Photosynthetic generation of oxygen

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 363, Issue 1504, 2008, Pages 2665-2674

  Barber, James ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Evolution; Manganese cluster; Oxygen evolving centre; Photosystem II; Structure; Water oxidation

Indexed keywords

ALGA; ATMOSPHERIC CHEMISTRY; CALCIUM; CATALYSIS; CRYSTALLOGRAPHY; CYANOBACTERIUM; EVOLUTION; MANGANESE; OXIDATION; OXYGEN; PHOTOSYNTHESIS; PROTEIN;

ALGAE; CYANOBACTERIA;

EID: 47249122894     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2008.0047     Document Type: Conference Paper

References (67)

1. Barbato, R., Race, H. L., Friso, G. & Barber, J. 1991 Chlorophyll levels in the pigment binding proteins of PSII: a study based on the chlorophyll to cytochrome ratio in different PSII preparations. FEBS Lett. 286, 86-90. (doi:10.1016/0014-5793(91)80947-2)
2. Barber, J. 1987 Photosynthetic reaction centres: a common link. Trends Biochem. Sci. 12, 321-326. (doi:10.1016/0968-0004(87)90151-4)
3. Barber, J. 2002 Photosystem II: a multisubunit membrane protein that oxidises water. Curr. Opin. Struct. Biol. 12, 523-530. (doi:10.1016/S0959-440X(02)00357-3)
4. Barber, J. 2003 Photosystem II: the engine of life. Q. Rev. Biophys. 36, 71-89. (doi:10.1017/S0033583502003839)
5. 2+-cluster of photosystem II and its protein environment as revealed by X-ray crystallography. Phil. Trans. R. Soc. B 363, 1129-1138. (doi:10.1098/rstb.2007.2208)
6. Blankenship, R. E. & Hartman, H. 1998 The origin and evolution of oxygenic photosynthesis. Trends Biochem. Sci. 23, 94-97. (doi:10.1016/S0968-0004(98)01186-4)
7. Chen, M., Hillier, R. G., Howe, C. J. & Larkum, A. W. 2005 Unique origin and lateral transfer of prokaryotics chlorophyll-b and chlorophyll-d light-harvesting systems. Mol. Biol. Evol. 22, 21-28. (doi:10.1093/molbev/msh250)
8. De Las Rivas, J. & Barber, J. 2004 Analyses of the structure of the PsbO protein and its implications. Photosyn. Res. 81, 329-343. (doi:10.1023/B:PRES.0000036889.44048.e4)
9. De Las Rivas, J., Balsera, M. & Barber, J. 2004 Evolution of oxygenic photosynthesis: genome-wide analysis of the OEC extrinsic proteins. Trends Plant Sci. 9, 18-25. (doi:10.1016/j.tplants.2003.11.007)
10. 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. Biochim. Biophys. Acta 1503, 164-186. (doi:10.1016/S0005-2728(00)00221-8)
11. Deisenhofer, J., Epp, O., Miki, K., Huber, R. & Michel, H. 1985 Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3Å resolution. Nature 318, 618-624. (doi:10.1038/318618a0)
12. 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. Biochim. Biophys. Acta 1503, 147-163. (doi:10.1016/S0005-2728(00) 00220-6)
13. Diner, B. A. & Babcock, G. T. 1996 Structure, dynamics and energy conversion efficiency in photosystem II. In Oxygenic photosynthesis: the light reactions (eds D. R. Ort & C. F. Yocum), pp. 213-247. Dordrecht, The Netherlands: Kluwer Academic Publications.
14. Dobbek, H., Svetlitchnyi, V., Gremer, L., Huber, R. & Meyer, O. 2001 Crystal structure of carbon monoxide dehydrogenase reveals a [Ni-4Fe-5S] cluster. Science 293, 1281-1285. (doi:10.1126/science.1061500)
15. Emsley, P. & Cowtan, K. 2004 Coot: model-building for molecular graphics. Acta Cryst. Sec. D: Biol. Cryst. 60, 2126-2132. (doi:10.1107/S0907444904019158)
