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‘Photosystem II: the water splitting enzyme of photosynthesis and the origin of oxygen in our atmosphere’

Published online by Cambridge University Press:  01 August 2016

James Barber
James Barber*
Affiliation:
Department of Life Sciences, Imperial College London, Sir Ernst Chain Building, South Kensington Campus, London SW7 2AZ, UK
*
*Author for correspondence: James Barber, Department of Life Sciences, Imperial College London, Sir Ernst Chain Building, South Kensington Campus, London SW7 2AZ, UK. Tel. : +44 208 747 1165; Fax: +44 207 594 5267; Email: j.barber@imperial.ac.uk
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Abstract

About 3 billion years ago an enzyme emerged which would dramatically change the chemical composition of our planet and set in motion an unprecedented explosion in biological activity. This enzyme used solar energy to power the thermodynamically and chemically demanding reaction of water splitting. In so doing it provided biology with an unlimited supply of reducing equivalents needed to convert carbon dioxide into the organic molecules of life while at the same time produced oxygen to transform our planetary atmosphere from an anaerobic to an aerobic state. The enzyme which facilitates this reaction and therefore underpins virtually all life on our planet is known as Photosystem II (PSII). It is a pigment-binding, multisubunit protein complex embedded in the lipid environment of the thylakoid membranes of plants, algae and cyanobacteria. Today we have detailed understanding of the structure and functioning of this key and unique enzyme. The journey to this level of knowledge can be traced back to the discovery of oxygen itself in the 18th-century. Since then there has been a sequence of mile stone discoveries which makes a fascinating story, stretching over 200 years. But it is the last few years that have provided the level of detail necessary to reveal the chemistry of water oxidation and O–O bond formation. In particular, the crystal structure of the isolated PSII enzyme has been reported with ever increasing improvement in resolution. Thus the organisational and structural details of its many subunits and cofactors are now well understood. The water splitting site was revealed as a cluster of four Mn ions and a Ca ion surrounded by amino-acid side chains, of which seven provide direct ligands to the metals. The metal cluster is organised as a cubane structure composed of three Mn ions and a Ca2+ linked by oxo-bonds with the fourth Mn ion attached to the cubane. This structure has now been synthesised in a non-protein environment suggesting that it is a totally inorganic precursor for the evolution of the photosynthetic oxygen-evolving complex. In summary, the overall structure of the catalytic site has given a framework on which to build a mechanistic scheme for photosynthetic dioxygen generation and at the same time provide a blue-print and incentive to develop catalysts for artificial photo-electrochemical systems to split water and generate renewable solar fuels.

Type
Review
Information
Quarterly Reviews of Biophysics , Volume 49 , 2016 , e14
Copyright
Copyright © Cambridge University Press 2016 

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References

Arakawa, H., Aresta, M., Armor, J. N., Barteau, M., Beckman, E. J., Bell, A. T. A., & Domen, K. (2001). Catalysis research of relevance to carbon management: progress, challenges, and opportunities. Chemical Reviews 101, 953–996.CrossRefGoogle ScholarPubMed
Arnon, D. I. & Whatley, F. R. (1949). Is chloride a coenzyme of photosynthesis? Science 110, 554–556.CrossRefGoogle ScholarPubMed
Barber, J. (1987). Photosynthetic reaction centres: a common link. Trends in Biochemical Sciences 12, 321–326.CrossRefGoogle Scholar
