. Rodriguez-Morgade, A. Medina, T. Torres, Chem. Rev. 114 (2014) 2192–2227. [237] G. Zango, J. Zirzimerier, C.G. Classens, T. Clark, M.V. Martinez, D.M. Guldi, T. Torres, Chem. Sci. 6 (2015) 5571–5577. [238] S. Nakano, Y. Kage, H. Furuta, N. Kobayashi, S. Shimizu, Chem. Eur. J. 22 (2016) 7706–7710. [239] M. Shi, J. Mack, X. Wang, Z. Shen, J. Mater. Chem. C 4 (2016) 7783–7789. [240] J.-H. Kim, M.E. El-Khouly, Y. Araki, O. Ito, K.-Y. Kay, Chem. Lett. 37 (2008) 544–545. [241] M.E. El-Khouly, D.K. Ju, K.-Y. Kay, F. D’souza, S. Fukuzumi, Chem. Eur. J. 16 (2010) 6193–6202. [242] D. Gonález-Rodríguez, T. Torres, M.M. Olmstead, J. Rivera, M.Á. Herranz, L. Echegoyen, C.A. Castellanos, D.M. Guldi, J. Am. Chem. Soc. 128 (2006) 10680–10681. [243] M.E. El-Khouly, S.H. Shim, Y. Araki, O. Ito, K.-Y. Kay, J. Phys. Chem. B 112 (2008) 3910–3917. [244] M.E. El-Khouly, J.-H. Kim, J.-H. Kim, K.-Y. Kay, S. Fukuzumi, J. Phys. Chem. C 116 (2012) 19709–19717.

81

[245] M.E. El-Khouly, J.B. Ryu, K.-Y. Kay, O. Ito, S. Fukuzumi, J. Phys. Chem. C 113 (2009) 15444–15453. [246] R.A. Marcus, Angew. Chem. Int. Ed. 32 (1993) 1111–1121. [247] A. Treibs, F.H. Kruzer, Justus Liebigs Ann. Chem. 718 (1968) 208–223. [248] T.G. Pavlopoulos, M. Shah, J.H. Boyer, Appl. Opt. 27 (1988) 4998–4999. [249] M. Shah, K. Thangaraj, M.-L. Soong, L.T. Wolford, J.H. Boyer, I.R. Politzer, T.G. Pavlopoulos, Heteroatom Chem. 1 (1990) 389–399. [250] T.G. Pavlopoulos, J.H. Boyer, M. Shah, K. Thangaraj, M.-L. Soong, Appl. Opt. 29 (1990) 3885–3886. [251] J. Karolin, L.B.-A. Johansson, L. Strandberg, T. Ny, J. Am. Chem. Soc. 116 (1994) 7801–7806. [252] F. López Arbeloa, T. López Arbeloa, I. López Arbeloa, I. García-Moreno, A. Costela, R. Sastre, F. Amat-Guerri, Chem. Phys. 236 (1998) 331–341. [253] F. López Arbeloa, J.B. Prieto, I.L. Arbeloa, A. Costela, I. García-Moreno, C. Gómez, F. Amat-Guerri, M. Liras, R. Sastre, Photochem. Photobiol. 78 (2003) 30–36. [254] R.Y. Lai, A.J. Bard, J. Phys. Chem. B 107 (2003) 5036–5042. [255] Z. Shen, H. Röhr, K. Rurack, H. Uno, M. Spieles, B. Schulz, G. Reck, N. Ono, Chem. Eur. J. 10 (2004) 4853–4871. [256] W. Qin, M. Baruah, M. van der Auweraer, F.C. De Schryver, N. Boens, J. Phys. Chem. A 109 (2005) 7371–7384. [257] A.D. Quartorolo, N. Russo, E. Sicilia, Chem. Eur. J. 12 (2006) 6797–6803. [258] S. Badré, V. Monnier, R. Méallet-Renault, C. Dumas-Verdes, E.Y. Schmidt, B.A. Trofimov, R.B. Pansu, J. Photochem. Photobiol. A 183 (2006) 238–246. [259] A. Cui, X. Peng, J. Fan, X. Chen, Y. Wu, B. Guo, J. Photochem. Photobiol. A 186 (2007) 85–92. [260] C.A. Wijesinghe, M.E. El-Khouly, J.D. Blakemore, M.E. Zandler, S. Fukuzumi, F. D’souza, Chem. Commun. 