Metal-oxo-mediated OO bond formation reactions in

DOI 10.1515/irm-2012-0004

BioInorg React Mech 2012; 8(1-2): 41–57

Review Subrata Kundu, Matthias Schwalbe* and Kallol Ray*

Metal-oxo-mediated O-O bond formation reactions in chemistry and biology Abstract: O-O bond formation is one of the key reactions that ensure life on earth. Dioxygen is produced in photosystem II, as well as in chlorite dismutase. The reaction mechanisms occurring in the enzyme active sites are controversially discussed – although their structures have been resolved with less unambiguity. Artificial molecular catalysts have been developed in the last years to obtain vital insights into the O-O bond formation step. This review put together the scarce literature on the topic that helped in understanding the key steps in the O-O bond formation reactions mediated by high-valent oxo complexes of the first-row transition metals. Keywords: dismutase activity; first-row transition metals; metal-oxo; O-O bond formation; water oxidation.

*Corresponding authors: Matthias Schwalbe and Kallol Ray, Department of Chemistry, Humboldt-Universität zu Berlin, Brook-Taylor Strasse 2, 12489 Berlin, Germany, e-mail: [email protected]; [email protected] Subrata Kundu: Department of Chemistry, Humboldt-Universität zu Berlin, Brook-Taylor Strasse 2, 12489 Berlin, Germany

Introduction Dioxygen O-O bond-cleaving and bond-forming reactions occur at transition metal centers in a number of metalloenzymes. For example, heme and nonheme monooxygenases bind and activate O2 to generate high-valent metal-oxo intermediates via rate-determining homolytic or heterolytic O-O bond cleavage of the metal-dioxygen intermediates (Collman et al., 2004; Chufan et al., 2007; Nam, 2007 et al., 2007; Hohenberger et al., 2012). The O-O bond activation of metal-O2 adducts has been intensively investigated over the past several decades for that reason and is now well understood (Wertz and Valentine, 2000; Collman et al., 2004; Groves, 2005; Shaik et al., 2005; Chufan et al., 2007; Nam, 2007; Collman and Ghosh, 2010; Halime et al., 2010; Hohenberger et al., 2012). In photosystem II (PSII; McEvoy

and Brudvig, 2006; Meyer et al., 2007; Barber, 2009; Romain et al., 2009) or in chlorite dismutase (Cld; Lee et al., 2008), the microscopic reverse process, which is the metaloxo-mediated O-O bond formation reaction, is considered to be the most critical part of dioxygen evolution. However, the mechanism of the O-O bond formation step in PSII has proven to be a subject of great controversy (Pecoraro et al., 1998; Vrettos et al., 2001; Siegbahn, 2006, 2008a; Pecoraro and Hsieh, 2008; Sproviero et al., 2008; Tagore et al., 2008). The major problem is the absence of any isolable intermediate during the course of the oxygen evolution, which prevents the unambiguous assignment of mechanism(s). Biomimetic studies can also aid in our understanding of the fundamental reactivity of the metal-oxo species in dioxygen production. A number of transition metal complexes have been recently shown to form O-O bonds; a variety of ligands and nuclearities that comprise many complex topologies have been developed, but only in rare cases has an unambiguous assignment of the mechanism been provided (Liu et al., 2008; Concepcion et al., 2009; Dismukes et al., 2009; Romain et al., 2009; Chen et al., 2010; Dau et al., 2010; Llobet and Romain, 2010; Meyer, 2011; Siegbahn, 2011a; Tong et al., 2011). Moreover, although a large number of high-valent metal-oxo complexes have been synthesized in the last 10–20 years (Nam, 2007; Hohenberger et al., 2012), only a few are found to be efficient in initiating O-O bond formation reaction. In this review, we describe the sparse literature existing on the detailed mechanistic studies of the metal-oxomediated O-O bond formation reactions, focusing mainly on the cheap and abundant first-row biorelevant transition metals such as Mn, Fe, Co, Ni, and Cu. Metal-oxo complexes based on early transition metals such as Ti, V, and Cr are reported to be too stable against O-O bond formation reaction. The reactions mediated by Ru, Os (Kunkely and Vogler, 2009), or Ir (McDaniel et al., 2008; Hull et al., 2009; Lalrempuia et al., 2010) complexes are not considered in this review. Detailed accounts of the rutheniumoxo-mediated O-O bond formation reactions can be found in reviews by Llobet, Siegbahn, and Meyer (Liu et al., 2008; Concepcion et al., 2009; Dismukes et al., 2009; Chen et al.,

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S. Kundu et al.: Metal-oxo-mediated O-O bond forming reactions

2010; Dau et al., 2010; Llobet and Romain, 2010; Meyer, 2011; Siegbahn, 2011a; Tong et al., 2011). This review is organized into two main sections: mechanistic possibilities for the metal-oxo-mediated O-O bond formation reactions and survey of metal-oxo-mediated O-O bond formation reactions. In the first part, we provide a theoretical account of how different electronic structures of metal-oxos can control the mechanism of the O-O bond formation step. The survey, which is organized by metals, describes both biological and inorganic O-O bond formation reactions. Reversible O-O bond cleavage and formation reactions, which are observed in few rare cases, are also included in the survey.

