Architecture of the Photosynthetic Oxygen-Evolving Center

Photosynthesis uses light energy to drive the oxidation of water at an oxygen-evolving catalytic site within photosystem II (PSII). We report the structure of PSII of the cyanobacterium Thermosynechococcus elongatus at 3.5 angstrom resolution. We have assigned most of the amino acid residues of this 650-kilodalton dimeric multisubunit complex and refined the structure to reveal its molecular architecture. Consequently, we are able to describe details of the binding sites for cofactors and propose a structure of the oxygen-evolving center (OEC). The data strongly suggest that the OEC contains a cubane-like Mn3CaO4 cluster linked to a fourth Mn by a mono-μ-oxo bridge. The details of the surrounding coordination sphere of the metal cluster and the implications for a possible oxygen-evolving mechanism are discussed.

[1]  R. D. Britt,et al.  EPR/ENDOR characterization of the physical and electronic structure of the OEC Mn cluster. , 2001, Biochimica et biophysica acta.

[2]  G. Feher,et al.  Structure of the reaction center from Rhodobacter sphaeroides R-26: protein-cofactor (quinones and Fe2+) interactions. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Fabrice Rappaport,et al.  Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. , 2002, Annual review of plant biology.

[4]  P. Fromme,et al.  A common ancestor for oxygenic and anoxygenic photosynthetic systems: a comparison based on the structural model of photosystem I. , 1998, Journal of molecular biology.

[5]  J. Deisenhofer,et al.  Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3Å resolution , 1985, Nature.

[6]  J. D. Paula,et al.  Magnetic properties of manganese in the photosynthetic O2-evolving complex. 2. Evidence for a manganese tetramer , 1986 .

[7]  G. Babcock,et al.  A metalloradical mechanism for the generation of oxygen from water in photosynthesis. , 1997, Science.

[8]  B. Diner 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. , 2001, Biochimica et biophysica acta.

[9]  Fabrice Rappaport,et al.  Kinetics and pathways of charge recombination in photosystem II. , 2002, Biochemistry.

[10]  G. Habermehl,et al.  ReviewPure appl. Chem: Rinehart, K. L., et al. Marine natural products as sources of antiviral, antimicrobial, and antineoplastic Agents. 53, 795 (1981). (K. L. Rinehart, University of Illinois, Urbana, IL 61801, U.S.A.) , 1983 .

[11]  G. Dismukes,et al.  An evaluation of structural models for the photosynthetic water-oxidizing complex derived from spectroscopic and X-ray diffraction signatures , 2001, JBIC Journal of Biological Inorganic Chemistry.

[12]  Petra Fromme,et al.  Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution , 2001, Nature.

[13]  D. Klug,et al.  A quantitative structure–function relationship for the Photosystem II reaction center: Supermolecular behavior in natural photosynthesis , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[14]  A. Rutherford,et al.  Carotenoid oxidation in photosystem II. , 1999, Biochemistry.

[15]  J. Rivas,et al.  β-Carotene within the isolated Photosystem II reaction centre: photooxidation and irreversible bleaching of this chromophore by oxidised P680 , 1991 .

[16]  G. Brudvig,et al.  Cytochrome b559 of photosystem II. , 1998, Biochimica et biophysica acta.

[17]  B. Diner,et al.  Site-directed mutations at D1-His198 and D2-His197 of photosystem II in Synechocystis PCC 6803: sites of primary charge separation and cation and triplet stabilization. , 2001, Biochemistry.

[18]  G. Smestad The photosystems: Structure, function and molecular biology , 1994 .

[19]  J. Barber,et al.  P680, the primary electron donor of photosystem II , 2001 .

[20]  C. Putnam-Evans,et al.  Site-directed mutagenesis of basic arginine residues 305 and 342 in the CP 43 protein of photosystem II affects oxygen-evolving activity in Synechocystis 6803. , 1999, Biochemistry.

[21]  R. Debus Amino acid residues that modulate the properties of tyrosine YZ and the manganese cluster in the water oxidizing complex of photosystem II , 2001 .

[22]  Petra Fromme,et al.  Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution , 2001, Nature.