46 (2010) 3301–3303. [261] A. Loudet, K. Burgess, Chem. Rev. 107 (2007) 4891–4932. [262] G. Hu, R. Liu, E.J. Alexy, A.K. Manadal, D.F. Bocian, D. Holten, J.S. Lindsey, New J. Chem. 40 (2016) 8032–8052. [263] J.Y. Liu, M.E. El-Khouly, S. Fukuzumi, D.K.P. Ng, Chem. Asian J. 6 (2011) 174–179. [264] F. Li, S.I. Yang, T. Ciringh, J. Seth, C.H. Martin, D.L. Singh, D. Kim, R.R. Birge, D.F. Bocian, D. Holten, J.S. Lindsey, J. Am. Chem. Soc. 120 (1998) 10001–10017. [265] A. Gorman, J. Killoran, C. O’shea, T. Kenna, W.M. Gallagher, D.F. O’shea, J. Am. Chem. Soc. 106 (2004) 10619–10631. [266] M.J. Hall, S.O. McDonnell, J. Killoran, D.F. O’shea, J. Org. Chem. 70 (2005) 5571–5578. [267] A. Loudet, K. Burgess, Chem. Rev. 107 (2007) 4891–4932. [268] A. Palma, M. Tasior, D.O. Frimannsson, T.T. Vu, R. Meallet-Renault, D.F. Meallet-O’shea, Org. Lett. 11 (2009) 3638–3641. [269] P.A. Bouit, K. Kamada, P. Feneyrou, G. Berginc, L. Toupet, O. Maury, C. Andraud, Adv. Mater. 21 (2009) 1151–1154. [270] M. Yuan, X. Yin, H. Zheng, C. Ouyang, Z. Zuo, H. Liu, Y. Li, Chem. Asian J. 4 (2009) 707–713. [271] J. Murtagh, D.O. Frimannsson, D.F. O’shea, Org. Lett. 11 (2009) 5386–5389. [272] K. Flavin, K. Lawrence, J. Bartelmess, M. Tasior, C. Navio, C. Bittencourt, D.F. O’shea, D.M. Guldi, S. Giordani, ACS Nano 5 (2011) 1198–1206. [273] S.Y. Leblebici, L. Catane, D.E. Barclay, T. Olson, T.L. Chen, B. Ma, ACS Appl. Mater. Interfaces 3 (2011) 4469–4474. [274] M. Grossi, A. Palma, S.O. McDonnell, M.J. Hall, D.K. Rai, J. Muldoon, D.F. O’shea, J. Org. Chem. 77 (2012) 9304–9312. [275] K. Flavin, I. Kopfa, J. Murtagh, M. Grossi, D.F. O’shea, S. Giordani, Supramol. Chem. 24 (2012) 23–28. [276] T. Shiragami, K. Tanaka, Y. Andou, S.I. Tsunami, J. Matsumoto, H. Luo, Y. Araki, O. Ito, H. Inoue, M. Yasuda, J. Phtochem. Photobiol. A 170 (2005) 287–297. [277] M.E. El-Khouly, C. Göl, M.M. El-Hendawy, S. Yes¸ilot, M. Durmus¸, J. Porphyrins Phthalocyanines 19 (2015) 261–269. [278] M. Deniz, O. Altan Bozdemir, E.U. Akkaya, Org. Lett. 8 (2006) 2871–2873. [279] R. Ziessel, G. Ulrich, A. Haefele, A. Harriman, J. Am. Chem. Soc. 135 (2013) 11330–11344. [280] M.E. El-Khouly, A.N. Amin, M.E. Zandler, S. Fukuzumi, F. D’souza, Chem. Eur. J. 18 (2012) 5239–5247. [281] V. Bandi, K. Ohkubo, S. Fukuzumi, F. D’souza, Chem. Commun. 49 (2013) 2867–2869. [282] W.