Mechanistic possibilities for the metal-oxo-mediated O-O bond formation reactions Several mechanistic possibilities have been proposed for the O-O bond formation reactions taking place in biological and chemical systems (Figure 1) (Betley et al., 2008a,b; Siegbahn, 2008b; Hetterscheid et al., 2009). Metal-oxos are proposed as critical intermediates in all cases, except one. Milstein and coworkers have recently offered an alternative pathway for the O-O bond formation reaction via a mononuclear ruthenium complex (Figure 1, pathway D) (Kohl et al., 2009). In contrast to all previous approaches, the O-O coupling step is shown not to involve any high-valent oxo species but is initiated via photoinduced reductive elimination of hydrogen peroxide from a mononuclear low-valent ruthenium dihydroxo species. However, there is no evidence

in the literature that shows that the mechanism proposed by Milstein and coworkers can be extended to other chemical or biological systems, especially to first row transition metals. Hence, for the purpose of this review, we will limit our discussion to O-O bond formation reactions at metal-oxo active sites, which fall under two general classifications: the acid-base (AB) mechanism in which nucleophilic oxygen of water or hydroxide attacks the electrophilic oxygen of the metal-oxo intermediate (Figure 1, pathway A) or the radical coupled (RC) mechanism where radical-like oxygen species couple with each other (Figure 1, pathways B and C) (Betley et al., 2008a,b; Siegbahn, 2008b; Hetterscheid et al., 2009). Whereas the AB mechanism requires a metal-oxo unit with an electrophilic oxygen atom, the radical character at the oxygen of the metal-oxo center is critical to advancing the RC strategy for O-O bond formation. Additionally, an RC strategy demands that two oxos are sufficiently close to each other for their effective coupling. Thus, both sterics and electronics play a vital role in determining the mechanism of the metal-oxo-mediated O-O bond formation reaction. The electronics are predominantly controlled by the electron count and the different ligand fields in which the metal-oxo resides, which in turn control the strength of the metal-oxo bond. Figure 2 shows the qualitative frontier molecular orbital splitting diagrams for a metal-oxo residing in various ligand fields. The stability of the oxo is largely determined by the occupancy of the metal-oxo π-antibonding d(xz/yz) molecular orbitals (Betley et al., 2008a,b). If the d(xz/yz) orbital set is empty, then it is able to accept the px and py electron pairs from an oxo ligand to effectively form metaloxo multiple bonds. This situation also makes the oxo extremely electrophilic, thereby making the M-O unit ideal for undergoing O-O bond coupling via the AB mechanism.

Figure 1 Generally considered pathways for the formation of O-O bonds in chemistry and biology.



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Figure 2 Qualitative frontier molecular orbital splitting diagrams for metal-oxo species in tetragonal and trigonal ligand fields.

Increasing population of the d(xz/yz) orbital set, however, lowers the bond order of the M-O bond, thereby making the oxo nucleophilic. This, in turn, favors the RC mechanism for the O-O coupling step. It is important to note that the electron pair in the d(xy) orbital is also found to have some effect in determining the reactivity of the metal-oxo unit, although it is effectively nonbonding in all geometries shown in Figure 2. Thus, if the electrons are completely removed from d(xy), i.e., a d0 metal center such as M=VV, TiIV, or ZrIV, the metal-oxo unit becomes extremely stable against O-O bond formation reactions. This becomes very obvious in case of Cr(VI) compounds that possess a very strong and stable Cr≡O triple bond.

Survey of metal-oxo-mediated O-O bond formation reactions Manganese Dioxygen is a necessity for the evolution of respiratory bioenergetics and thus of higher life forms on earth. In nature, light-driven water oxidation to dioxygen occurs in PSII by extraction of four electrons and four protons from two water molecules. The oxidation is efficiently catalyzed by a protein-bound oxygen evolving center (OEC), which is composed of four manganese atoms and one calcium atom connected by several μ-oxo bridges and water molecules (Yano and Yachandra, 2008; Grundmeier and Dau, 2012). There has been a long-standing discussion about the structure of the OEC and the reaction mechanism of the O-O bond formation. In recent years, more and more consensus has been reached about both points of conten-

tion. The appearance of a 1.9-Å resolution structure of the OEC especially assisted in understanding the structural architecture (Siegbahn, 2011a; Umena et al., 2011), i.e., the CaMn3O4 cube (shown in Figure 3), where an Mn3Ca cube is connected to a ‘dangling’ manganese center by an oxo bridge. It is important to note that the X-ray crystal structure represents a very reduced state of the OEC (Grundmeier and Dau, 2012). Despite numerous experimental and theoretical model studies, the actual mechanism for the formation of molecular oxygen is not clear yet. It is well known that oxidation of water occurs via the Kok cycle through the S0–S4 states and O2 is released from the S4 state (Kok et al., 1970; Dau and Haumann, 2008). The nature of the highly oxidized S4 state is, however, controversially discussed in the literature – although all agree with a formal oxidation state of [MnIV3MnV1] (Messinger et al., 2001; McEvoy and Brudvig, 2006). Presently, there are three different possibilities for the formation of the O-O bond: nucleophilic attack of water or hydroxide on a formally MnV oxo species (Pecoraro et al., 1998; Yocum, 2008), radical coupling of two bridging oxos (McEvoy and Brudvig, 2006), and radical coupling of the dangling [MnIV-O•] species with a bridging oxygen in the manganese cluster (shown in Figure 3) (Siegbahn and Lundberg, 2005; Siegbahn, 2006, 2008c, 2009a, 2011b). The uncertainty related to the O-O bond formation mechanism in PSII inspired bioinorganic chemists to simulate the structural motif of the OEC and use molecular complexes for O-O bond formation reactions, so as to obtain a better understanding of the oxygen evolution mechanism (Ruettinger et al., 2000; Mukhopadhyay et al., 2004; Kanady et al., 2011; Nayak et al., 2011). Attempts were made to prepare MnV-oxo complexes from species related to the OEC to support their involvement in the


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Figure 3 Structure of the OEC as obtained from the X-ray crystallography (left) (Kok et al., 1970; Umena et al., 2011) and in the S4 state schematically showing the attack of a MnIV-oxyl on a bridging oxo ligand (right) (Siegbahn, 2011b). The oxygen atoms participating in O-O bond formation are shown in red.