Barber, J. (2003). Photosystem II: the engine of life. Biophysics Quarterly Reviews 36, 71–89.Google Scholar
Barber, J. (2009). Photosynthetic energy conversion: natural and artificial. Chemical Society Reviews 38, 185–196.Google Scholar
Barber, J. & Andersson, B. (1992). Too much of a good thing: light can be bad for photosynthesis. Trends in Biochemical Sciences 17, 61–66.Google Scholar
Barber, J. & Archer, M. D. (2001). P680, the primary electron donor of PSII. Journal of Photochemistry and Photobiology A142, 97–106.CrossRefGoogle Scholar
Barber, J., Ferreira, K., Maghlaoui, K. & Iwata, S. (2004). Structure of the oxygen evolving center of photosystem II and its mechanistic implications. Physical Chemistry Chemical Physics 6, 4737–4742.CrossRefGoogle Scholar
Bassi, P. S., Gurudayal, , Wong, L. H. & Barber, J. (2014). Iron based photoanodes for solar fuel production. Physical Chemistry Chemical Physics 16, 11834–11842.Google Scholar
Batista, V. S., Sprovier, E. M., Gascon, J. A., McEvoy, J. P. & Brudvig, G. W. (2008). Computational studies of the O2-evolving complex of photosystem II and biomimetic oxo manganese complexes. Coordination Chemistry Reviews 252, 395–415.Google Scholar
Boardman, K. & Anderson, J. (1964). Isolation from spinach chloroplasts of particles containing different proportions of chlorophyll a and chlorophyll b and their possible role in the light reactions of photosynthesis. Nature 203, 166–167.CrossRefGoogle Scholar
Bossingault, J. B. (1854). De la vegetation dans l'obscurite. Annals of Science Nature (Paris) 1, 314–324.Google Scholar
Bove, J. M., Bove, C., Whatley, F. R. & Arnon, D. I. (1963). Chloride requirement for oxygen evolution in photosynthesis. Zeitschrift fur Naturforschung 18b, 683–688.CrossRefGoogle Scholar
Brudvig, G. W. (2008). Water oxidation chemistry of photosystem II. Philosophical Transaction of the Royal Society of London B 363, 1211–1218.Google Scholar
Cox, N., Rapatskiy, L., Su, J. H., Pantazis, D. A., Sugiura, M., Kulik, L., & Messinger, J. (2011). Effect of Ca2+/Sr2+ substitution on the electronic structure of the oxygen-evolving complex of photosystem II: a combined multifrequency EPR, 55Mn-ENDOR, and DFT study of the S2 state. Journal of the American Chemical Society 133, 3635–3648.Google Scholar
Cox, N., Retegan, M., Neese, F., Pantais, D. A., Boussac, A. & Lubitz, W. (2014). Electronic structure of the oxygen-evolving complex in photosystem II prior to OO bond formation. Science 345, 804–808.Google Scholar
Dau, H., Grundmeier, A., Loja, P. & Haumann, M. (2008). On the structure of the manganese complex of photosystem II: extended-range EXAFS data and specific atomic-resolution models for four S-states. Philosophical Transaction of the Royal Society of London B 363, 1237–1243.CrossRefGoogle ScholarPubMed
Debus, R. J. (1992). The manganese and calcium-ions of photosynthetic oxygen evolution Biochimica et Biophysica Acta 1102, 269–352.Google Scholar
Debus, R. J. (2001). Amino acid residues that modulate the properties of tyrosine Y–Z and the manganese cluster in the water oxidizing complex of photosystem II. Biochimica et Biophysica Acta 1503, 164–186.Google Scholar
Debus, R. J. (2008). Protein ligation of the photosynthetic oxygen-evolving center. Coordination Chemistry Reviews 252, 244–258.CrossRefGoogle ScholarPubMed
De Las Rivas, J., Balsera, M. & Barber, J. (2004). Evolution of oxygenic photosynthesis: genome-wide analysis of the OEC extrinsic proteins. Trends in Plant Science 9, 18–25.Google Scholar
De Saussure, N.-T. (1804). Reserches chimique sur la vegetation. Annales de chimie (“Annals of Chemistry”), Nyon, Paris.Google Scholar
Diesenhofer, J., Epp, O., Miki, O., Huber, R. & Michel, H. (1985). Structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas viridis at 3A resolution. Nature 318, 618–624.Google Scholar
