The Origin and Evolution of Photosynthetic Oxygen

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C. Existing Organisms that May Be Transitional Forms . .... Abbreviations: EPR – electron paramagnetic resonance; EXAFS. – extended x-ray absorption ...
FIRST PROOF

Editor: Wydrzynski

Chapter 30 The Origin and Evolution of Photosynthetic Oxygen Production G. Charles Dismukes*

Department of Chemistry and Princeton Environmental Institute, Princeton University, Princeton, NJ, [zipcode please] U.S.A.

Robert E. Blankenship

Department of Chemistry and Biochemistry, Arizona State University, Tempe, AZ 85287-1604, U.S.A.

Summary ................................................................................................................................................................... 2 I. The Timetable and Biogeochemical Consequences of Oxygenic Photosynthesis ............................................. 2 II. Minimal Cofactor Diversity in Water Oxidizing Complexes ................................................................................ 3 A. Polypeptide Binding Site ....................................................................................................................... 3 B. The Inorganic Cofactors ........................................................................................................................ 4 1. Manganese and Calcium ............................................................................................................. 4 2. Role of Bicarbonate in the WOC.................................................................................................. 4 III. Transitional Electron Donors and ‘Missing Links’ ................................................................................................ 5 A. Was There a Transitional Electron Donor Before Water? ...................................................................... 5 B. Electron Donors in Anoxygenic Bacteria ............................................................................................... 5 C. Existing Organisms that May Be Transitional Forms ............................................................................ 6 IV. Possible Evolution Pathways for PS II-WOC ...................................................................................................... 6 A. Chemical Speciation in the Archean Ocean: Mn2+ and HCO3– ............................................................. 6 B. Redox Properties of Mn-Bicarbonate .................................................................................................... 8 C. Thermodynamics of Oxygen Production from Bicarbonate versus Water ............................................. 9 D. Mineral Building Blocks/Remnants of Oxygenic Photosynthesis? ........................................................ 9 E. Bicarbonate as Evolutionary Substrate and Cofactor for Mn Core Assembly ......................................10 V. Concluding Remarks .........................................................................................................................................11 Acknowledgments.....................................................................................................................................................11 References ...............................................................................................................................................................11

Typesetter’s note: This chapter should not have been sent to me as it does not appear to be a final version. The in-text references were incorrectly done and the end references were formatted incorrectly and using some bizarre scheme that necessitated redoing almost all of them. One entire section of the paper is missing (V. Concluding Remarks). I’ve marked problems I could not solve.

*Author for correspondence, email: [email protected] T. Wydrzynski and K. Satoh (eds): Photosystem II: The Water/Plastoquinone Oxido-Reductase in Photosynthesis, pp. 000–000. © 2005 Springer. Printed in The Netherlands.

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G. Charles Dismukes and Robert E. Blankenship

Summary This chapter reviews some of the evidence and the postulated proposals for how oxygenic photosynthesis first emerged as a distinct form of photoautotrophic metabolism using water as an electron donor. This form of photosynthesis is the most successful photoautotrophic metabolism in the contemporary biosphere and is found in all higher plants, green and red algae and both cyano- and oxyphoto-bacteria. We summarize the timetable for emergence and the biogeochemical consequences of oxygenic photosynthesis. Particular attention is paid to evolution of the inorganic core of the enzyme that catalyzes water oxidation, chemical speciation of the inorganic cofactors and possible alterative substrates. We discuss possible mineral remnants of early oxygenic photosynthesis and the emerging role of bicarbonate in assembly of the inorganic core and as an hypothesized evolutionary cofactor. I. The Timetable and Biogeochemical Consequences of Oxygenic Photosynthesis The history of life on Earth since the beginning of the universe following the ‘big bang,’ can be traced through a number of biological ‘innovations’ that, like the geochemical beginning, had profound global impact. The innovation of anoxygenic photosynthetic metabolism probably occurred at an early stage following the beginning of chemosynthetic metabolism. (Des Marais, 2000) It enabled light energy to be utilized to drive unfavorable oxidation-reduction reactions using easily oxidizable reductants that yielded electrons of higher potential energy and chemiosmotic energy derived from proton gradients. Photosynthetic metabolism thrived in the early Archean era as reduced substrates (e.g., Fe2+, S2–, reduced carbohydrates, etc.) and CO2 were in great abundance. Geochemical evidence shows that these sources waned throughout the Archean era, (Holland et al., 1998) resulting in global depletion of the soluble electron donors and CO2 in the regions where anoxygenic photosynthesis once ruled. This consumption/loss of easily oxidizable substrates set the stage for the innovation of oxygenic photosynthesis in which water became the source of electrons and protons and oxygen gas formed as by-product. During the late Archean era, the concentration of atmospheric O2 rose dramatically circa 2.3 billion years ago (BYA) based on evidence from multiple chemical markers and microfossils. (Holland, 1984; Holland et al., 1998). This rise is almost universally attributed to photosynthetic O2 production from water, (Cloud, 1972; Holland et al., 1998; Abbreviations: EPR – electron paramagnetic resonance; EXAFS – extended x-ray absorption spectroscopy; OEC – oxygen evolution complex; PS II – Photosystem II; WOC – water oxidizing complex; XRD – X-ray diffraction