O-O bond formation process. The groups of Crabtree and Brudvig (Tagore et al., 2008) and Pecoraro and Hsieh (2008) have provided evidence for MnV-oxo intermediates related to the OEC that were very short lived. However, both porphyrins and corroles and some related complexes have also been shown to give MnV-oxo species with certain stability (Naruta et al., 1994; Groves et al., 1997; Gross et al., 2000; Jin et al., 2000; Golubkov et al., 2001; Mandimutsira et al., 2002; Liu et al., 2003; Shimazaki et al., 2004). Naruta and coworkers presented a phenylene-linked dimeric porphyrin complex (Figure 4) that could be oxidized with meta-chloroperoxybenzoic acid (mCPBA) to the bis MnV-oxo state under basic conditions (Shimazaki et al., 2004). Following acidification with trifluorsulfonic acid, the two [HO-MnV=O] centers have been proposed to release dioxygen. Unfortunately, it is not fully clear if the O-O bond formation happens via the AB or RC mechanism, although the latter was the preferred path by the authors. Recently, Gao et al. (2007, 2009) reported an elegant result that the reaction of MnV-oxo corroles (corrole=tolylcorrole or nitrophenylcorrole; Figure 4) and hydroxide affords O2 evolution; the O-O bond formation in the reaction was demonstrated to occur via nucleophilic

attack of hydroxide ion on a MnV-oxo moiety by UV-vis spectroscopy and high-resolution mass spectroscopy. Subsequent DFT calculations revealed that the differences in the electronic energy between the ground state (singlet) and the lowest excited states (triplet and quintet) of MnO-corrole are very small. The population depends on the hydrogen bonding ability of the solvent molecules surrounding the active center (Privalov et al., 2007); stronger hydrogen bonding ability was reported to make the highspin quintet Mn(IV)-O• oxyl radical state more stable. O-O bond formation still occurs via reaction with a hydroxide molecule assisted by extended hydrogen bonding interaction. Even for the dinuclear biscorrole complex (Figure 4), the radical coupling of the two MnO units was found to be energetically unfavored. The second metal-oxo unit, therefore, does not directly take part in the O-O bond formation step but only provides stabilization via a hydrogen bonding network to the first metal center at which the O-O bond formation occurs. Nam and coworkers have also demonstrated reversible O-O bond cleavage and formation between high-valent MnV-oxo and MnIV-peroxo units supported by a tris(3,5-trifluoromethylphenyl) corrole ligand (Figure 4) (Kim et al.,

Figure 4 Structures of the dinuclear (Naruta et al., 1994; Shimazaki et al., 2004; Gao et al., 2007) and mononuclear (Gao et al., 2007, 2009; Kim et al., 2010) oxo-Mn(V) centers supported on the porphyrin and corrole-based ligands.



2010). Addition of hydroxide to the low-spin S=0 MnV-oxo species affords the high-spin S=3/2 Mn(IV) peroxo compound. The side-on peroxo compound was demonstrated to reform the MnV-oxo state upon acidification. Interestingly, experimental evidence has also been obtained in favor of the reversible O-O bond formation step in PSII (Clausen and Junge, 2004). Thus, the reports of Gao et al. (2009) as well as Nam and coworkers (Kim et al., 2010) favor the AB O-O bond formation reaction taking place between MnV-oxo and water/hydroxide units. This mechanism, however, is disfavored in PSII by recent DFT calculations (Siegbahn and Lundberg, 2005; Siegbahn, 2006, 2008c, 2009a,b, 2011b). Although, Gao et al. (2007, 2009) recently demonstrated a water oxidation catalyst based on a mononuclear manganese center, it was previously thought that a minimum of two manganese atoms are necessary to drive the O-O bond formation step. Accordingly, a large number of dinuclear complexes were synthesized in that respect and their O-O bond formation abilities were studied in considerable detail (Lomoth et al., 2002; Mukhopadhyay et al., 2004; Kurz et al., 2007; Cady et al., 2008; Pecoraro and Hsieh, 2008). The mixed-valent complex [(terpy)(H2O) MnIV(μ-O)2MnIII(H2O)(terpy)]3+ (terpy=2,2′:6′,2″-terpyridine) (Figure 5; Limburg et al., 1999, 2001; Lundberg et al., 2004; Chen et al., 2007; Tagore et al., 2008; Wiechen et al., 2012) reported by the groups of Crabtree and Brudvig is one of the most studied complexes in this field. With more than 50 turnovers, it is also considered the most active complex of its type. The authors initially proposed (Limburg et al., 1999) an AB mechanism for the O-O bond formation step: two-electron oxidation leads to the formation of the catalytically active intermediate [(terpy)(H2O)MnIV(μO)2MnV(O)(terpy)]3+, which is then attacked by water or hydroxide. DFT calculations using the B3LYP functional on

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the complex [(terpy)(H2O)MnIV(μ-O)2MnIII(H2O)(terpy)]3+, however, revealed that radical formation is required for the O-O bond formation step (Lundberg et al., 2004). Thus, a MnIV-oxyl radical, instead of a MnV-oxo species, was proposed as the active intermediate. The attack of a water molecule was concluded to be assisted by hydrogen bonding to a bridging μ-oxo ligand, thereby forming a hydroxo bridge and a MnIII-hydroperoxide species as successive reaction intermediates. This mechanism involves one catalytic active metal center, whereas the other functions more as a spectator ligand. It is believed that most of the catalytically active dinuclear manganese complexes with the Mn2O2motif react in the same way (Gao et al., 2007; Privalov et al., 2007; Kurz, 2009; Wiechen et al., 2012). A proposal for the O-O bond formation step via radical coupling of two bridging oxides also exists in the synthetic model complexes. Poulsen et al. (2005) reported a dimeric Mn(II) complex with the ligand mcbpen (N-methyl-N′-carboxymethyl-N,N′bis(2-pyridylmethyl)ethane-1,2-diamine) that formed the [MnIV2(O)2(mcbpen)2]2+ species (Figure 6) after reaction with tert-butylhydrogenperoxide; [MnIV2(O)2(mcbpen)2]2+ could catalyze oxidation of water to dioxygen with an outstanding turnover number of 15 000. A suggested mechanism based on ESI-MS studies relies on the flexible carboxylate side arms, which assist in the formation and transformation of the bis(μ-oxo)-dimanganese intermediate into a μ-η2:η2-peroxo [MnIII2(O2)]2+ intermediate, which eventually evolves dioxygen (with concomitant replacement by water molecules) (Figure 6, pathway A). This reaction sequence is rather uncommon in manganese chemistry but has precedents observed in copper chemistry (see below) (Halfen et al., 1996). In subsequent studies (Sameera et al., 2011; Seidler-Egdal et al., 2011), however, a different mechanism was proposed, which involved an equilibrium between the