Diner, B. A. (2001). Amino acid residues involved in the coordination and assembly of the manganese cluster of photosystem II. Proton-coupled electron transport of the redox-active tyrosines and its relationship to water oxidation. Biochimica et Biophysica Acta 1503, 147–163.Google Scholar
Diner, B. A., Nixon, P. J. & Farchaus, J. W. (1991). Site-directed mutagenesis of photosynthetic reaction centers. Current Opinion in Structural Biology 1, 546–554.Google Scholar
Dismukes, G. C. & Siderer, Y. (1980). EPR spectroscopic observations of manganese center associated with water oxidation in spinach chloroplasts. FEBS Letters 121, 78–80.Google Scholar
Doring, G., Stiehl, H. H. & Witt, H. T. (1967). A second chlorophyll reaction in the electron chain of photosynthesis-registration by the repetitive excitation technique. Zeitschrift. Naturforschung 22b, 639–644.Google Scholar
Du, P. & Eisenberg, R. (2012). Catalysts made of earth-abundant elements (Co, Ni, Fe) for water splitting: recent progress and future challenges. Energy & Environmental Science 5, 6012–6021.Google Scholar
Duan, L., Bogoglian, F., Mandal, S., Stewart, B., Privalot, T., Llobet, A. & Sun, L-C. (2012). A molecular ruthenium catalyst with water-oxidation activity comparable to that of photosystem II. Nature Chemistry 4, 418–423.Google Scholar
Durrant, J. R., Kwa, S. L. S., Van Grondelle, R. V., Porter, G. & Klug, D. R. (1995). A multimer model for P680, the primary electron donor of photosystem II. Proceedings of the National Academy of Sciences of the United States of America 92, 4798–4802.Google Scholar
Duysens, L. N. M., Amesz, J. & Kamp, B. M. (1961). Two photochemical systems in photosynthesis. Nature 190, 510–511.Google Scholar
Eisenberg, E. & Gray, H. B. (2008). Preface to making oxygen. Inorganic Chemistry 47, 1697–1699.Google Scholar
Emerson, R. & Arnold, W. (1932). A separation of the reactions in photosynthesis by means of intermittent light. The Journal of General Physiology 16, 191–205.Google Scholar
Emerson, R. & Lewis, C. M. (1943). The dependence of the quantum yield of Chlorella photosynthesis on wavelength of light. American Journal of Botany 30, 165–178.Google Scholar
Faller, P., Debus, R. J., Brettel, K., Sugiura, M., Rutherford, A. W. & Boussac, A. (2001). Rapid formation of the stable tyrosyl radical in photosystem II. Proceedings of the National Academy of Sciences of the United States of America 98, 14368–14373.Google Scholar
Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J. & Iwata, S. (2004). Architecture of the Photosynthetic oxygen-evolving Center. Science 303, 1831–1838.CrossRefGoogle ScholarPubMed
Fujita, E. (2000). Carbon dioxide reduction. In McGraw-Hill Yearbook of Science & Technology (ed. Licker, M. D.), pp. 71–74. New York, NY: McGraw-Hill Book Co.Google Scholar
Gao, Y., Crabtree, R. H. & Brudvig, G. W. (2012). Water oxidation catalyzed by the Tetranuclear Mn complex: [MnIV 4O5(terpy)4(H2O)2](ClO4)6 . Inorganic Chemistry 51, 4043–4050.Google Scholar
Gersten, S. W., Samuels, G. J. & Meyer, T. J. (1982). Catalytic oxidation of water by an oxo-bridged ruthenium dimer. Journal of the American Chemical Society 104, 4029–4030.CrossRefGoogle Scholar
Govindjee, & Van Rensen, J. J. S. (1993). Photosystem II reaction center and bicarbonate. In The Photosynthetic Reaction Center (ed. Deisenhofer, J. B. & Norris, J.), pp. 357–389. San Diego: Academic Press.CrossRefGoogle Scholar
Grabolle, M., Haumann, M., Muller, C., Liebisch, P. & Dau, H. (2006). Rapid loss of structural motifs in the manganese complex of oxygenic photosynthesis by X-ray irradiation at 10–300 K. Journal of Biological Chemistry 281, 4580–4588.Google Scholar
Gurudayal, , Sabba, D., Kuma, M. H., Wong, L. H., Barber, J., Graetzel, M. & Mathews, N. (2015). Perovskite−Hematite Tandem cells for efficient overall solar DrivenWater splitting. Nano Letters 15, 3833–3839.Google Scholar