Farquhar et al., 2000; Kasting et al., 2002), although alternative theoretical hypotheses exist (Catling et al., 2001). There is also a minority view that states that the concentration of oxygen in the atmosphere has been substantial throughout all or most of the Earth’s history (Towe, 1994; Ohmoto, 1997; Lasaga et al., 2002). Cyanobacteria are the generally accepted source of the rise in atmospheric O2. This view is consistent with evidence from biomarkers that date to 2.7 BYA (Summons, 1999). Although photosynthesis is the accepted metabolic source of the archean atmospheric O2 flux, the pioneer oxyphotobacteria that invented water splitting chemistry have never been identified. However, it is also not clear that the 2.7 BYA organisms that produced the biomarkers that today are specific for cyanobacteria were themselves cyanobacteria with true oxygenic photosynthesis, or were rather the ancestors of these organisms that had not yet developed the capacity for water splitting, or possibly another bacterial line that has since gone extinct. So the precise date for the invention of oxygenic photosynthesis is not known from geological data, but a reasonable estimate is sometime between 2.7 and 2.3 BYA. An estimate based on molecular phylogeny is consistent with this, at 2.6 BYA (Hedges, 2001). The innovation of oxygenic photosynthesis set in motion a biological ‘big green bang’ that profoundly and forever transformed the Earth’s atmosphere and surface. The capacity to split water in the pioneer oxyphotobacteria freed photosynthesis to invade new environments. For the first time, photosynthesis had an unlimited source of electrons and protons by using water as reductant. Because water was distributed everywhere, oxygenic photosynthesis could now emerge on terrestrial habitats. This transformed the face of the Earth from a drab inorganic alumino-

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Origin and Evolution of Oxygen Production

silicate surface to a luscious organic green carpet of chlorophyll and other pigments. Oxygenic photosynthesis breathed copious amounts of O2 gas into Earth’s anaerobic atmosphere, transforming it into one suitable for the emergence of aerobic metabolism. As gaseous O2 accumulated in the atmosphere, new opportunities opened for heterotrophic organisms to evolve mechanisms that make direct use of oxygen via non-photosynthetic respiratory metabolism. Because aerobic metabolism has a much higher energy efficiency per substrate oxidized, the engine of life became supercharged. Photosynthetic oxygenation of the Earth’s atmosphere provided the metabolic oxidant that powered this biological explosion and permitted the evolution of all complex organisms, including humans. So, how did oxygenic photosynthesis emerge and are there multiple classes of photocatalysts for splitting water, much like there are numerous examples of anoxygenic photoautotrophism? Surprisingly, the available species of oxygenic photoautotrophs examined to date (cyanobacteria, green algae and higher plants) contain an inorganic catalyst having identical composition (Mn4Ca1OxCly), despite having evolved for circa 2.7 billion years. The water splitting reaction catalyzed by the contemporary WOC is a complex, concerted (all-or-nothing) four-electron step that is thermodynamically efficient. No other ‘molecular blueprint’ for this catalyst has been identified and no firm evidence for transitional Photosystem II water-oxidizing complexes (PS II-WOC) yet exists that can use other substrates for oxygen production. (Blankenship, 2002) It thus seems that the invention of oxygenic photosynthesis was a ‘singular event.’ The invariance of the inorganic catalyst in all contemporary oxygenic photoautotrophs indicates either an exceptionally rare example of biological non-adaptation over this vast geological period, or, more likely, the evidence for alternative catalysts has not yet been uncovered. Identification of the ‘missing links’ that served as transitional organisms in the evolution of the oxygen-producing photoautotrophs (cyano- and oxy-photobacteria) is based largely upon scant genomic and geochemical evidence which we review herein. Lastly, we consider how the geochemical composition of the early Earth’s atmosphere and oceans could have had a major influence in the emergence of oxygenic photosynthesis via adoption of bicarbonate as the transitional electron donor prior to water. Several essential questions need to be answered

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concerning the evolutionary process that led to water oxidation in photosynthesis. First, were transitional electron donors used by the first oxygen-producing phototrophs before water was adopted as the universal reductant (Olson, 1970, 2001; Blankenship et al., 1998). Second, how did the PS II photochemical apparatus evolve to generate a sufficiently strong oneelectron photooxidant as precursor to chlorophyll a found in all contemporary PS II organisms? Third, while the current day mechanism of O2 evolution from water produces no free, partially oxidized, intermediates, (i.e., is a concerted four-electron process), this may well not have been the case initially. How did the early system survive, as it was probably producing compounds, including the oxygen final product, that it or any other life forms were not equipped to deal with? Finally, did the linkage of the two types of reaction centers to form the tandem arrangement found today in all oxygenic photosynthetic organisms come before or after the development of the ability to make oxygen? We currently do not have adequate answers for any of these questions, so this entire area of research is still in its infancy. II. Minimal Cofactor Diversity in Water Oxidizing Complexes A. Polypeptide Binding Site The X-ray diffraction map of the PS II-WOC from two strains of Thermosynechococcus reveals 36 trans-membrane α-helices assigned to 17 protein subunits. (Zouni et al., 2001; Kamiya et al., 2003) The map reveals the location of the major reaction center subunits (D1 and D2), the two inner antennas (CP47, CP43), the two subunits of cytochrome b559, four unassigned transmembrane α-helices (genes Psb J, K L and X) and the two extrinsic subunits (the manganese-stabilizing protein or PsbO and cytochrome C550). The Mn-cluster is surrounded primarily by the lumenal surface of the D1 protein, as predicted by previous mutational studies (Diner, 1998, 2001; Debus, 2000, 2001) and model building (Dismukes, 1988; Svensson et al., 1996). The side chains of the specific residues involved in Mn coordination have not been fully resolved or modeled yet, but the location of the peptide backbones of the five trans-membrane α-helices of D1 were located and the extensions of these backbones into the lumenal aqueous space sur-