Figure 5 Reaction mechanism for the O-O bond formation in the [(terpy)(H2O)MnIV(μ-O)2MnIII(H2O)(terpy)]3+ system (Limburg et al., 1999; Limburg et al., 2001; Lundberg et al., 2004; Chen et al., 2007; Tagore et al., 2008; Wiechen et al., 2012).


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Figure 6 Two possible reaction mechanisms for the O-O bond formation in the [MnIV2(O)2(mcbpen)2]2+ system. Path A, radical coupling of two μ-Oxos (Poulsen et al., 2005); path B, attack of water to a Mn(IV)oxyl intermediate (Sameera et al., 2011).

diamond-core MnIV(μ-O)2MnIV structure and a mixed-valent MnIII(μ-O)MnIV-O• oxyl radical species (Figure 6, pathway B). The carboxylate groups on the side arms have been suggested to play a vital role in the proposed O-O bond formation step. First, they stabilize the ‘open’ mixed-valent form because of their coordination ability. Second, they were suggested to act as intramolecular base by abstracting a proton from the incoming H2O molecule, thereby assisting in the O-O bond formation step to yield a hydroperoxo intermediate. A subsequent proton transfer to the bridging oxo ligand releases O2. The first functional model of the cubic form of the OEC was introduced in 2000 by Dismukes and coworkers. The Mn4O4 cubane-like complex (dpp)6Mn4O4 (dpp=diphenylphosphinate anion; Figure 7) is reported to release its bridging oxides as O2 upon (UV-) photoexcitation (Ruettinger et al., 2000). Starting from the MnIII2MnIV2 ground state, photoexcitation leads to an initial loss of a phosphinate ligand followed by the radical coupling of two μ-O

bridges to form a peroxo core intermediate [MnIII4O2(O22-)]6+. Eventual release of dioxygen results in the formation of the photoproduct [MnII2MnIII2O2(dpp)5]+ (Kuznetsov et al., 2010). The cubane complex has been shown to catalyze the oxidation of water much more efficiently when doped into a proton conducting Nafion membrane, which was thought to assist the proton transfer processes (Brimblecombe et al., 2008, 2009). Very recently, however, a related synthetic tetranuclear manganese cluster impregnated into a Nafion matrix was demonstrated to decompose under catalytic conditions to MnOx nanoparticles, which makes the suggested reaction mechanism of Dismukes and coworkers highly questionable (Hocking et al., 2011).

Iron Two examples of iron-oxo-mediated O-O bond formation reactions are known in biology. The first example is



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Figure 7 Photoinduced O-O bond formation mediated by the (dpp)6Mn4O4 complex (Dismukes et al., 2009).

reported in the enzyme Cld (Lee et al., 2008), which is an iron-containing heme protein that transforms toxic chlorite (ClO2-) into innocuous chloride and molecular oxygen. Cld is the only enzyme other than PSII to catalyze O-O bond formation as its primary function. Based on detailed kinetic studies, Abu-Omar, DuBois, and coworkers favor a mechanism (Figure 8, pathway A) that involves the ratedetermining formation of a Fe(IV)-oxo porphyrin π-cation radical (Cld compound I) intermediate and a hypochlorite (ClO-) anion from the reaction of the ferric-heme with chlorite anion (Lee et al., 2008). Although the oxygen atom of ClO- is extremely nucleophilic in character, the compound I intermediate, a formally oxo-Fe(V) species, is known to possess an electrophilic oxygen atom (Hohenberger et al., 2012). Hence, in the next step, a very fast AB O-O bond

formation reaction is proposed between the oxygen atoms of the resulting hypochlorite/compound I pair, thereby resulting in the elimination of dioxygen and chloride via a fleeting, isomerized peroxyhypochlorite intermediate. Such a mechanism is consistent with both 18OH2 and Cl18O2labeling studies, which definitively show that the evolved O2 originates entirely from chlorite and not from solvent water. It is important to note, however, that the compound I intermediate could not be trapped on the way to oxygen evolution; its involvement is inferred mainly from the demonstrated ability of Cld to form Cpd-I in the presence of peroxyacetic acid (PAA). Based on the rate of decay of Cpd-I intermediate generated in the presence of PAA and the turnover number for Cld, a first-order rate constant of 107 s-1 was determined for the AB O-O bond formation step

Figure 8 Possible mechanisms for the dismutation of chlorite in chemistry (Zdilla et al., 2008) and biology (Lee et al., 2008). (A) Formation of Cpd-I by oxygen atom transfer from chlorite, followed by its rebound with ClO-. (B) Concerted rearrangement of bound chlorite without formation of Cpd-I. (C) Sequential oxygen atom transfer reaction through Cpd-I. (D) Decay of Cpd-I to Cpd-II observed in the artificial system (Zdilla et al., 2008).