[23]  V. Yachandra,et al.  X-ray spectroscopy-based structure of the Mn cluster and mechanism of photosynthetic oxygen evolution. , 2001, Biochimica et biophysica acta.

[24]  A. Rutherford,et al.  Beta-carotene redox reactions in photosystem II: electron transfer pathway. , 2001, Biochemistry.

[25]  P. Siegbahn,et al.  Manganese Oxyl Radical Intermediates and O−O Bond Formation in Photosynthetic Oxygen Evolution and a Proposed Role for the Calcium Cofactor in Photosystem II , 1999 .

[26]  James Barber,et al.  Photosystem II: the engine of life , 2003, Quarterly Reviews of Biophysics.

[27]  J. Barber,et al.  beta-Carotene quenches singlet oxygen formed by isolated photosystem II reaction centers. , 1994, Biochemistry.

[28]  R. van Grondelle,et al.  Primary charge separation in Photosystem II , 2004, Photosynthesis Research.

[29]  B. Forbush,et al.  COOPERATION OF CHARGES IN PHOTOSYNTHETIC O2 EVOLUTION–I. A LINEAR FOUR STEP MECHANISM , 1970, Photochemistry and photobiology.

[30]  B. Diner,et al.  Site-directed mutagenesis of photosynthetic reaction centers , 1991 .

[31]  G. Brudvig,et al.  Mechanism of photosynthetic water oxidation: combining biophysical studies of photosystem II with inorganic model chemistry. , 2001, Biochimica et biophysica acta.

[32]  H. Frank,et al.  Carotenoid photooxidation in photosystem II. , 2001, Archives of biochemistry and biophysics.

[33]  G. Brudvig,et al.  Characterization of carotenoid and chlorophyll photooxidation in photosystem II. , 2001, Biochemistry.

[34]  V. Pecoraro,et al.  A proposal for water oxidation in photosystem II , 1998 .

[35]  G. Christou,et al.  A molecular ‘double-pivot’ mechanism for water oxidation , 1987 .

[36]  Haumann,et al.  Photosynthetic water oxidation: a simplex-scheme of its partial reactions , 1999, Biochimica et biophysica acta.

[37]  J. Christian,et al.  Site-directed mutagenesis of glutamate residues in the large extrinsic loop of the photosystem II protein CP 43 affects oxygen-evolving activity and PS II assembly. , 1999, Biochemistry.

[38]  A. Rutherford,et al.  Rapid formation of the stable tyrosyl radical in photosystem II , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Nobuo Kamiya,et al.  Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[40]  P. Fromme,et al.  Functional implications on the mechanism of the function of photosystem II including water oxidation based on the structure of photosystem II. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[41]  J. Barber,et al.  Three-dimensional structure of the photosystem II core dimer of higher plants determined by electron microscopy. , 2001, Journal of structural biology.

[42]  G. Ananyev,et al.  Bicarbonate accelerates assembly of the inorganic core of the water-oxidizing complex in manganese-depleted photosystem II: a proposed biogeochemical role for atmospheric carbon dioxide in oxygenic photosynthesis. , 2000, Biochemistry.

[43]  I. V. van Stokkum,et al.  Pathways for energy transfer in the core light-harvesting complexes CP43 and CP47 of photosystem II. , 2002, Biophysical journal.

[44]  R. Debus,et al.  Amino acid residues that influence the binding of manganese or calcium to photosystem II. 2. The carboxy-terminal domain of the D1 polypeptide. , 1995, Biochemistry.

[45]  P. Siegbahn Quantum chemical studies of manganese centers in biology. , 2002, Current opinion in chemical biology.

[46]  C. Berthomieu,et al.  Bicarbonate binding to the non-heme iron of photosystem II investigated by Fourier transform infrared difference spectroscopy and 13C-labeled bicarbonate. , 1995, Biochemistry.

[47]  C. Tommos,et al.  Proton and hydrogen currents in photosynthetic water oxidation. , 2000, Biochimica et biophysica acta.

[48]  D. Klug,et al.  A multimer model for P680, the primary electron donor of photosystem II. , 1995, Proceedings of the National Academy of Sciences of the United States of America.