Guskov, A., Kern, J., Gabdulkhakov, A., Broser, M., Zouni, A. & Saenger, W. (2009). Cyanobacterial photosystem II at 2.9 Å resolution: role of quinones, lipids, channels and chloride. Nature Structure & Molecular Biology 16, 334–342.CrossRefGoogle ScholarPubMed
Hankamer, B., Barber, J. & Boekema, E. J. (1997). Structure and membrane organisation of PSII in green plants. Annual Review of Plant Physiology and Plant Molecular Biology 48, 641–671.Google Scholar
Hankamer, B., Morris, E. P. & Barber, J. (1999). Cryoelectron microscopy of photosystem two shows that CP43 and CP47 are located on opposite sides of the D1/D2 reaction centre proteins. Nature Structural Biology 6, 560–564.Google Scholar
Hankamer, B., Morris, E. P., Nield, J., Carne, A. & Barber, J. (2001a). Subunit positioning and transmembrane helix organisation in the core dimer of photosystem II. FEBS Letters 504, 142–151.Google Scholar
Hankamer, B., Morris, E. P., Nield, J., Gerle, C. & Barber, J. (2001b). Three-dimensional structure of photosystem II core dimer of higher plants determined by electron microscopy. Journal of Structural Biology 135, 262–269.Google Scholar
Hasegawa, K., Ono, T. A., Inoue, Y. & Kusunoki, M. (1999). Spin-exchange interactions in the S2-state manganese tetramer in photosynthetic oxygen-evolving complex deduced from g = 2 multiline EPR signal. Chemical Physics Letters 300, 9–19.Google Scholar
Hienerwadal, R. & Berthomieu, C. (1995). Bicarbonate binding to the non-heme iron of photosystem II investigated by Fourier transform infrared difference spectroscopy and 13C-labeled bicarbonate. Biochemistry 34, 16288–16297.Google Scholar
Hill, R. (1937). Oxygen evolution by isolated chloroplasts. Nature 139, 881–882.Google Scholar
Hill, R. & Bendall, F. (1960). Function of the two cytochromes in chloroplasts: a working hypothesis. Nature 186, 136–137.Google Scholar
Hoganson, C. W. & Babcock, G. T. (1997). A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science 277, 1953–1956.Google Scholar
Holzwarth, A. R., Muller, M. G., Rees, M., Nowaczyk, M., Sander, J. & Rogner, M. (2006). Kinetics and mechanism of electron transfer in intact photosystem II and in isolated reaction centers: Pheophytin is the primary acceptor. Proceedings of the National Academy of Sciences of the United States of America 103, 6895–6900.Google Scholar
Hwang, H. J., Dilbeck, P., Debus, R. J. & Burnap, R. L. (2007). Mutation of arginine 357 of the CP43 protein of photosystem II severely impairs the catalytic S-state cycle of the H2O oxidation complex. Biochemistry 46, 11987–11997.Google Scholar
Izawa, S., Heath, R. L. & Hind, G. (1969). Role of chloride ion in photosynthesis. 3. Effects of artificial electron donors upon electron transport. Biochimica et Biophysica Acta 180, 388–389.Google Scholar
Jiao, F. & Frei, H. (2010). Nanostructure manganese oxide clusters supported on mesoporous silica as efficient oxygen-evolving catalysts. Chem. Commun. 46, 2920–292.Google Scholar
Joliot, P., Barbieri, G. & Chabaud, R. (1969). Un nouveau modele des centres photochimiques du systeme II. Photochemistry and Photobiology 10, 309–329.Google Scholar
Jordan, P., Fromme, P., Witt, H. T., Klukas, O., Saenger, W. & Krauß, N. (2001). Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411, 909–917.Google Scholar
Kamiya, N. & Shen, J. R. (2003). Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. Proceedings of the National Academy of Sciences of the United States of America 100, 98–103.Google Scholar
Kanady, S., Tsui, E., Day, M. & Agapie, T. (2011). A synthetic model of the Mn3Ca subsite of the oxygen-evolving complex in photosystem II. Science 333, 733–736.Google Scholar
Kanan, M. W. & Nocera, D. G. (2008). In situ formation of an oxygen-evolving catalyst in neutral water containing phosphate and Co2+ . Science 321, 1072–1075.Google Scholar