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between the hypochlorite/Cpd-I pair. Such a fast recombination rate explains the transient nature of Cpd-I in presence of ClO- and is also consistent with the demonstrated high selectivity of the dismutation of chlorite to dioxygen and chloride with no other observed side products in presence of added co-substrates such as guaiacol and thioanisole. The study of Abu-Omar, DuBois, and coworkers, however, cannot rule out alternative mechanisms involving the decomposition of chlorite in a single, concerted step from a metal-bound chlorite (Figure 8, pathway B) or the reaction of Cpd-I and a second molecule of chlorite in the O-O bond formation step (Figure 8, pathway C). The reaction of Cpd-I generated in presence of PAA with externally added chlorite or hypochlorite anions may have provided additional mechanistic insights, which were unfortunately not performed in the studies by Abu-Omar, DuBois, and coworkers. The next report of O-O bond formation in biology was provided by Roth and Cramer (2008) in their detailed mechanistic study of the reaction of Fe(III)-horseradish peroxidase with hydrogen peroxide to generate the HRP Cpd-I intermediate. The formation of HRP Cpd-I can take place from the Fe(III) hydroperoxo species either in a single step by O-O heterolysis or in two steps involving O-O homolysis to first form the oxo-Fe(IV) intermediate (Cpd-II) (and hydroxyl radical) that can subsequently form Cpd-I by a proton-coupled electron transfer (PCET) mechanism (Figure 9). Before the study of Roth and Cramer (2008), it was commonly assumed that O-O bond heterolysis is the rate-determining step for the activation of HRP by H2O2 (Baek and Van Wart, 1992; Newmyer and

Ortiz de Montellano, 1995; Rodriguez-Lopez et al., 2000, 2001; Jones and Dunford, 2005; Shintaku et al., 2005). However, based on the experimentally determined isotope labeled 18-oxygen kinetic isotope effect, which was found to be significantly lower than that calculated by DFT methods for an O-O heterolysis process, Roth and Cramer (2008) proposed a reversible O-O cleavage before a rate-limiting transformation to Cpd-I. This mechanism is also consistent with the demonstrated incorporation of 18OH2 into the unreacted H2O2. Thus, the oxo-Fe(IV) unit of Cpd-II and hydroxyl radical formed in the first step can recombine by an RC mechanism to yield back the Fe(III)-hydroperoxo species. This study by Roth and Cramer (2008) represents the only example till date where a reversible O-O cleavage/formation occurs in a heme protein. It is important to note that for heme proteins both Cpd-I and Cpd-II intermediates possess intermediate-spin Fe(IV) center with a d-electron configuration of d(xy)2 d(xz,yz)2 (Nam, 2007; Hohenberger et al., 2012). Thus, the Fe-O bond distances (1.64–1.68 Å) are found to be similar in the two cases, as in both cases two electrons are present in the Fe-O π-antibonding d(xz,yz) orbital pair (Nam, 2007; Hohenberger et al., 2012). Despite their similar Fe-O bond distances, the O-O bond formation reactions mediated by Cpd-I and Cpd-II intermediates follow different mechanisms. Although an AB mechanism is favored for Cpd-I (Lee et al., 2008), Cpd-II follows an RC approach (Roth and Cramer, 2008). Thus, the additional porphyrin-centered electron-hole in Cpd-I makes the oxygen atom sufficiently electrophilic to be attacked by the oxygen atom

Figure 9 Alternative mechanisms of H2O2 activation in horseradish peroxidase (Roth and Cramer, 2008).



of ClO- in Cld (Lee et al., 2008). Moreover, the radical-coupled O-O bond-forming ability of Cpd-II is consistent with a recent study of Ye and Neese (2011), where they demonstrated that for C-H bond activation reactions mediated by nonheme oxo-Fe(IV) complexes, the active species is in fact an oxyl-ferric species that is generated by an iron-oxo bond lengthening of the oxo-Fe(IV) reactant en route to the transition state. A similar situation may be envisaged for the Cpd-II-mediated O-O formation reaction taking place in HRP (Lee et al., 2008), where the hydroxyl radical can react with the oxyl-ferric species, thereby regenerating the Fe(III)-hydroperoxo unit. The first example of an iron-based O-O bond formation reaction in a molecular system is provided by Suzuki and coworkers in their report of reversible O-O bond cleavage and formation of a peroxo group involving a Fe(III) complex containing a peroxocarbonate ligand (Furutachi et al., 2005). Although high-valent oxo-Fe(IV) or oxo-Fe(V) intermediates are proposed based on resonance Raman studies, the actual mechanism of the O-O bond formation reaction (AB vs. radical-coupled) has not been unambiguously determined in the study. Zdilla et al. (2008) reported the second example of iron-oxo-mediated O-O bond formation reaction in synthetic model complexes. In their study, a water-soluble iron porphyrin system 5,10,15,20-tetrakis(tetrafluoro-N,N,Ntrimethylanilinium)porphyrinato-Fe(III) [Fe(TF4TMAP)] (Figure 8) is demonstrated as an active catalyst for the dismutation of chlorite to chloride and dioxygen. On the basis of a detailed mechanistic study, Zdilla et al. were also able to provide an unambiguous assignment for the dismutase activity. First of all, in the reaction of [Fe(TF4TMAP)] with 1:1 Cl16O2- and isotopically labeled Cl18O2- at pH 7.14, Zdilla et al. demonstrated the generation of 16O2 and 18O2 as the major products. The absence of mixed-labeled 16O18O dioxygen showed that each oxygen atom in the molecular dioxygen product originates from the same chlorite ion. Thus, dismutation of chlorite occurs by either pathway A involving oxoferryl intermediate or a concerted rearrangement mechanism (pathway B in Figure 8). Additionally, facile appearance of Cpd-II on the stopped-flow timescale could be demonstrated, which favored the pathway A. Cpd-II has been argued to be not directly involved in the Cld activity and proposed to generate from the comproportionation of the active Cpd-I intermediate with Fe(III) (pathway D in Figure 8). Indeed, the Cld Cpd-I generated in the presence of PAA was found to undergo fast decay to Cpd-II, which is consistent with the proposition of Zdilla et al. The accumulation of Cpd-II in the model complex, however, reveals a relatively slower O-O bond formation rate for the hypochlorite/Cpd-I pair as compared with