-J. Shi, M.E. El-Khouly, K. Ohkubo, S. Fukuzumi, D.K.P. Ng, Chem. Eur. J. 19 (2013) 11332–11341. [283] A. Eggenspiller, A. Takai, M.E. El-Khouly, K. Ohkubo, C.P. Gros, C. Bernhard, C. Goze, F. Denat, J.-M. Barbe, S. Fukuzumi, J. Phys. Chem. A 116 (2012) 3889–3898. [284] R. Chitta, Master Thesis, University of Hyderabed, 2002. [285] J.M. Lehn, Angew. Chem. Int. Ed. 29 (1990) 1304–1319. [286] J.M. Lehn, Science 260 (1993) 1762–1763. ¯ [287] M.M. Safont-Sempere, G. Fernandez, F. Würthner, Chem. Rev. 111 (2011) 5784–5814. [288] C.B. KC, F. D’souza, Coord. Chem. Rev. 322 (2016) 104–141. [289] F. D’souza, G.R. Deviprasad, M.E. Zandler, V.T. Hoang, A. Klykov, M. VanStipdonk, A. Perera, M.E. El-Khouly, M. Fujitsuka, O. Ito, J. Phys. Chem. A 106 (2002) 3243–3252. [290] F. D’souza, P.M. Smith, S. Gadde, A.L. McCarty, M.J. Kullman, M.E. Zandler, M. Itou, Y. Araki, O. Ito, J. Phys. Chem. B 108 (2004) 11333–11343. [291] F. D’souza, G.R. Deviprasad, M.E. El-Khouly, M. Fujitsuka, O. Ito, J. Am. Chem. Soc. 123 (2001) 5277–5284.

82


[292] F. D’souza, M.E. El-Khouly, S. Gadde, A.L. McCarty, P.A. Karr, M.E. Zandler, Y. Araki, O. Ito, J. Phys. Chem. B 109 (2005) 10107–10114. [293] J. Otsuki, A. Suka, K. Yamazaki, H. Abe, Y. Araki, O. Ito, Chem. Commun (2004) 1290–1291. [294] F. D’souza, P.M. Smith, M.E. Zandler, A.L. McCarty, M. Itou, Y. Araki, O. Ito, J. Am. Chem. Soc. 126 (2004) 7898–7907. [295] Y. Rio, W. Seitz, A. Gouloumis, P. Vázquez, J.L. Sessler, D.M. Guldi, T. Torres, Chem. Eur. J. 16 (2010) 1929–1940. [296] F. D’souza, A.N. Amin, M.E. El-Khouly, N.K. Subbaiyan, M.E. Zandler, S. Fukuzumi, J. Am. Chem. Soc. 134 (2012) 654–664. [297] V. Garg, G. Kodis, P.A. Liddell, Y. Terazono, T.A. Moore, A.L. Moore, D. Gust, J. Phys. Chem. B 17 (2013) 11299–11308. [298] N. Kobayashi, Coord. Chem. Rev. 227 (2002) 129–252. [299] N. Kobayashi, T. Ishizaki, K. Ishii, H. Konami, J. Am. Chem. Soc. 121 (1999) 9096–9110. [300] H.S. Nalwa, M. Hanack, G. Pawlowski, M.K. Engel, Chem. Phys. 245 (1999) 17–26. [301] D. Dini, M. Barthel, M. Hanack, Eur. J. Org. Chem (2001) 3759–3769. [302] Y. Chen, S. O’Flaherty, M. Fujitsuka, M. Hanack, L.R. Subramanian, O. Ito, W.J. Blau, Chem. Mater. 14 (2002) 5163–5168. [303] N. Kobayashi, H. Miwa, V.N. Nemykin, J. Am. Chem. Soc. 124 (2002) 8007–8020. [304] N. Kobayashi, J. Mack, K. Ishii, M. Stillman, J. Inorg. Chem. 41 (2002) 5350–5363. [305] X. Zhang, Y. Zhang, J. Jiang, J. Molecular Structure 673 (2004) 103–108. [306] L. Macor, F. Fungo, T. Tempesti, E.N. Durantini, L. Otero, E.M. Barea, F. Fabregat-Santiagob, J. Bisquert, Energy