Kargul, J., Maghlaoui, K., Murray, J. W., Deak, Z., Boussac, A., Rutherford, A. W., Vass, I. & Barber, J. (2007). Purification, crystallization and X-ray diffraction analyses of the T. elongatus PSII core dimer with strontium replacing calcium in the oxygen-evolving complex. Biochimica et Biophysica Acta 1767, 404–413.Google Scholar
Kashino, Y., Takahashi, T., Inoue-Kashino, N., Ban, A., Yohei- Ikeda, Y., Satoh, K. & Sugiura, M. (2007). Ycf12 is a core subunit in the Photosystem II complex. Biochimica et Biophysica Acta 1767, 1269–1275.Google Scholar
Kawakami, K., Umena, Y., Kamiya, N. & Shen, J.-R. (2009). Location of chloride and its possible functions in oxygen-evolving photosystem II revealed by X-ray crystallography. Proceedings of the National Academy of Sciences of the United States of America 106, 8567–8572.Google Scholar
Khare, V., Zaharieva, I., Gerencser, L., Chernev, P. & Dau, H. (2009). Cobalt-oxo core of a water-oxidizing catalyst film. Cobalt−Oxo Core of a Water-Oxidizing Catalyst Film. Journal of the American Chemical Society 131, 6936–6937.Google Scholar
Kok, B., Forbush, B. & McGLOIN, M. (1970). Cooperation of charges in photosynthetic O2 evolution. 1. A linear four step mechanism. Photochemistry and Photobiology 11, 457–475.Google Scholar
Li, X. & Siegbahn, P. E. (2015). Alternative mechanisms for O2 release and O-O bond formation in the oxygen evolving complex of photosystem II. Physical Chemistry Chemical Physics 17, 12168–12174.Google Scholar
Limberg, J., Vrettos, J. S., Liable-Sands, L. M., Rheingold, A. L., Crabtree, R. H. & Brudvig, G. W. (1999). A functional model for O–O bond formation by the O2-evolving complex in photosystem II. Science 283, 1524–1527.Google Scholar
Liu, F., Concepcion, J. J., Jurss, J. W., Cardolaccia, T., Templeton, J. L. & Meyer, T. J. (2008). Mechanisms of water oxidation from the blue dimer to photosystem II. Inorganic Chemistry 47, 1727–1752.Google Scholar
Loll, B., Kern, J., Saenger, W., Zouni, A. & Biesiadka, J. (2005). Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438, 1040–1044.Google Scholar
Luber, S., Rivalta, I., Umena, Y., Kawakami, K., Shen, J.-R., Kamiya, N., Brudvig, G. W. & Batista, V. S. (2011). S1-state model of the O2-evolving complex of photosystem II. Biochemistry 50, 6308–6311.Google Scholar
Lunberg, M. & Siegbahn, P. E. M. (2004). Theoretical investigations of the structure and mechanism of the oxygen-evolving complex in PSII. Phys. Physical Chemistry Chemical Physics 6, 4772–4780.CrossRefGoogle Scholar
McEvoy, J. P. & Brudvig, G. W. (2004). Structure-based mechanism of photosynthetic water oxidation. Physical Chemistry Chemical Physics 6, 4754–4763.Google Scholar
McEvoy, J. P. & Brudvig, G. W. (2006). Water-splitting chemistry of photosystem II. Chemical Reviews 106, 4455–4483.Google Scholar
Messinger, J., Badger, M. & Wydrzynski, T. (1995). Detection of one slowly exchanging substrate water molecule in the S3 State of Photosystem II. Proceedings of the National Academy of Sciences of the United States of America 92, 3209–3213.Google Scholar
Merki, D. & Hu, X. (2011). Recent developments of molybdenum and tungsten sulfides as hydrogen evolution catalysts. Energy & Environmental Science 4, 3878–3888.Google Scholar
Michel, H. & Deisenhofer, J. (1988). Relevance of the photosynthetic reaction center of purple bacteria to the structure of photosystem II. Biochemistry 27, 1–7.Google Scholar
Misra, A., Wernsdorfer, W., Abboud, K. A. & Christou, G. (2005). The first high oxidation state manganese-calcium cluster: relevance to the water oxidizing complex of photosynthesis. Chemical Communications 1, 54–56.Google Scholar
Mukherjee, S., Stull, J. A., Yano, J., Stamatatos, T., Pringouri, K. & Stich, T. A., Abboud, K. A., Britt, R. D., Yachandra, V. K. & Christou, G. (2012). Synthetic model of the asymmetric [Mn3CaO4] cubane core of the oxygen-evolving complex of photosystem II proc. Proceedings of the National Academy of Sciences of the United States of America 109, 2257–2262.CrossRefGoogle Scholar