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rounding the Mn cluster could be discerned. In both structures the location of the Mn cluster is within 10 Å to four or five lumenal domains of the D1 protein. The complexity of the emerging protein structure indicates that no single domain of the D1 protein comprises the binding site for the inorganic core. B. The Inorganic Cofactors 1. Manganese and Calcium The inorganic components of the catalyst responsible for oxygen evolution are Mn4OxCa1Cl y in all photosynthetic organisms studied to date, including higher plants, green algae and cyanobacteria. (Debus, 1992; Raven et al., 1999; Ananyev et al., 2001); (Vrettos et al., 2001). A range of ten allowed core structures has been inferred from XRD, EXAFS and EPR studies. (Robblee et al., 2001; Zouni et al., 2001; Carrell et al., 2002; Kamiya et al., 2003) All of these structures formulate the catalyst as having a tetramanganese core, while the EXAFS and EPR data further indicate oxo/hydroxo-bridges between the Mn ions that enable intermanganese electronic coupling essential for the multi-electron catalysis. Several core geometries are compatible with the available electron density and magnetic resonance data for the reduced core, including a funnel-shaped-Mn4O4(OHx)2 core and a Mn4O2(OHx)2-butterfly/cubane core(Carrell et al., 2002). EPR and EXAFS studies further indicate that Ca2+ is an integral cofactor of the core. Although not yet resolved in the XRD maps, the EPR and EXAFS data indicate a possible location that is juxtaposed to the Mn4 cluster, possibly as a capping Ca(OX)2 unit bridging between a pair of Mn atoms. Removal of Ca2+ lowers the Mn ionization potential and alters the strength of the intermanganese coupling to a degree that water splitting activity is lost. Strontium is the only other element that can replace Ca2+ in water splitting, albeit with 35% lower steady-state rate of O2 evolution. (Boussac et al., 1988) No naturally occurring inorganic mutants have yet been observed in the environment. Several proposals exist for how these physico-chemical properties are important for catalysis (see other chapters [Author, please list the corresponding chapters or delete]). 2. Role of Bicarbonate in the WOC Biogenesis of the inorganic core of the WOC occurs in vivo by ligation and photo-oxidation of Mn2+

G. Charles Dismukes and Robert E. Blankenship to apo-WOC-PS II in the presence of the other elementary inorganic ions: Ca2+, Cl–, H2O or HCO3–. This process, called photoactivation after Cheniae, creates a functional catalyst (reviewed in Chapter 14). Bicarbonate was found to stimulate the rate and yield of the first step of photoassembly involving photooxidation of Mn2+ in spinach(Baranov et al., 2000, 2004). The data clearly establish that the high affinity Mn2+ site in PS II has a specific interaction with bicarbonate with a binding constant that is orders of magnitude larger than is the affinity between Mn2+ and bicarbonate alone. Bicarbonate/carbonate is also a weak chelating ligand that leads to the formation of Mn2+-bicarbonate/carbonate complexes in solution. (Dismukes et al., 2001) Paradoxically, formation of these free complexes in solution (> 1 mM) does not stimulate the photoassembly process in spinach apoWOC-PS II, but rather actually slows the assembly rate and lowers the yield of active centers (Baranov et al., 2004). This decrease is attributed to electron donation to PS II by free Mn-bicarbonate complexes in solution that compete with the native site. The photoassembly data suggest a possible evolutionary role for bicarbonate in promoting selectivity for Mn2+ binding and photooxidation by apo-WOCPS II over other divalent metals. Geochemical evidence indicates that the ferrous ion was considerably more concentrated in the anaerobic archean seas than it is today in oxygen-rich seas. So how does PS II discriminate between Mn2+ and Fe2+, particularly since the Fe2+ concentration is likely to have been higher than Mn2+ in an anaerobic world? The answer appears to be that the high affinity Mn2+ site in the apo-WOC-PS II is tailored to bind [Mn2+(OH–)]+ or [Mn2+(HCO3–)]+ instead of Mn2+aq ions. This is seen in the size and charge density selectivity for inhibition of photoassembly. (Ananyev et al., 1999) For example, the alkali metal ions inhibit the first step in photoassembly according to their size (Cs+ >Rb+ >K+ >Na+ >Li+) with Cs+ affinity being comparable to Mn2+ affinity and 3000 fold higher affinity constant than Li+. Similarly, large metal-oxo cations (VO2+, UO22+) are among the most potent inhibitors of photoassembly. (Ananyev et al., 2001) Fe2+ inhibits photoassembly and when used in mixed ratios with Mn2+ blocks photoassembly of active WOC centers without added bicarbonate. (Ananyev et al., 2001) The dissociation constants for Mn2+ and Fe2+ as steady-state electron donors (i.e., multi-electron turnover) to apo-WOCPS II are about 1 and 2 μM, respectively, without added bicarbonate. (Semin et al., 2002) Atmospheric

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dissolved CO2 gives about 10 μM bicarbonate at pH 6, which is already enough to partially stimulate electron donation by Mn2+ (bicarbonate KD = 20–34 μM). (Klimov et al., 2001) Upon increasing the bicarbonate concentration to saturating value the Mn2+ affinity increases, as seen by a decrease in the Michaelis constant. This increase in Mn2+ affinity is also seen in photoassembly kinetics and yield. Thus, the ternary complex of Mn2+-bicarbonate-apo-WOC is recognized rather than the free ion. Studies of the bicarbonate effect on electron donation by Fe2+ have not yet been done to see whether bicarbonate can aid discrimination between Mn2+ and Fe2+. The mechanism of Fe2+ inhibition of Mn2+ photoassembly is due to competitive photooxidation of Fe2+ which binds tightly to the apo-WOC-PS II complex but can be removed by use of excess reducing agents.[Semin, 2002 #2132—what is this???] Bicarbonate also enhances the thermal stability of the holo-WOC-enzyme isolated as detergent extracted PS II membranes possibly by preventing protein denaturation. (Klimov et al., 2001) The rate of thermoinactivation at 40 °C was shown to decrease by 3 fold in the presence of bicarbonate. This greater thermal stability could have been important for the emergence of the first WOC in the archean era when the average temperature was predicted to have been considerably warmer than the mean temperature over the last 20,000 years. III. Transitional Electron Donors and ‘Missing Links’ A. Was There a Transitional Electron Donor Before Water? An appealing idea that was first advanced by Olson (Olson, 1970) is that transitional electron donors may have existed in early organisms, and that a series of donors of increasing redox potential may have existed. In this view, the system slowly gained the ability to oxidize weaker and weaker reductants until it eventually was able to use water as an electron donor. Olson (Olson, 1970) proposed a series of nitrogen compounds, including hydrazine and hydroxylamine as transitional donors. Other authors have proposed other compounds, including hydrogen peroxide (Blankenship et al., 1998) and Mn bicarbonate complexes (Dismukes et al., 2001).