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that in the enzymatic systems. This leads to unwanted side reactions (Cpd-II and chlorate formation; see Figure 8, pathway D), which explain the low yield of dioxygen (18%) in the model system. Iron-based water oxidation catalysts (Enthaler et al., 2008) are extremely important in the context of obtaining a cheaper alternative energy source. To date, however, only two artificial water oxidation iron catalysts that operate in homogeneous condition have been discovered. The first comes from the groups of Collins and Bernhard, who described that Fe(III) complexes with tetraamido macrocyclic ligands (Fe-TAMLs) are fast water oxidation catalysts (Ellis et al., 2010). However, the activity of the Fe-TAMLs was reported to vanish after few seconds (turnover number=16) and also no detailed mechanistic studies were performed to understand the mechanism of the O-O bond formation step. Fillol et al. (2011) were the first to make an important breakthrough in this field. They recently reported a large family of catalytic systems based on iron and containing straightforward, accessible modular tetradentate nitrogen-based ligands, which are able to perform the oxidation of water with high efficiency in presence of cerium ammonium nitrate at pH 1. The values of the catalytic cycles per metal center (>1000) attained by these iron catalysts are the highest reported for any homogeneous system based on first-row transition metals and are comparable to those of the most active Ru- (Liu et al., 2008; Concepcion et al., 2009; Dismukes et al., 2009; Chen et al., 2010; Dau et al., 2010; Llobet and Romain, 2010; Meyer, 2011; Siegbahn, 2011a; Tong et al., 2011) and Ir-based (McDaniel et al., 2008; Hull et al., 2009; Lalrempuia et al., 2010) systems. Moreover, screening of a large number of iron complexes with different structural motifs allowed Fillol et al. to establish that the presence of two cis free coordination sites is a structural prerequisite for water oxidation catalysis (Figure 10). Additionally, a detailed kinetic study enabled Fillol et al. to propose the mechanism shown in Figure 10, where an Fe(V)-oxo hydroxo species has been proposed as the active species responsible for the AB O-O bond formation step. It is important to note that an Fe(V)oxo hydroxo species has also been implicated as the active oxidant responsible for other oxidation reactions such as cis-dihydroxylation of C=C double bonds in a number of iron-containing nonheme natural and model systems but with only indirect proof of its existence (Prat et al., 2011; Hohenberger et al., 2012). In the catalytic cycle shown in Figure 10, the proposed Fe(V)-oxo hydroxo species could not also be trapped on the way to oxygen generation; the only intermediate observed was the oxo-Fe(IV) complex, which has been proposed as the resting state. The rate-


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Figure 10 Postulated mechanism for water oxidation by iron complexes containing two cis-labile sites (inset) (Fillol et al., 2011).

determining step has been determined to be the reaction of oxo-Fe(IV) species, with Ce4+ yielding the active Fe(V)oxo hydroxo intermediate, thereby excluding the possibility of a bimetallic O-O bond formation mechanism involving two Fe(IV)-oxo complexes. However, Kundu et al. (2012) demonstrated such an RC O-O bond formation reaction involving two Fe(IV)-oxo units bound to a central stannoxane core. The O-O bond formation is proposed to occur in a series of electron-transfer steps with the oxygen progressing through terminal oxo, bridging peroxo, and superoxo states concomitant with a decrease in the formal iron oxidation state (Figure 11) (Kundu et al., 2012).

Cobalt Nature does not use cobalt to achieve O-O bond formation reactions. However, cobalt-based O-O bond formation reaction has proven to be a subject of great interest in the last 5 years following the groundbreaking report of Nocera and coworkers (Kanan and Nocera, 2008; Kanan et al., 2009; Surendranath et al., 2010, 2012; Kanan et al., 2010; Nocera, 2012) about a highly active cobalt-based oxygen-evolving catalyst that forms a thin film on inert electrodes when aqueous solutions of Co2+ salts are electrolyzed in the presence of phosphate (Co-Pi) or borate

(Co-Bi) buffer. These catalysts are of interest because they (1) form in situ under mild conditions on a variety of conductive substrates, (2) exhibit high activity in pH 7–9 water at room temperature, (3) are functional in salt water, (4) self-heal by reversing catalyst corrosion at open circuit upon application of a potential, and (5) can be interfaced with light absorbing and charge separating materials to effect photoelectrochemical water splitting. Accordingly, detailed structural and mechanistic studies have been performed on these systems so as to establish a structure-function correlation. To obtain structural information on the catalytic active species, in situ X-ray absorption spectroscopy (XAS) was performed at cobalt K-edge at a potential corresponding to water oxidation (Risch et al., 2009; Kanan et al., 2010). Extended X-ray fine structure (EXAFS) spectra indicated that the active species is composed of bis-μ-oxo/hydroxo-linked Co ions. A comparison of the EXAFS spectra to the spectrum of a cobaltate compound, CoO(OH), supported a molecular cobaltate cluster model for the active species. In this model, the Co-oxo/hydroxo clusters are proposed to possess the same structural motif found in the extended planes of cobaltates – edge-sharing CoO6 octahedra – but having molecular dimensions (Figure 12). X-ray absorption near-edge structure (XANES) spectroscopy, electron paramagnetic resonance (EPR), and



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Figure 11 RC O-O bond formation mediated by a polynuclear Fe(II) complex (only two iron centers shown for simplicity) in presence of iodosobenzene (Kundu et al., 2012).