Environ. Sci. 2 (2009) 529–534. [307] K. Ishii, Coord. Chem. Rev. 256 (2012) 1556–1568. [308] A. Takeda, T. Oku, A. Suzuki, T. Akiyama, Y. Yamasaki, Synth. Met. 177 (2013) 48–51. [309] M.E. El-Khouly, L.M. Rogers, M.E. Zandler, G. Suresh, M. Fujitsuka, O. Ito, F. D’souza, ChemPysChem 4 (2003) 474–481. [310] M.E. El-Khouly, S. Gadde, G.R. Deviprasad, M. Fujitsuka, O. Ito, F. D’souza, J. Porphyrins Phthalocyanines 7 (2003) 1–7. [311] M.E. El-Khouly, Y. Araki, O. Ito, S. Gadde, M.E. Zandler, F. D’souza, J. Porphyrins Phthalocyanines 10 (2006) 1156–1164. [312] M.E. El-Khouly, Phys. Chem. Chem. Phys. 12 (2010) 12746–12752. [313] M.E. El-Khouly, A.M. Gutiérrez, Á. Sastre-Santos, F. Fern˘andez-L˘azaro, S. Fukuzumi, Phys. Chem. Chem. Phys. 14 (2012) 3612–3621. [314] M.E. El-Khouly, A.G. Moiseev, A. van der Est, S. Fukuzumi, ChemPhysChem 13 (2012) 1191–1198. [315] C. Pederson, J. Am. Chem. Soc. 89 (1967) 7017–7036. [316] M.J. Deetz, M. Shang, B.D. Smith, J. Am. Chem. Soc. 122 (2000) 6201–6207. [317] K. Datta, M. Banerjee, A.K. Mukherjee, S.K. Nayak, J. Phys. Chem. B 108 (2004) 16100–16106. [318] M. Mazik, M. Kuschel, W. Sicking, Org. Lett. 8 (2006) 855–858. [319] R.M. Izzat, J.S. Bradshaw, S.A. Nielson, J.D. Lamb, J.J. Christensen, D. Sen, Chem. Rev. 85 (1985) 271–339. [320] N. Soladie, M.E. Walther, M. Gross, M.F. Duarte, C. Bourgogne, J.-F. Nierengarten, Chem. Commun (2003) 2412–3413. [321] J.-F. Nierengarten, U. Hahn, T.M.F. Duarte, F. Cardinali, N. Solladie, M.E. Walther, A.V. Dorsselaer, H. Herschbach, E. Leize, A.-M.A. Gary, A. Trabolsi, M. Elhabiri, C.R. Chemie 9 (2006) 1022–1030. [322] E. Maligaspe, N.V. Tkachenko, N.K. Subbaiyan, R. Chitta, M.E. Zandler, H. Lemmetyinen, F. D’souza, J. Phys. Chem. A 113 (2009) 8478–8489. [323] F. D’souza, C.A. Wijesinghe, M.E. El-Khouly, J. Hudson, M. Niemi, H. Lemmetyinen, N.V. Tkachenko, M.E. Zandler, S. Fukuzumi, Phys. Chem. Chem. Phys. 113 (2011) 18168–18178. [324] F. D’souza, R. Chitta, S. Gadde, M.E. Zandler, A.S.D. Sandanayaka, Y. Araki, O. Ito, Chem. Comm (2005) 1279–1281. [325] S. Dayal, R. Krolicki, Y. Lou, X. Qiu, J.C. Berlin, M.E. Kenney, M.E. Burda, Appl. Phys. B 84 (2006) 309–315. ¯ ¯ [326] M. Sibrian-Vazquez, J. Ortiz, I.V. Nesterova, F. Fernandez-L azaro, Á. Sastre-Santos, S.A. Soper, M.G.H. Vicente, Bioconjugate Chem. 18 (2007) 410–420. [327] M. Zhang, T. Murakami, K. Ajima, K. Tsuchida, A.S.D. Sandanayaka, O. Ito, S. Iijima, M. Yudasaka, Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 14773–14778. [328] J.D. Miller, E.D. Baron, H. Scull, A. Hsia, J.C. Berlin, T. McConnick, V. Colussi, M.E. Kenney, K.D. Cooper, N.L. Oleinick, Toxicol. Appl. Pharmacol. 