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T he driving force for all these proposals is that the jump in capabilities of the reaction center is so huge to permit it to use water as an electron donor that it is difficult to imagine how this process might have taken place while preserving a functional system. This is analogous to the classic problem of the evolution of the eye, addressed by Darwin and countless others. How can such a complex organ as an eye ever evolve if selection can only work to improve a system that functions already? The eye of a complex animal like a human is such that all the parts are required to make it functional, so how could it possibly have arisen and evolved? Darwin himself advanced the answer to this question, which is still valid today. The complex eye of humans did not appear in one jump from nothingness. Rather, a whole series of light-sensitive organs can be identified in simpler organisms, each of which is of immense benefit to the organisms that possess them. The old saying, ‘In the land of the blind, the one-eyed man is king,’ describes graphically how much benefit even a primitive light sensing system will be to the only organism that possesses it. The evolution of the eye can thereby easily be traced from the most rudimentary light sensitive spot in microorganisms through nonfocusing eyes of invertebrates all the way to the incredibly sophisticated human eye. The same logic applies so that an organism that has even a rudimentary system to oxidize water or other ubiquitous substrates will be at a huge selective advantage, provided that it doesn’t kill itself with the toxic products of this newly acquired activity. B. Electron Donors in Anoxygenic Bacteria We will now examine the sorts of substrate oxidation systems that can be identified in known photosynthetic organisms, and consider whether any of these could possibly be intermediates in the development of the WOC. Unfortunately, none of these systems turn out to be very helpful in understanding the origin of the WOC. Anoxygenic bacterial phototrophs use a variety of substrates that donate electrons to the photooxidized reaction center. These include Fe2+, H2S, Sx, numerous reduced carbon sources and others. Even some cyanobacteria can use H2S as an electron donor, thereby carrying out a form of anoxygenic photosynthesis driven by Photosystem I (Cohen, 1986). However, these organisms also still retain the complete mechanism for carrying out water oxidation, so are probably best considered as more recent adaptations to sulfide

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rich environments rather than transitional forms. The nature of the catalysts that mediate all these substrate oxidations in anoxygenic bacterial photosynthesis is relatively poorly understood. The best understood of these donor capabilities is the system that uses sulfur compounds as electron donors (Brune, 1995), while the specific proteins and cofactors that are involved in Fe2+ oxidation are completely unknown. In some cases, such as sulfur oxidation, donation appears to occur at the level of the quinone pool, so that reducing equivalents do not directly interact with the oxidized reaction center. Nothing that is known about any of these donation systems suggests that they may have been adapted by evolution to form the WOC. Sulfur oxidation in these organisms is mediated by soluble enzymes that have no apparent cofactor or mechanistic similarity to how oxygen is produced from water oxidation in the integral membrane reaction center protein of PS II. At the current level of knowledge of these systems, there are no clues to how the WOC originated or evolved. C. Existing Organisms that May Be Transitional Forms One type of organism has recently been discovered that may possibly be a transitional form between anoxygenic and oxygenic photosynthesis, although it too might in the end turn out to be an adaptation to a particular environmental niche. The Chl-d containing cyanobacterium Acaryochloris marina was discovered as a symbiont in a marine ascidian (Miyashita et al., 1996). It contains Chl d as its principal photopigment, although it also contains traces of Chl a. Chl d has been suggested as a possible transitional pigment between bacteriochlorophyll a and Chl a (Blankenship et al., 1998), because it is both structurally and energetically intermediate between these two pigments. For this reason, this organism or others like it may be critical in understanding the transitional forms that almost certainly had to have existed. The absorbance maximum of Chl d is intermediate between those of BChl a and Chl a, with the major in vivo maximum at 710 nm. Biochemical and spectroscopic studies by (Hu, 1998) have clearly shown that the Photosystem I complex contains only Chl d, including as the photoactive special pair, which absorbs at 740 nm in this organism. It is not yet certain whether the Photosystem II complex also utilizes Chl d, which is the more important point for the purposes of this discussion. There is conflicting

G. Charles Dismukes and Robert E. Blankenship evidence on this point (Mimuro et al., 1999; Itoh et al., 2001). IV. Possible Evolution Pathways for PS IIWOC All evidence to date indicates that the biogenesis of the inorganic core of the WOC in extant phototrophs does not require the binding of ‘ready-made’ Mn clusters from solution, but rather occurs by photoassembly from the free inorganic constituents. Additionally, there is no evidence for chemical extraction of a whole or partial Mn cluster from the intact WOC from any organism. Extraction of the inorganic core from PS II leads to cluster fragmentation, suggesting it may be an intrinsically unstable core in the absence of suitable ligands. Hence, efforts to identify novel manganese minerals as natural building blocks for biosynthesis of the core or as remnants of a decomposed photosynthetic core have not been essential, based on the currently available evidence. In sections D and E of part V we examine a few novel proposals that have been postulated for how natural Mn minerals or soluble Mn clusters could have ‘jump-started’ the evolution of oxyphotobacteria in the early geochemistry of the Earth. We begin by discussing the question of availability and speciation of Mn in the archean seas (A) and relate this to the redox chemistry of Mn, bicarbonate and water (B and C). A. Chemical Speciation in the Archean Ocean: Mn2+ and HCO3– The inorganic composition of ‘Darwin’s little pond’ that spawned the first oxygenic phototroph in the archean era is not likely to ever be known accurately. Hence, we focus on the average composition of the early oceans and ask: did these constitute a permissive habitat for oxygenic photosynthesis to emerge? Geochemical markers indicate that the archean seas had different chemical composition, pH and temperature than the contemporary seas that foster photosynthetic life (Table 1). (Dismukes et al., 2001) The pH of the archean oceans is predicted to have been 1–4 pH units lower than the contemporary oceans, based on evidence from archean ferruginous cherts (Sugisaki et al., 1995) and model calculations (Grotzinger et al., 1993; Morse, 1998) It is generally accepted that the CO2 partial pressure in the atmosphere has fallen by many orders of