electrochemical studies have been used to obtain detailed insights into the mechanism of O-O bond formation reaction mediated by the Co-Pi catalyst (Risch et al., 2009; Kanan et al., 2010; Nocera, 2012). XANES data were found to be consistent with an appreciable population of CoIV when the cobalt films were held at potentials sufficient for water oxidation. In situ EPR studies also showed an S=1/2 low-spin CoIV signal in about 3% yield under catalytic conditions (McAlpin et al., 2010). On the basis of XANES and EPR studies, the EPR active CoIII/IV mixed valence clusters were therefore proposed as the catalyst resting state. Further electrochemical and labeled 18-oxygen studies (Surendranath et al., 2010; Nocera, 2012) established a PCET conversion of CoIII-OH to CoIV-O as a key mechanistic step before oxygen evolution. Accordingly, the mechanism shown in Figure 12 has been proposed, where at the rate-determining step, the mixed-valent CoIII(OH)2(μ-O)CoIV(OH)2 species is converted to CoIV(O) (OH)(μ-O)CoIV(OH)2, which is then followed by the O-O bond formation step that eventually results in the release of dioxygen. The actual mechanism of the O-O bond formation mechanism is, however, still ambiguous. It is not clear whether the O-O bond formation step proceeds via an RC or an AB mechanism. However, the ligand-field picture shown in Figure 2 favors an RC O-O bond formation reaction mediated by CoIV-O species. In the proposed octahedral coordination environment, the CoIV-O species will have an electronic configuration of d(xy)2 d(xz,yz)3, and correspondingly, as found in the spectroscopically characterized [CoIV(O)(TMG3tren)]2+ complex (Figure 12, inset) reported by Pfaff et al. (2011), the CoIV-O unit is expected to have predominant CoIII-O• character. Hence, an RC O-O bond formation reaction between the terminal oxo with a μ-oxo/hydroxo bridge in CoIV(O)(OH)(μ-O) CoIV(OH)2 is expected, which is also the mechanism presently favored by Nocera and coworkers (Surendranath et al., 2010; Nocera, 2012). In addition to the Nocera systems, there are few other reports of water oxidation catalysts based on cobalt-containing polyoxometalates (Yin et al., 2010; Huang et al., 2011) and cobalt-oxo clusters (McCool et al., 2011). However, detailed mechanistic studies have not been performed on these systems, and

thus, the mechanism of the O-O bond formation step is not well understood. Moreover, a recent study has shown that cobalt-containing polyoxometallates essentially act as precatalysts, providing an accessible source of cobalt ions for the formation of cobalt oxide amorphous materials under catalytic conditions, which function in a same way as the Nocera system (Stracke and Finke, 2011). The only existing mononuclear cobalt complex [CoII(OH2)Py5]2+, Py5=2,6-(bis(bis-2-pyridyl)-methoxymethane)-pyridine that is capable of driving O-O bond formation reaction comes from the group of Berlinguette (Wasylenko et al., 2011, 2012). The electrochemical behavior of [CoII(OH2)Py5]2+ in aqueous media has recently been studied in significant details. Cyclic voltammograms (CVs) recorded at various pH levels demonstrated that the Co(II) compound is oxidized electrolytically in a first step (via PCET) to furnish [CoIII(OH)Py5]2+. A second oxidation process was identified at ca. +1.4 V vs. NHE over the pH range 7.6–10.3, which was postulated to be indicative of a catalytic wave corresponding to water oxidation. A reaction rate coefficient (kcat) of ~79 s-1 for water oxidation was calculated. The proposed mechanism involves the oneelectron oxidation of [CoIII(OH)Py5]2+ followed by baseassisted deprotonation of [CoIV-OH(Py5)]4+ to yield [CoIV(O) Py5]2+. For the O-O bond formation step, an AB mechanism involving the nucleophilic attack of an incoming water/ hydroxide substrate to the [CoIV(O)Py5]2+ species has been favored. However, the proposed AB mechanism is not in agreement with a Co(IV)-oxo species in an octahedral coordination environment, which is expected to possess an electron-rich oxo group (Betley et al., 2008a,b; Siegbahn, 2008b) and therefore being not amenable to nucleophilic attack.

Nickel To the best of our knowledge, there is no homogeneous nickel complex reported in the literature functioning as a water oxidation catalyst (Du and Eisenberg, 2012). However, Nocera and coworkers have recently demonstrated O-O bond formation reaction in an oxygen evolution


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L Figure 12 O-O bond formation reactions mediated by cobalt phosphate and nickel borate films on inert electrodes (Dinca et al., 2010; Surendranath et al., 2010; Bediako et al., 2012). The inset shows the structure of the only known spectroscopically characterized high-valent Co(IV)-oxo species in the literature (Pfaff et al., 2011).

catalyst that forms as a thin film from Ni(aq)2+ solutions containing borate electrolyte (Ni-Bi) (Figure 12) (Dinca et al., 2010; Bediako et al., 2012). In situ XAS (Risch et al., 2011; Bediako et al., 2012) reveals that the activated catalyst films comprise bis-oxo/hydroxo-bridged nickel centers organized into sheets of edge-sharing NiO6 octahedra. Moreover, coulometric measurements correlated with XANES spectra of the active catalyst show that the nickel centers in activated films possess an average oxidation state of +3.6, indicating that a substantial proportion of nickel centers exist in a formal oxidation state of Ni(IV). In contrast, nickel centers in nonactivated films were found to exist predominantly as Ni(III). The nickel-based system is therefore structurally and functionally similar to that of the Co-Pi catalyst reported before. Accordingly, an RC O-O bond formation reaction has also been proposed for the Ni-Bi catalyst, similar to the Co-Pi system.