224 (2007) 290–299. [329] Y. Cheng, A.C. Samia, J. Li, M.E. Kenney, A. Resnick, C. Burda, Langmuir 26 (2010) 2248–2255. [330] X.J. Jiang, P.C. Lo, Y.M. Tsang, S.L. Yeung, W.P. Fong, D.K.P. Ng, Chem. Eur. J. 16 (2010) 4777–4783. [331] B.H. Lessard, T.M. Grant, R. White, E. Thibau, Z.-H. Lu, T.P. Bender, J. Mater. Chem. A 3 (2015) 24512–24524. [332] S. Honda, H. Ohkita, H. Benten, O. Ito, Chem. Commun. 46 (2010) 6596–6598. [333] J. Huang, Y. Wu, D. Wang, Y. Ma, Z. Yue, Y. Lu, M. Zhang, Z. Zhang, P. Yang, Appl. Mater. Interfaces 7 (2015) 3732–3741. [334] G. Kodis, C. Herrero, R. Palacios, E. Marino-Ochoa, S. Gould, L. de la Garza, R. van Grondelle, D. Gust, T.A. Moore, A.L. Moore, J.T.M. Kennis, J. Phys. Chem. B 108 (2004) 414. ¯ ¯ [335] J.L. Rodríguez-Redondo, Á. Sastre-Santos, F. Fernandez-L azaro, D. Soares, G.C. Azzellini, B. Elliot, L. Echegoyen, Chem. Commun. 126 (2006) 5–1267. [336] C. Farren, C.A. Christensen, S. FitzGerald, M.R. Bryce, A. Beeby, J. Org. Chem. 67 (2002) 9130–9139.

[337] E.A. Ermilov, S. Tannert, T. Werncke, M.T.M. Choi, D.K.P. Ng, B. Röder, Chem. Phys. 328 (2006) 428–437. [338] K. Ishii, M. Iwasaki, N. Kobayashi, Chem. Phys. Lett. 436 (2007) 94–98. ˜ [339] G. Kodis, C. Herrero, R. Palacios, E. Marino-Ochoa, S. Gould, L. de la Garza, R. van Grondelle, D. Gust, T.A. Moore, A.L. Moore, J.T.M. Kennis, J. Phys. Chem. B 108 (2004) 414–425. [340] S. Tannert, E.A. Ermilov, J.O. Vogel, M.T.M. Choi, D.K.P. Ng, B. Röder, J. Phys. Chem. B 111 (2007) 8053. ¯ ¯ [341] L. Martın-Gomis, K. Ohkubo, F. Fernandez-L azaro, S. Fukuzumi, Á. Sastre-Santos, Org. Lett. 9 (2007) 3441–3444. ¯ ¯ [342] L. Martın-Gomis, K. Ohkubo, F. Fernandez-L azaro, S. Fukuzumi, Á. Sastre-Santos, J. Phys. Chem. A 112 (2008) 10744–10752. [343] M.E. El-Khouly, J.-H. Kim, K.-Y. Kay, S. Fukuzumi, J. Porphyrins Phthalocyanines 17 (2013) 1055–1063. [344] M.E. El-Khouly, J.H. Kim, K.-Y. Kay, C.S. Choi, O. Ito, S. Fukuzumi, Chem. Eur. J. 15 (2009) 5301–5310. [345] M.E. El-Khouly, E.S. Kang, K.-Y. Kay, C.S. Choi, Y. Araki, O. Ito, Chem. Eur. J. 13 (2007) 2854–2863. [346] J.L. Sessler, P.A. Gale, W.