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Originally published in Science Express on 5 February 2004
Science 19 March 2004:
Vol. 303. no. 5665, pp. 1831 - 1838
DOI: 10.1126/science.1093087
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Research Articles

Architecture of the Photosynthetic Oxygen-Evolving Center

Kristina N. Ferreira,1* Tina M. Iverson,2* Karim Maghlaoui,1 James Barber,1{dagger} So Iwata1,2,3{dagger}

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 Department of Biological Sciences, Imperial College London, London, SW7 2AZ, UK.
2 Division of Biomedical Sciences, Imperial College London, London, SW7 2AZ, UK.
3 ATP System Project, ERATO, Japan Science and Technology Corporation, 5800-3 Nagatsuta, Midori-ku, Yokohama 226-0026, Japan.



* These authors contributed equally to this work.

{dagger} To whom correspondence should be addressed. E-mail: s.iwata{at}imperial.ac.uk (S.I.); j.barber{at}imperial.ac.uk (J.B.)

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PLANT CELL 18, 955-969
   Abstract »    Full Text »    PDF »
Structural and Computational Analysis of the Quinone-binding Site of Complex II (Succinate-Ubiquinone Oxidoreductase): A MECHANISM OF ELECTRON TRANSFER AND PROTON CONDUCTION DURING UBIQUINONE REDUCTION.
R. Horsefield, V. Yankovskaya, G. Sexton, W. Whittingham, K. Shiomi, S. Omura, B. Byrne, G. Cecchini, and S. Iwata (2006)
J. Biol. Chem. 281, 7309-7316
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Rapid Loss of Structural Motifs in the Manganese Complex of Oxygenic Photosynthesis by X-ray Irradiation at 10-300 K.
M. Grabolle, M. Haumann, C. Muller, P. Liebisch, and H. Dau (2006)
J. Biol. Chem. 281, 4580-4588
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The Impact of Structural Genomics: Expectations and Outcomes.
J.-M. Chandonia and S. E. Brenner (2006)
Science 311, 347-351
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The FtsH Protease slr0228 Is Important for Quality Control of Photosystem II in the Thylakoid Membrane of Synechocystis sp. PCC 6803.
J. Komenda, M. Barker, S. Kuvikova, R. de Vries, C. W. Mullineaux, M. Tichy, and P. J. Nixon (2006)
J. Biol. Chem. 281, 1145-1151
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PsbR, a Missing Link in the Assembly of the Oxygen-evolving Complex of Plant Photosystem II.
M. Suorsa, S. Sirpio, Y. Allahverdiyeva, V. Paakkarinen, F. Mamedov, S. Styring, and E.-M. Aro (2006)
J. Biol. Chem. 281, 145-150
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Construction and Characterization of Genetically Modified Synechocystis sp. PCC 6803 Photosystem II Core Complexes Containing Carotenoids with Shorter {pi}-Conjugation than {beta}-Carotene.
J. A. Bautista, C. A. Tracewell, E. Schlodder, F. X. Cunningham Jr., G. W. Brudvig, and B. A. Diner (2005)
J. Biol. Chem. 280, 38839-38850
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Photosynthetic O2 Formation Tracked by Time-Resolved X-ray Experiments.
M. Haumann, P. Liebisch, C. Muller, M. Barra, M. Grabolle, and H. Dau (2005)
Science 310, 1019-1021
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Changes in Structural and Functional Properties of Oxygen-evolving Complex Induced by Replacement of D1-Glutamate 189 with Glutamine in Photosystem II: LIGATION OF GLUTAMATE 189 CARBOXYLATE TO THE MANGANESE CLUSTER.
Y. Kimura, N. Mizusawa, A. Ishii, S. Nakazawa, and T.-a. Ono (2005)
J. Biol. Chem. 280, 37895-37900
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Induced conformational changes upon Cd2+ binding at photosynthetic reaction centers.
H. Ishikita and E.-W. Knapp (2005)
PNAS 102, 16215-16220
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Protein Interactions Limit the Rate of Evolution of Photosynthetic Genes in Cyanobacteria.
T. Shi, T. S. Bibby, L. Jiang, A. J. Irwin, and P. G. Falkowski (2005)
Mol. Biol. Evol. 22, 2179-2189
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Evidence That Bicarbonate Is Not the Substrate in Photosynthetic Oxygen Evolution.
J. Clausen, K. Beckmann, W. Junge, and J. Messinger (2005)
Plant Physiology 139, 1444-1450
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Psb29, a Conserved 22-kD Protein, Functions in the Biogenesis of Photosystem II Complexes in Synechocystis and Arabidopsis.
N. Keren, H. Ohkawa, E. A. Welsh, M. Liberton, and H. B. Pakrasi (2005)
PLANT CELL 17, 2768-2781
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Initial electron donor and acceptor in isolated Photosystem II reaction centers identified with femtosecond mid-IR spectroscopy.
M. L. Groot, N. P. Pawlowicz, L. J. G. W. van Wilderen, J. Breton, I. H. M. van Stokkum, and R. van Grondelle (2005)
PNAS 102, 13087-13092
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Effects of Solar UV Radiation on Morphology and Photosynthesis of Filamentous Cyanobacterium Arthrospira platensis.
H. Wu, K. Gao, V. E. Villafane, T. Watanabe, and E. W. Helbling (2005)
Appl. Envir. Microbiol. 71, 5004-5013
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The PsbH protein is associated with the inner antenna CP47 and facilitates D1 processing and incorporation into PSII in the cyanobacterium Synechocystis PCC 6803.
J. Komenda, M. Tichy, and L. A. Eichacker (2005)
Plant Cell Physiol. 46, 1477-1483
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