Copper To date, there is no direct evidence for copper-mediated O-O bond formation reactions in biology. However, it is well established that binuclear copper enzymes such as tyrosinase and catechol oxidase adopt the side-on μ-η2:η2peroxo structure, as do a large number of synthetic model complexes (Halfen et al., 1996; Tolman, 1997; Hatcher and Karlin, 2004; Mirica et al., 2004). Moreover, from theoretical calculations (Cramer et al., 1996; Henson and Mukherjee, 1999; Spuhler and Holthausen, 2003) the free

energy of the μ-η2:η2-peroxo-binding motif has been demonstrated to be very small as compared with that of the high-valent dicopper(III) bis μ-oxo species, which predicts a low barrier for interconversion between the two forms (Figure 13). This is experimentally observed in many synthetic systems where the side-on peroxo dicopper(II) and bis μ-oxo dicopper(III) coexist in a dynamic equilibrium, which is strongly influenced by the nature of the ligand and reaction conditions including concentration, counterion, temperature, and solvent (Halfen et al., 1996; Tolman, 1997). Thus, oxygenation of the Cu(I) complex [LiPr3CuI(CH3CN)](O3SCF3) (LiPr3=1,4,7-triisopropyl-1,4,7-triazacyclononane) in tetrahydrofuran (THF) at -78°C yields [(LiPr3Cu)2(μ-O)2] (O3SCF3)2. However, dilution of the THF solution with dichloromethane (CH2Cl2) results in the radical coupling of the two bridging oxos in [(LiPr3CuIII)2(μ-O)2] (O3SCF3)2 to yield the [(LiPr3CuII)2(μ-O2)] (O3SCF3)2 species (Halfen et al., 1996). As side-on μ-η2:η2peroxo bindings are extremely common in biological systems (Figure 13, inset), the above-described reversible O-O bond formation and cleavage steps may also be taking place in metalloenzymes.

Conclusion and future challenges The photoproduction of hydrogen and oxygen from water and sunlight represents an attractive means of artificial energy conversion for a world still largely dependent on fossil fuels. A practical technology for producing solar-



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Figure 13 Reaction demonstrating the solvent dependent interconversions between the [(LiPr3CuIII)2(μ-O)2] and [(LiPr3Cu)2(μ-O)2] forms (Halfen et al., 1996). The inset shows the side-on μ-η2:η2-peroxo core observed in oxy-hemocyanin (Hatcher and Karlin, 2004).

derived hydrogen remains an unachieved goal, however, and is dependent on developing a better understanding of the key step, the O-O bond formation reaction leading to the oxidation of water to dioxygen. The recent results presented here from the bioinorganic chemistry community lend credence to the participation of high-valent manganese and iron oxo species in the O-O bond formation reaction in PSII and Cld, respectively. Moreover, the ability to form O-O bonds was found to be not only unique for oxomanganese or oxo-iron units but could also be extended to other mid- to late-transition metals. The mechanism of the O-O bond formation step, however, differs depending on the nature of the transition metal involved. In a valencebond picture, a [MO](n-2)+ unit can be described as a resonance hybrid of two contributing forms: Mn+=O↔M(n-1)O•. The oxometal complexes of first-row late-transition metals such as Co, Ni, and Cu have a major contribution of the M(n-1)O• form owing to the strong electron-electron repulsion (Limberg, 2009) between the electron-rich oxo and the filled d(xz,yz) π*-levels of the central metal. Correspondingly, oxometal complexes of Co, Ni, and Cu perform O-O bond formation predominantly by an RC mechanism. For Fe and Mn, on the other hand, both AB and RC mechanisms are feasible depending on the oxidation state of the central metal ion. Mn(V) and Fe(V) favor an AB mechanism, whereas an RC mechanism is favored by Mn(IV) or

Fe(IV). This trend is also found to be valid for the heavier congeners: an AB mechanism is demonstrated for RuVO (Concepcion et al., 2008; Romain et al., 2009), RuVIO (Romain et al., 2009), or IrVO (Hull et al., 2009; Vilella et al., 2011) and an RC mechanism for RuIVO (Romain et al., 2009; Wasylenko et al., 2010). Additional factors such as hydrogen bonding interactions or base-assisted reactions can also play a vital role in the O-O bond formation step. In PSII (Siegbahn, 2008c; Umena et al., 2011; Grundmeier and Dau, 2012) and in some molecular catalysts (Privalov et al., 2007; Sameera et al., 2011), such interactions are proposed to result in a strongly delocalized system, where the Mn+=O and M(n-1)O• forms contribute equally in the equilibrium. In such cases, it is not possible to discern between the AB or RC mechanism. As both the AB and RC mechanisms are possible for the O-O bond formation reactions mediated by iron and manganese centers, a detailed knowledge of the active species responsible for the O-O bond formation step is warranted so as to make an unambiguous assignment of the mechanism. However, there are no reports of the successful trapping of the proposed oxo-Mn(V) or oxoFe(V) intermediates in PSII and Cld, respectively, which are responsible for the O-O bond formation step leading to the eventual release of dioxygen. Although a Mn(V)oxo species has been recently shown to be capable of


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initiating an O-O bond formation reaction, direct evidence of the involvement of oxo-Fe(V) units in O-O bond formation is lacking in the literature. The spectroscopically characterized [(TAML)FeV(O)]- anion (Hohenberger et al., 2012), which is the only known oxo-Fe(V) species in the literature, has not been tested on its ability to initiate an O-O bond formation reaction. An RC oxo-Fe(IV)-mediated O-O bond formation step has, however, been recently demonstrated, which supports a similar mechanism for the dinuclear Ru-Hbpp water oxidation catalyst reported by Llobet and Romain (2009). In summary, the ambiguity related to the nature of the active species has led to a lot of controversy regarding the mechanism of the Fe- and Mn-mediated O-O bond formation reactions in chemistry and biology. Future efforts

should, therefore, be dedicated toward the characterization of the active species responsible for the O-O bond formation step, including all relevant higher oxidation states, intermediates, and transition states. Only then an unambiguous assignment of the mechanism will be possible, which may provide vital insights into the prerequisites necessary for the design and discovery of cheap and efficient artificial catalysts for water oxidation. Acknowledgments: S.K. and K.R. gratefully acknowledge the financial support from the Cluster of Excellence ‘Unifying Concepts in Catalysis’ (EXC 314/1). M.S. thanks the DFG (SCHW 1454/41-1) for funding. Received May 15, 2012; accepted June 8, 2012

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