-S. Cho, Anion Receptor Chemistry, Royal Society of Chemistry, Cambridge, UK, 2006. [347] H. Popelkova, A. Commet, T. Kuntzleman, C.F. Yocum, Biochemistry 47 (2008) 12593. [348] N. Busschaert, C. Caltagirone, W. Van Rossom, P.A. Gale, Chem. Rev. 115 (2015) 8038–8155. [349] P.E.M. Siegbahn, R.H. Crabtree, J. Am. Chem. Soc. 121 (1999) 117–127. [350] R. Jou, J.A. Cowan, J. Am. Chem. Soc. 113 (1991) 6685–6686. [351] J.L. Sessler, P.A. Gale, in: K.M. Kadish, K.M. Smith, R. Guilard (Eds.), The Porphyrin Handbook, vol. 6, Academic Press, San Diego, CA, 2000, pp. 257–258. [352] A. Guskov, J. Kern, A. Gabdulkhakov, M. Broser, A. Zouni, W. Saenger, Nat. Struct. Mol. Biol. 16 (2009) 334–342. [353] J.Q. Barber, Rev. Biophys. 36 (2003) 71–89. [354] H.J. van Gorkom, C.F. Yocum, Photosystem II: The Light-Driven Water: Plastoquinone Oxidoreductase, in: T.J. Wydrzynski, K. Satoh (Eds.), Springer Dordrecht, 2005, pp. 307–328. [355] K. Lindberg, T. Vanngard, L.-E. Andréasson, Photosynth. Res. 38 (1993) 401–408. [356] H. Wincencjusz, C.F. Yocum, H.J. van Gorkom, Biochemistry 38 (1999) 3719–3725. [357] H. Popelkova, C.F. Yocum, Photosynth. Res. 93 (2007) 111–121. [358] A. Guskov, J. Kern, A. Gabdulkhadov, M. Broser, A. Zouni, W. Saenger, Nat. Struct. Mol. Biol. 16 (2009) 334–342. [359] J.W. Murray, K. Maghlaoui, J. Kargul, N. Ishida, T.-L. Lai, A.W. Rutherford, M. Sugiura, A. Boussac, J. Barber, Energy Environ. Sci. 1 (2008) 161–166. [360] C.F. Yocum, Coord. Chem. Rev. 252 (2008) 296–305. [361] Y. Xie, J.P. Hill, A.L. Schumacher, A.S.D. Sandanayaka, Y. Araki, P.A. Karr, J. Labuta, F. D’souza, O. Ito, C.E. Anson, A.K. Powell, K. Ariga, J. Phys. Chem. C 112 (2008) 10559–10572. [362] F. D’souza, N.K. Subbaiyan, Y. Xie, J.P. Hill, K. Ariga, K. Ohkubo, S. Fukuzumi, J. Am. Chem. Soc. 131 (2009) 16138–16146. [363] J.P. Hill, M.E. El-Khouly, R. Charvet, N.K. Subbaiyan, K. Ariga, S. Fukuzumi, F. D’souza, Chem. Commun. 46 (2010) 7933–7935. [364] D. Subois, G. Moninot, W. Kunter, M.T. Jones, K.M. Kadish, J. Phys. Chem. 96 (1992) 7137–7145. [365] M. Grätzel, Acc. Chem. Res. 14 (1981) 376–384. [366] S.-F. Chan, M. Chou, C. Creutz, T. Matsubara, N. Sutin, J. Am. Chem. Soc. 103 (1981) 369–379. [367] C.V. Krishnan, B.S. Brunschwig, C. Creutz, N. Sutin, J. Am. Chem. Soc. 107 (1985) 2005–2015. [368] P. Du, J. Schneider, P. Jarosz, R. Eisenberg, J. Am. Chem. Soc. 128 (2006) 7726–7727. [369] E.H. Yonemoto, R.L. Riley, Y.I. Kim, S.J. Atherton, R.H. Schmehl, T.E. Mallouk, J. Am. Chem. Soc. 114 (1992) 8081–8087. [370] N. Toshima, K. Hirakawa, Polym. J. 31 (1999) 1127–1132. [371] I. Okura, N. Kim-Thuan, J. Mol. Catal. 6 (1979) 227–230. [372] I. Okura, Coord. Chem. Rev. 68 (1985) 53–99. [373] Y. Amao, Y. Tomonou, I. Okura, Solar Energy Mater. Solar Cells 79 (2003) 103–111. [374] I. Okura, H. Hosono, J. Phys. Chem. 96 (1992) 4466–4469. [375] L. Persaud, A.J. Bard, A. Campion, M.A. Fox, T.E. Mallouk, S.E. Webber, J.M. White, J. Am. Chem. Soc. 109 (1987) 7309–7314. [376] D.