Murphy, A. B., Barnes, P. R. F., Randeniyqa, L. K., Plumb, I. C., Grey, I. E., Horne, M. D. & Glasscock, J. A. (2006). Efficiency of solar water splitting using semiconductor electrodes. International Journal of Hydrogen Energy 31, 1999–2017.Google Scholar
Murray, J. W. & Barber, J. (2007). Structural characteristics of channels and pathways in Photosystem II including the identification of an oxygen channel. Journal of Structural Biology 159, 228–237.Google Scholar
Murray, J. W., Duncan, J. & Barber, J. (2006). CP43-like chlorophyll binding proteins: structural and evolutionary implications. Trends in Plant Science 11, 152–158.Google Scholar
Murray, J. W., Maghlaoui, K., Kargul, J., Ishid, N., Lai, T.-L., Rutherford, A. W., Sugiura, M., Boussac, A. & Barber, J. (2008). X-ray crystallography identifies two chloride binding sites in the oxygen evolving centre of photosystem II. Energy & Environmental Science 1, 161–166.CrossRefGoogle Scholar
Najafpour, M. M. (2011). Calcium-manganese oxides as structural and functional models for active site in oxygen evolving complex in photosystem II: lessons from simple models. Journal of Photochemistry and Photobiology B: Biology 104, 111–117.Google Scholar
Najafpour, M. M., Ehrenberg, T., Wiechen, M. & Kurz, P. (2010). Calcium manganese(III) oxides (CaMn2O4⋅x H2O) as biomimetic oxygen-evolving catalysts. Angewandte Chemie International Edition 49, 2233–2237.Google Scholar
Pecoraro, V. L., Baldwin, M. J., Caudle, M. T., Hsieh, W.-Y. & Law, N. A. (1998). A proposal for the water oxidation in Photosystem II. Pure and Applied Chemistry 70, 925–929.Google Scholar
Peloquin, J. M., Campbell, K. A., Randall, D. W., Evanchik, M. A., Pecoraro, V. L., Armstrong, W. H. & Britt, R. D. (2000). 55Mn ENDOR of the S2-state multiline EPR signal of Photosystem II: implications on the structure of the tetranuclear Mn cluster. Journal of American Chemical Society 122, 10926–10942.Google Scholar
Pirson, A., Tichy, C. & Wilhelmi, G. (1951). Metabolism and mineral salt diet unicellular green algae. Planta 40, 199–253.Google Scholar
Priestley, J. (1772). Observations on different kinds of air. Philosophical Transaction of the Royal Society of London 62, 147–264.Google Scholar
Reece, S. Y., Hamel, J. A., Sung, K., Jarvi, T. D., Esswein, A. J., Pijpers, J. J. H. & Nocera, D. G. (2011). Wireless solar water splitting using silicon-based semiconductors and earth-abundant catalysts. Science 334, 645–648.CrossRefGoogle ScholarPubMed
Rhee, K.-H., Morris, E. P., Barber, J. & Keubrandt, W. (1998). Three-dimensional structure of the photosystem II reaction centre at 8 Å resolution. Nature 396, 283–286.Google Scholar
Rhee, K.-H., Morris, E. P., Zheleva, D., Hankamer, B., Kuhbrandt, W. & Barber, J. (1997). Two-dimensional structure of plant photosystem II at 8 Å resolution. Nature 389, 522–526.Google Scholar
Risch, M., Ringle, F., Kohlhoff, M., Bogdanoff, P., Chemev, P., Zaharieva, I. & Dau, H. (2015). Water oxidation by amorphous cobalt-based oxides: in situ tracking of redox transitions and mode of catalysis. Energy & Environmental Science 8, 661–674.Google Scholar
Rivalta, I., Amin, M., Luber, S., Vassiliev, S., Pokhrel, R., Umena, Y., Kawakami, K., Shen, J.-R., Kamiya, N., Bruce, D., Brudvig, G. W., Gunner, M. R. & Batista, V. S. (2011). Structural-Functional role of chloride in photosystem II. Biochemistry 50, 6312–6315.Google Scholar
Romero, I., Rodriguez, M., Sens, C., Mola, J., Kollipara, M. R., Francas, L., Mas-Marza, E., Escriche, L. & Llobet, A. (2008). Ru complexes that can catalytically oxidize water to molecular dioxygen. Inorganic Chemistry 47, 1824–1834.Google Scholar
Ruben, S., Randle, M., Kaman, M. & Hyde, J. L. (1941). Heavy oxygen (O18) as a tracer in the study of photosynthesis. Journal of the American Chemical Society 63, 877–879.Google Scholar