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Table 1. Composition of the Archean ocean and atmosphere Component Contemporary Archean (>2.2 BYA) PCO2 , atmosphere (kPa) 0.03 O.9a, 9b, 900c HCO3– seawater (mM) 2 10-200 (5–100×)e 2+ d Mn , seawater (mean) (ng/kg) 20 40-100 (2–5×)f 2+ 2+ Mn speciation in seawater Mn aq [Mn(HCO3 )2]n (g) pH 8.1 4~7 a,h a b c d Holland (1984), Kasting (1993), Walker (1985), Bruhland (1983), e estimation from atmospheric CO2 using equilibrium data, f Precambrian vs Phanerozoic limestones (Holland et al., 1998), g predicted archaean speciation based on binding constant data in Table 2: +  Mn ( HCO3 )2  Mn ( HCO3 ) n = 0.6 − 12; = 0.11 − 48 2+ Mn Mn 2 + , h Archean ferruginous cherts (Sugisaki et al., 1995) and CO2 dissolution (Grotzinger et al., 1993).

magnitude since the formation of the atmosphere. Models predict that the partial pressure of CO2 fell continuously throughout the Hadeon era (4.3–3.8 BYA) from a maximum value of 10 atm to about 0.5 atm (Morse, 1998) Biogeochemical evidence indicates that the partial pressure of CO2 in the archean era was drawn down by photosynthetic carbon fixation, yet was 30 to 3 × 104-fold greater than the contemporary atmosphere. This greatly elevated CO2 level is consistent with the predicted lower archean pH, owing to formation of carbonic acid. The predicted concentrations of dissolved carbonic acid and bicarbonate in the archean seas were proportionately higher (Table 1) based on estimates from the Henry’s law constant for CO2 dissolution in water and the proton equilibrium constants. A key consequence of the elevated bicarbonate concentration is that certain metal ions will speciate in solution as the metalx-bicarbonatey complex in preference to the metal-aquo complex. As a result of the lower archean pH, precipitation of the insoluble metal-carbonate/hydroxide minerals is suppressed, thus leading to increased concentration of the metalbicarbonate complexes in solution. The favorable oxidation potentials of the resulting Mn-bicarbonate species enables them to serve as electron donors to photosynthetic prokaryotes. This shift in Mn-bicarbonate speciation with pH can be calculated using the thermodynamic phase equilibria for the ternary water/Mn/CO2 system at the CO2 fugacity of both the current atmospheric (approximately equal to the mean fugacity since the last ice age) and the estimated archean fugacity (3000-fold higher; 105 Pascal) (see for example Fig. 24 in Russell et al. (2003). In this calculation the association constant for the formation of the

1:1 Mn2+(HCO3–) complex reported in the literature was used (Table 2). Two features emerge from this analysis. As a result of the lower pH, the boundary between aquo-Mn2+ and rhodochrosite, MnCO3(s), drops by two pH units to 6.5, corresponding to the lower limit imposed by the buffering due to carbonic acid/bicarbonate equilibrium (pKa = 6.3). As a result of the elevated bicarbonate concentration in solution, thermodynamic equilibrium predicts that a window of 1 pH unit now supports the existence of Mn2+(HCO3–) as the major soluble Mn2+ species at the phase boundary between aquo-Mn2+ and rhodochrosite. Using a concentration of 1 μM for the total dissolved Mn2+, the equilibrium calculation predicts that the concentration of [Mn2+(HCO3–)]+ exceeds that of aquo-Mn2+ between pH 6.5 and 7. Thus, it can be concluded from elementary thermodynamic considerations that the archean oceans would have provided more favorable conditions than the contemporary oceans for the speciation of soluble (Mn2+)x(bicarbonate)y complexes as the dominant forms of soluble Mn2+. Electrochemical data for the reduction of aqueous Mn2+ solutions to Mn0 as a function of ligand concentration further suggest that bicarbonate is capable of forming two Mn-bicarbonate species with stoichiometries 2:1 and 1:2, corresponding to complexes with empirical formulas, MnII2(HCO3)3+ and [MnII(HCO3)2]n. (Dismukes et al., 2001) Thus, oligomeric Mn-bicarbonate complexes may also have existed in the Archean seas in sufficient abundance at pH values close to the rhodochrosite precipitation boundary. The two component system of CO2/water has a much higher buffer capacity than pure water and as a result can serve as an abundant source of bicarbonate ions within the pKa range of bicarbonate (6.3–10.3).

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Table 2. Manganese-bicarbonate physico-chemical data Mn(II) species

E0 (V, NHE) for oxidation b

Catalase Activityc

Mn2+aq.

KB HCO3– binding, M–1 –

1.20

zero

[Mn2+(HCO3–)]+

11–60a,b

0.92. irrev.

?