-L. Jiang, C.-K. Choi, K. Honda, W.-S. Li, T. Yuzawa, T. Aida, J. Am. Chem. Soc. 126 (2004) 12084–12089. [377] S. Fukuzumi, Eur. J. Inorg. Chem (2008) 1351–1362. [378] S. Fukuzumi, S. Koumitsu, K. Hironaka, T. Tanaka, J. Am. Chem. Soc. 109 (1987) 305–316. [379] S. Fukuzumi, H. Imahori, K. Okamoto, H. Yamada, M. Fujitsuka, O. Ito, D.M. Guldi, J. Phys. Chem. A 106 (2002) 1903–1908. [380] S. Fukuzumi, H. Kotani, K. Ohkubo, S. Ogo, N.V. Tkachenko, H. Lemmetyinen, J. Am. Chem. Soc. 126 (2004) 1600–1601. [381] H. Kotani, K. Ohkubo, S. Fukuzumi, Faraday Discuss. 155 (2012) 89–102. [382] H. Kotani, K. Ohkubo, Y. Takai, S. Fukuzumi, J. Phys. Chem. B 110 (2006) 24047–24053. [383] H. Kotani, T. Ono, K. Ohkubo, S. Fukuzumi, Phys. Chem. Chem. Phys. 9 (2007) 1487–1492. [384] G. Gahleitner, Int. J. Hydrogen Energy 38 (2013) 2039–2061.

M.E. El-Khouly et al. / Journal of Photochemistry and Photobiology C: Photochemistry Reviews 31 (2017) 36–83 [385] S. Fukuzumi, Y. Yamada, T. Suenobu, K. Ohkubo, H. Kotani, Energy Environ. Sci. 4 (2011) 2754–2766. [386] R.S. Disselkamp, Int. J. Hydrogen Energy 35 (2010) 1049–1053. [387] L. An, T. Zhao, X. Yan, X. Zhou, P. Tan, Sci. Bull. 60 (2015) 55–64. [388] S. Fukuzumi, Y. Yamada, K.D. Karlin, Electrochim. Acta 82 (2012) 493–511. [389] S. Fukuzumi, Y. Yamada, Aust. J. Chem. 67 (2014) 354–364. [390] S. Fukuzumi, Biochim. Biophys. Acta 1857 (2016) 604–611. [391] S. Kato, J. Jung, T. Suenobu, S. Fukuzumi, Energy Environ. Sci. 6 (2013) 3756–3764. [392] Y. Isaka, S. Kato, D. Hong, T. Suenobu, Y. Yamada, S. Fukuzumi, J. Mater. Chem. A 3 (2015) 12404–12412. [393] Y. Isaka, Y. Yamada, T. Suenobu, S. Fukuzumi, Catal. Sci. Technol. 6 (2016) 681–684.

83

[394] Y. Isaka, Y. Yamada, K. Ohkubo, T. Suenobu, S. Fukuzumi, RSC Adv. 6 (2016) 42041–42044. [395] K. Mase, M. Yoneda, Y. Yamada, S. Fukuzumi, Nat. Commun. 7 (2016) 11470, http://dx.doi.org/10.1038/ncomms11470. [396] Y. Yamada, S. Yoshida, T. Honda, S. Fukuzumi, Energy Environ. Sci. 4 (2011) 2822–2825. [397] S.A.M. Shaegh, N.T. Nguyen, S.M.M. Ehteshami, S.H.A. Chan, Energy Environ. Sci. 5 (2012) 8225–8228. [398] Y. Yamada, M. Yoneda, S. Fukuzumi, Inorg. Chem. 53 (2014) 1272–1274. [399] Y. Yamada, M. Yoneda, S. Fukuzumi, Energy Environ. Sci. 8 (2015) 1698–1701. [400] K. Mase, M. Yoneda, Y. Yamada, S. Fukuzumi, ACS Energy Lett. 1 (2016) 913–919.