Rutherford, A. W. (1989). Photosystem II: the water splitting enzyme. Trends in Biochemical Science 14, 227–232.Google Scholar
Schubert, W. D., Klukas, O., Saenger, W., Witt, H. T., Fromme, P. & Krauss, N. (1998). A common ancestor for oxygenic and anoxygenic photosynthetic systems: a comparison based on the structural model of Photosystem I. Journal of Molecular Biology 280, 297–341.Google Scholar
Senebier, J. (1788). Expériences sur l'action de la lumière solaire dans la vegetation. Genève: Pub Barde Ed Manget & Cie.Google Scholar
Service, R. J., Hillier, W. & Debus, R. J. (2010). Evidence from FTIR difference spectroscopy of an extensive network of hydrogen bonds near the oxygen-evolving Mn4Ca cluster of photosystem II involving D1-Glu65, D2-Glu312, and D1-Glu329. Biochemistry 49, 6655–6669.Google Scholar
Siegbahn, P. E. M. (2006). O-O bond formation in the S4-state of the oxygen evolving complex in Photosystem II. Chemistry – A European Journal 12, 9217–9237.Google Scholar
Siegbahn, P. E. M. (2008). A structure-consistent mechanism for dioxygen formation in photosystem II. Chemistry 14, 8290–8302.Google Scholar
Siegbahn, P. E. M. (2009). Structures and energetics for O2 formation in photosystem II. Accounts of Chemical Research 42, 1871–1880.Google Scholar
Siegbahn, P. E. M. (2012). Mechanisms for proton release during water oxidation in the S2 to S3 and S3 to S4 transitions in photosystem II. Physical Chemistry Chemical Physics 17, 12168–12174.Google Scholar
Siegbahn, P. E. (2013). Water oxidation mechanism in photosystem II, including oxidations, proton release pathways, O–O bond formation and O2 release. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1827, 1003–1019.Google Scholar
Sivula, K. L. E., Formal, F. & Graezel, M. (2011). Solar water splitting: progress using Hematite (α-Fe2O3) photoelectrodes. ChemSusChem 4, 432–449.Google Scholar
Sproviero, E. M., Gascon, J. A., McEvoy, J. P., Brudvig, G. W. & Batista, V. S. (2006). QM/MM models of the O2-evolving complex of photosystem II. Journal of Chemical Theory and Computation 2, 1119–1134.Google Scholar
Sproviero, E. M., Gascon, J. A., McEvoy, J. P., Brudvig, G. W. & Batista, V. S. (2007). Quantum mechanics/molecular mechanics structural models of the oxygen-evolving complex of photosystem II. Current Opinion in Structural Biology 17, 173–180.Google Scholar
Sproviero, E. M., Gascon, J. A., McEvoy, J. P., Brudvig, G. W. & Batista, V. S. (2008). Quantum mechanics/molecular mechanics study of the Catalytic cycle of water splitting in photosystem II J. American Chemical Society 130, 3428–3442.Google Scholar
Stewart, D. H. & Brudvig, G. W. (1998). Cytochrome b559 of Photosystem II. Biochimica et Biophysica Acta 1367, 63–87.Google Scholar
Suga, M., Akita, F., Hirata, K., Ueno, G., Murakami, H., Nakajima, Y., Shimizu, T., Yamashita, K., Yamamoto, M., Ago, H. & Shen, R.-J. (2015). Native structure of photosystem II at 1.95A° resolution viewed by femtosecond X-ray pulses. Nature 517, 99–103.Google Scholar
Tagore, R., Crabtree, R. H. & Brudvig, G. W. (2008). Oxygen evolution Catalysis by a Dimanganese complex and its relation to Photosynthetic water oxidation. Inorganic Chemistry 47, 1815–1823.Google Scholar
Telfer, A. (2005). Too much light? How β-carotene protects the photosystem II reaction centre. Photochemical & Photobiological Sciences 4, 950–956.Google Scholar
Tran, P. D., Artero, V. & Fontecave, M. (2010). Water electrolysis and photoelectrolysis on electrodes engineered using biological and bio-inspired molecular systems. Energy & Environmental Science 3, 727–747.CrossRefGoogle Scholar
Tran, P. D. & Barber, J. (2012). Proton reduction to hydrogen in biological and chemical systems. Physical Chemistry Chemical Physics 14, 13772–13784.Google Scholar