[Mn (HCO3 )2]n

4 –20

0.52–0.61 irrev.

active

2+

–

b

Smith et al. (1976), b Kozlov et al., 1997; Dismukes et al. (2001), c catalysis of peroxide dismutation: 2 H2O2 → 2 H2O + O2, d Stadtman et al. (1990). a

For each mole of CO2 that is dissolved in water only 8.6 kcal/mol are required for dissociation into bicarbonate and proton, whereas dissociation of one mole of water to hydroxide and protons requires 21.4 kcal/mol. Hence, any system that can use bicarbonate as a source for generation of hydroxide will need to input only 8.9 kcal/mol to release it from CO2, versus 21.4 kcal/mol to ionize pure water. Moreover, if the system can use bicarbonate as a direct surrogate for hydroxide than no further energy input is needed in the two component system! This energetic advantage of bicarbonate as a source for hydroxide can be equivalently expressed in terms of the dissociation constants: H2O ↔ H+ + HO – + K = 2 × 10–15 HCO3– ↔ CO2 + HO– K = 2.8 × 10–7 In other words, at neutral pH a solution containing 0.1M bicarbonate ion will contain 106-fold more bicarbonate ion than the concentration of hydroxide ion in pure water. The measured stability constants for the formation of Mn-bicarbonate complexes (Table 2) together with estimates for the Mn2+aq concentration in the Archean ocean (Table 1) indicate that these Mn-bicarbonate complexes would have represented the dominant form of soluble Mn2+ present in the Archean ocean, unlike today where the speciation favors the monomeric aquo ion Mn2+aq. The pKa of Mn2+aq is 10.5. Hence, at the pH of the contemporary ocean (~ 8) the fractional concentration of Mn(OH)+ would be vanishingly small (10–2.5 × Mn2+aq) if there was no bicarbonate to serve as hydroxide source. In the Archean ocean (pH ~4-7) it would have been even smaller. Thus, bicarbonate, not free hydroxide, is the major source of hydrolytic species formed from Mn2+aq, including Mn(OH)+, in both the contemporary and Archean oceans.

B. Redox Properties of Mn-Bicarbonate Electrochemical oxidation of these MnII-bicarbonate complexes in the presence of excess bicarbonate leads to formation of MnIII-bicarbonate complexes at much more favorable potentials (Table 2) than for Mn2+aq (E0 = 1.18 V). (Kozlov et al., 1997) Importantly, other coordinating ligands (Cl–, NO3–, formate, acetate) form only 1:1 complexes with Mn2+ and these do not exhibit such favorable oxidation potentials. The electrochemical data do not reveal whether bicarbonate binds to manganese or delivers hydroxide to form the corresponding Mn-hydroxo/oxo species. These potential shifts are sufficiently large that they would enable Mn-bicarbonate clusters to function as electron donors to reaction centers from anoxygenic phototrophs utilizing BChl a as their primary photooxidant. (Dismukes et al., 2001) Evidence in the literature shows that solutions of Mn2+ and bicarbonate catalyze the two-electron dismutation of hydrogen peroxide (H2O2 → O2 + 2H2O), or the so-called catalase activity. (Stadtman et al., 1990; Sychev et al., 1993) The rate of Mn-dependent dismutation depends on the bicarbonate concentration to the third power, suggesting the formation of an active species with 1:3 Mn:bicarbonate stoichiometry. Electrochemical evidence suggests the active species could be dimanganese-bicarbonate complexes or oligomers. (Dismukes et al., 2001) It is also known that all manganese catalases, which are found exclusively in prokaryotes, contain dimanganese centers. Similarly, all efficient abiotic manganese catalase model complexes contain di- or multi-manganese centers. In summary, coupled proton-electron transfer chemistry of H2O2 occurs most efficiently via dimanganese centers than mono-manganese centers and the former use the Mn2(II,II) → (III,III) redox transition. Bicarbonate further enhances this activity, possibly by serving as a proton transfer catalyst.

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Table 3. Oxidation of bicarbonate is thermodynamically favored over water oxidation Reaction

E o (V), pH 7

ΔG0, kcal/mol

a

2 H2O ↔ O2 + 4 e– + 4 H+

–0.81

74.6

b

2 HCO3– ↔ O2 + 4 e– + 2 CO2 + 2 H+

–0.54

49.6

C. Thermodynamics of Oxygen Production from Bicarbonate versus Water

D. Mineral Building Blocks/Remnants of Oxygenic Photosynthesis?

This brings us to the key issue relevant to the thermodynamics of water oxidation. By use of a thermodynamic cycle one can calculate the experimentally unmeasured free energy change for the oxidation of bicarbonate ion to form O2 (Dismukes et al., 2001). Table 3 lists some possible overall reactions leading to O2 production. Formation of one mole O2 from bicarbonate costs (b) 49.6 vs. (a) 74.6 kcal/mol from water. In other words, it is 25 kcal/mol easier (34% lower free energy) to produce one mole O2 from bicarbonate than water at pH 7. Thus, thermodynamic considerations reveal that bicarbonate is a better electron donor than water for O2 evolution. An additional energy advantage is realized if bicarbonate were to serve as a base to neutralize the protons released by bicarbonate or water oxidation. This very substantial energetic advantage together with the predicted abundance of bicarbonate in the archean seas raises the possibility that bicarbonate could have been the transitional electron donor prior to water that enabled the evolution of simpler anoxygenic photosynthetic metabolism to oxygenic phototrophism. This possibility remains untested. Alternatively, bicarbonate may have merely served as a cofactor within the early WOC that stimulates the enzyme to oxidize water more efficiently. A key aspect of this chemistry is that the enzyme needs to provide only sufficient free energy to convert substrate to product and not to form the substrate by hydration of CO2. The latter free energy is extracted from the system (not the enzyme) upon dissolution of atmospheric CO2. Because reaction b serves as a pump to drive CO2 back into the atmosphere, bicarbonate oxidation by photosynthesis in the early Earth would have been a powerful throttle for movement of CO2 out of the ocean and into longer term terrestrial deposits via acid rain.

Russell and Hall have postulated that colloidal clusters of a precursor to the mineral ranciete, [CaMn4O9.3H2O], might have been produced by abiotic photochemistry and subsequently taken up by an anoxygenic phototroph for incorporation into a type II reaction center protein. (Russell et al., 2002, 2003) Following subsequent mutations of the protein to form a binding site this sequence of event was proposed as a possible route to a precursor of the WOC. There are two novel aspects to this proposal related to the structure of the minerals and their hypothesized photochemical origin. Powder XRD data indicate that rancieite [(CaO)Mn4O8.3H2O] and birnessite MnO2.nH2O are both mainly comprised of Mn(IV)O2 units forming two-dimensional layered sheets separated by water molecules. (Sauer et al., 2002) The layered structure provides open access to water and mobile cations. In rancieite the interlayer sites contain Ca2+ ions with charge neutralization by an additional O2–, while birnessite contains a variety of minor cations that adsorb together with hydroxide or oxide counterions [(Na,Ca,K)(Mg,Mn)Mn6O14·5H2O] (Russell et al., 2003) These MnO2 lattices are generally imperfect such that loss of (MnIVO)2+ sites can occur by exchange with cations (Ca2+ in the case of rancieite). Because the local structure of these defects is not fully revealed, there is incomplete structural information known about the most interesting local sites in these minerals. In the bulk structure, each MnIV ion is octahedrally coordinated to O2– or H2O ligands. All oxides are sp3 hybridized and occupy apical bridging sites between Mn3 units. Sauer and Yachandra note that both structures contain the characteristic 2.7–2.8 Å Mn-Mn scattering vector of the WOC, but lack the 3.3–3.4 Å Mn-Mn scattering vector and thus are not accurate structural models (of the partially reduced S0, S1, S2 and S3(?) states). However, the latter shortcoming may not invalidate this proposal, as the rancieite core structure was postulated as a model for the

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Scheme 1. Possible evolution of the inorganic core of the WOC-PS II from an anoxygenic phototroph to cyanobacterium via two intermediate forms not known to exist or not yet identified in contemporary relics.

reactive O2 producing WOC, e.g., the S4 state. There are no structural data for the S4 state. Moreover, this state is believed to be structurally different from the partially reduced S states on the basis of the substantial activation energy for the reaction S3 → S4 → S0 + O2. Russell and Hall hypothesize that placement of a Ca2+ at an (MnO)2+ vacancy in rancieite could prevent the insertion of Mn2+ or other cations and provide a geometry suitable for water binding and activation that enables O2 production. The ranciete hypothesis is intuitively appealing and should be examined further. Sauer and Yachandra have extended the structural comparison to include other classes of MnO2 minerals. (Sauer et al., 2002) It may be significant that the sp3 hybridized 2– O bridges present in rancieite (the only type of bulk O2– ions) are structurally analogous to the O2– bridges found in the corners of the ‘cubane’ cores [Mn4O4]6+ and [Mn4O4]7+ present in the molecular complexes [Mn4O4(O2PPh2)6]0/+, respectively. The Mn4O4-cubane topology of these complexes has been shown to be key to their unique ability to release O2 following removal of a capping chelate (Ph2PO2–, diphenylphosphinate) from its bridging position on one of the faces of the cube. (Ruettinger et al., 2000; Yagi et al., 2001) The resulting reduced [Mn4O2]6+ core has a bent butterfly geometry with wingtip Mn2+ ions. The critical requirements for O2 release in the cubanes are the presence

of unusually long (e.g., weak) Mn-O bonds (~2.0 Å), the corner bridging location of the sp3 hybridized O2–, and the Mn2IIIMn2IV oxidation state. It has been hypothesized that the role of Ca2+(OHx) in such a mechanism might be to occupy a bridging position on the face of the cube for substrate activation and for preventing access to the open butterfly core in the reduced S states. (Dismukes et al., 1998) This idea is echoed in the rancieite postulate. One element of the mineral theory origin of the WOC that has not been addressed is that it is not clear what sorts of biological processes could take place that could encode the structural information necessary to carry out the synthesis and assembly of the WOC. How the transition could have taken place from organisms that simply incorporated the preformed cores to the modern situation in which the WOC is assembled stepwise from soluble cofactors is difficult to envision. E. Bicarbonate as Evolutionary Substrate and Cofactor for Mn Core Assembly Scheme 1 summarizes an hypothesis by Dismukes and coworkers for the origin and sequence of evolution of the WOC-PS II based on the proposition that Mn-bicarbonate complexes were the building blocks for constructing the inorganic core. (Dismukes et al.,

Note: the original figure is in color. Is a color version supposed to go in the Color Plate section? Also, the original is printed on regular printer paper so it has a fuzzy look and does not have the sharp appearance it would have if printed on glossy photo-paper.