Tran, P. D., Chiam, S. Y., Boix, P. P., Ren, Y., Pramana, S. S., Fize, J., Artero, V. & Barber, J. (2013). Novel Ternary metal sulfide catalysts for Electrocatalytic Hydrogen generation in water. Energy & Environmental Sciences 6, 2452–2459.Google Scholar
Tran, P. D., Wong, L. H., Barber, J. & Loo, J. S. C. (2012). Recent advances in hybrid photocatalysts for solar fuel production. Energy & Environmental Sciences 5, 5902–5918.Google Scholar
Umena, Y., Kawakami, K., Shen, J. R. & Kamiya, N. (2011). Crystal structure of oxygen evolving photosystem II at a resolution of 1.9 angstrom. Nature 473, 55–65.Google Scholar
van Gorkom, H. J. & Yochum, C. F. (2005). The calcium and chloride cofactors. In Photosystem II. The Light-Driven Water Plastoquinone Oxido-reductase (eds. Wydrzynski, T. J. & Satoh, K.), pp. 307–327. Dordrecht: Pub. Springer.Google Scholar
van Ingen-Housz, J. (1779). Experiments upon Vegetables, Experiments upon vegetables discovering their great power of purifying the common air in the sun-shine, and of injuring it in the shade and at night: to which is joined, a new method of examining the accurate degree of salubrity of the atmosphere. Pub P. Elmsly and H. Payne London.Google Scholar
Vinyard, D. J., Khan, S. & Brudvig, G. W. (2015). Photosynthetic water oxidation: binding and activation of substrate waters for O–O bond formation. Faraday Discussions 185, 37–50.Google Scholar
Wang, M., Chen, L. & Sun, L. (2012). Recent progress in electrochemical hydrogen production with earth-abundant metal complexes as catalysts. Energy & Environmental Science 5, 6763–6778.Google Scholar
Wincencjus, H., Van Gorkom, H. J. & Yocum, C. F. (1997). The photosynthetic oxygen evolving complex requires chloride for its redox state S2→ S3 and S3→ S0 transitions but not for S0→ S1 or S1→ S2 transitions. Biochemistry 36, 3663–3670.Google Scholar
Yachandra, V. K. (2002). Structure of the Mn complex in Photosystem II: insights from X-ray spectroscopy. Philosophical Transaction of the Royal Society of London B 357, 1347–1358.Google Scholar
Yano, J., Kern, J., Irrgang, K.-D., Lattimer, M. J., Bergmann, U., Glatzel, P., Pushkar, Y., Biesiadka, J., Loll, B., Sauer, K., Messinger, J., Zouni, A. & Yachandra, V. K. (2005). X-ray damage to the Mn4Ca complex in photosystem II crystals: a case study for metallo-protein X-ray crystallography. Proceedings of the National Academy of Sciences of the United States of America 102, 12047–12052.Google Scholar
Yano, J., Kern, J., Sauer, K., Latimer, M. J., Pushkar, Y., Biesiadka, J., Loll, B., Saenger, W., Messinger, J., Zouni, A. and Yachandra, V. K. (2006). Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster. Science 314, 821–825.Google Scholar
Yin, Q., Tan, J. M., Besson, C., Geletii, Y. V., Musaev, D. G., Kuznetsov, A. E., Luo, Z., Hardcastle, K. I. & Hill, C. L. (2010). A fast soluble carbon-free molecular water oxidation catalyst based on abundant metals. Science 328, 342–345.Google Scholar
Yocum, C. F. (2008). The calcium and chloride requirements of the O2 evolving complex. Coordination Chemistry Reviews 252, 296–305.Google Scholar
Zaharieva, I., Najafpour, M. M., Wiechert, M., Haumann, M., Kurz, P. & Dau, H. (2011). Synthetic manganese-calcium oxides mimic the water-oxidizing complex of photosynthesis functionally and structurally. Energy & Environmental Science 4, 2400–2408.Google Scholar
Zhang, C., Chen, C., Dong, H., Shen, J. R., Dau, H. & Zhao, J. (2015). A synthetic Mn4Ca-cluster mimicking the oxygen-evolving center of photosynthesis. Science 348, 690–693.Google Scholar
Zong, X., Han, J., Ma, G., Yan, H., Wu, G. & Li, C. (2011). Photocatalytic H2 evolution on CdS loaded with WS2 as Cocatalyst under visible light irradiation. Journal of Physical Chemistry C 115, 12202–12208.Google Scholar
Zouni, A., Witt, H. T., Kern, J., Fromme, P., Krauss, N., Saenger, W. & Orth, P. (2001). Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409, 739–743.Google Scholar