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2001) It is postulated that preformed MnII-bicarbonate clusters that were widely distributed as described above, served initially as terminal substrates to anoxygenic phototrophs containing type II reaction centers, such as the green non-sulfur bacteria or purple bacteria (Mn-Bicarbonate Oxidase, stage 1). Mn-bicarbonate clusters would have been feasible, although inefficient, electron donors to these bacteria owing to the mismatch in electrochemical potentials for the primary BChl-a pigment found in the reaction center. In the next evolutionary step, two features may have been adopted in the Archean period which characterize the ‘missing link’ in evolutionary development (Bicarbonate Oxidase, stage 2): 1) mutations in the L/M type II reaction center proteins occurred which favored binding of a tetramanganese-bicarbonate cluster, Mn4Ox(HCO3)y, and 2) evolution of a higher potential photooxidant, such as BChl g, the suggested evolutionary precursor pigment to Chl a. (Xiong et al., 2000) These developments could have been sufficient to enable bicarbonate to serve as an inefficient substrate for the concerted four-electron oxidation to O2. The most recent proposed stage of development represents the emergence of cyano- and oxyphotobacteria and thus is denoted the Water Oxidase Stage. This stage was brought on by the enormous reduction of atmospheric CO2 in the post archean period. Although it is unclear how this transition occurred, it would have required the evolution of a stronger inorganic catalyst and a stronger photooxidant in order to split water efficiently. It was postulated that this developmental stage may correspond to the incorporation of Ca2+ as integral cofactor within the Mn cluster.[Dismukes, 2001 #1183 what is this?????] The Ca2+ cofactor boosts the electrochemical potential of the Mn cluster in the contemporary WOC by 0.6 to 1 eV, thus permitting weaker reductants such as water to serve as terminal substrates. Importantly, the adoption of a stronger photooxidant such as Chl a or Chl d would have greatly increased the quantum efficiency of water oxidation, owing to its considerably higher potential. (Blankenship et al., 1998) This final stage of development is postulated to include the incorporation of two catalytically essential classes of amino acid residues in the reaction center protein environment. Tyrosine-Z , Yz, of the D1 subunit (homolog of L/M) is conserved in all oxygenic phototrophs (Diner et al., 2002) and may have been introduced as this stage. Placement of YZ in between the photooxidant and the Mn cluster could serve two

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developmental functions. First, it suppresses the rate of charge recombination reactions in the proto-enzyme between QA–[Mn4]+ by increasing the distance by another 8-12 Å. Second, it reduces the yield of excited state quenching of the primary photoexcited pigment that is essential for forming a high yield of the primary photooxidant. (Abrahamsson et al., 2002) Direct evidence for tyrosine oxidation by BChl-a has been demonstrated in a ‘Yz mutant’ of Rhodobacter sphaeroides. (Kalman et al., 1999) Also, the introduction of basic amino acid residues within the D1 subunit to serve as proton acceptor/transfer cofactors in water splitting and assembly of the inorganic core is an essential developmental step in evolution. This step could have been triggered by the disappearance of the copious bicarbonate buffer from the oceans following the archean period. V. Concluding Remarks This entire section is missing! Acknowledgments We thank Michael Russell for stimulating discussions, Ken Sauer and Vittal Yachandra for a preprint and stimulating discussions. References Abrahamsson MLA, Baudin HB, Tran A, Philouze C, Berg KE, Raymond-Johansson MK, Sun LC, Akermark B, Styring S and Hammarstrom L (2002) Ruthenium-manganese complexes for artificial photosynthesis: Factors controlling intramolecular electron transfer and excited-state quenching reactions. Inorg Chem 41: 1534–1544 Ananyev GM, Murphy A, Abe Y and Dismukes GC (1999) Remarkable affinity and selectivity for Cs+ and uranyl (UO22+) binding to the manganese site of the apo-water oxidation complex of Photosystem II. Biochemistry 38: 7200–7209 Ananyev GM, Zaltsman L, Vasko C and Dismukes GC (2001) The inorganic biochemistry of photosynthetic oxygen evolution/water oxidation. Biochim Biophys Acta 1503: 52–68 Baranov S, Tyryshkin A, Katz D, Ananyev G, Klimov V and Dismukes G (2004) Bicarbonate is a native cofactor for assembly of the manganese cluster of the photosynthetic water oxidizing complex: II. Kinetics of reconstitution of O2 evolution by photoactivation. Biochemistry 43: 2070–2079 Baranov SV, Ananyev GM, Klimov VV and Dismukes GC (2000) Bicarbonate accelerates assembly of the inorganic core of the water-oxidizing complex in manganese-depleted Photo-

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Olson JM (2001) ‘Evolution of photosynthesis’ (1970) re-examined thirty years later. Photosynth Res 68: 95–112 Raven JA, Evans MCW and Korb RE (1999) The role of trace metals in photosynthetic electron transport in O2-evolving organisms. Photosynth Res 60: 111–149 Robblee JH, Cinco RM and Yachandra VK (2001) X-ray spectroscopy-based structure of the Mn cluster and mechanism of photosynthetic oxygen evolution. Biochim Biophys Acta 1503: 7–23 Ruettinger W, Yagi M, Wolf K, Bernasek S and Dismukes GC (2000) O2 evolution from the manganese-oxo cubane core [Mn4O4]6+: A molecular mimic of the photosynthetic water oxidation enzyme? J Am Chem Soc 122: 10353–10357 Russell MJ and Hall AJ (2002) From geochemistry to biochemistry: Chemiosmotic coupling and transition element clusters in the onset of life and photosynthesis. Geochem News 113: 6–12 Russell MJ, Hall AJ and Mellersh AR (2003) On the dissipation of thermal and chemical energies on the early Earth: The onsets of hydrothermal convection, chemiosmosis, genetically regulated metabolism and oxygenic photosynthesis. In: Ikan R (ed) Natural and Laboratory-Simulated Thermal Geochemical Processes. Kluwer Academic Publishers, Dordrecht Sauer K and Yachandra VK (2002) A possible evolutionary origin for the Mn4 cluster of the photosynthetic water oxidation complex from natural MnO2 precipitates in the early ocean. Proc Nat Acad Sci USA 99: 8631–8636 Semin BK, Ghirardi ML and Seibert M (2002) Blocking of electron donation my Mn(II) to Yz following incubation of Mn-depleted PS II membranes with Fe(II) in the light. Biochemistry 41: 5854–5864 Smith RM and Martell AE (1976) Critical Stability Constants. Plenum, New York Stadtman ER, Berlett PB and Chock PB (1990) Manganese-dependent disproportionation of hydrogen peroxide in bicarbonate buffer. Proc Nat Acad Sci USA 87: 384–388

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