16. Faller, P., Pascal, A. & Rutherford, A. W. 2001 β-carotene redox reactions in photosystem II: electron transfer pathway. Biochemistry 40, 6431-6440. (doi:10.1021/bi0026021)
17. Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J. & Iwata, S. 2004 Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831-1838. (doi:10.1126/science.1093087)
18. Hankamer, B., Barber, J. & Boekema, E. J. 1997 Structure and membrane organisation of PSII in green plants. Annu. Rev. Plant Phys. Mol. Biol. 48, 641-671. (doi:10.1146/annurev.arplant.48.1.641)
19. 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. Nat. Struct. Biol. 6, 560-564. (doi:10.1038/9341)
20. Hankamer, B., Morris, E. P., Nield, J., Gerle, C. & Barber, J. 2001 Three-dimensional structure of photosystem II core dimer of higher plants determined by electron microscopy. J. Struct. Biol. 135, 262-269. (doi:10.1006/jsbi.2001.4405)
21. 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. Chem. Phys. Lett. 300, 9-19. (doi:10.1016/S0009-2614(98)01369-4)
22. Hoganson, C. W. & Babcock, G. T. 1997 A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science 277, 1953-1956. (doi:10.1126/science.277.5334.1953)
23. Joliot, P., Barbieri, G. & Chabaud, R. 1969 Un nouveau modele des centres photochimiques du systeme II. Photochem. Photobiol. 10, 309-329. (doi:10.1111/j.1751-1097.1969.tb05696.x)
24. Jordan, P. et al. 2001 Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411, 909-917. (doi:10.1038/35082000)
25. Kamiya, N. & Shen, J. R. 2003 Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. Proc. Natl Acad. Sci. USA 100, 98-103. (doi:10.1073/pnas.0135651100)
26. Kashino, Y., Koike, H., Yoshio, M., Egashira, H., Ikeuchi, M., Pakrasi, H. B. & Satoh, K. 2002 Low-molecular-mass polypeptide components of a photosystem II preparation from the thermophilic cyanobacterium Thermosynechococcus vulcanus. Plant Cell Physiol. 43, 1366-1373. (doi:10.1093/pcp/pcf168)
27. 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. Biochim. Biophys. Acta 1767, 1269-1275. (doi:10.1016/j.bbabio.2007.08.008)
28. 2 evolution. 1. A linear four step mechanism. Photochem. Photobiol. 11, 457-475. (doi:10.1111/j.1751-1097.1970. tb06017.x)
29. 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. (doi:10.1038/nature04224)
30. Lundberg, M. & Siegbahn, P. E. M. 2004 Theoretical investigations of the structure and mechanism of the oxygen-evolving complex in PSII. Phys. Chem. Chem. Phys. 6, 4772-4780. (doi:10.1039/b406552b)
31. xCa structures for the catalytic site and spectroscopic data. Phys. Chem. Chem. Phys. 6, 4764-4771. (doi:10.1039/b406437b)
32. 3 state of photosystem II. Proc. Natl Acad. Sci. USA 92, 3209-3213. (doi:10.1073/pnas.92.8.3209)
33. McEvoy, J. P. & Brudvig, G. W. 2004 Structure-based mechanism of photosynthetic water oxidation. Phys. Chem. Chem. Phys. 6, 4754-4763. (doi:10.1039/b407500e)
34. McEvoy, J. P. & Brudvig, G. W. 2006 Water-splitting chemistry of photosystem II. Chem. Rev. 106, 4455-4483. (doi:10.1021/cr0204294)
35. Michel, H. & Deisenhofer, J. 1988 Relevance of the photosynthetic reaction center of purple bacteria to the structure of photosystem II. Biochemistry 27, 1-7. (doi:10.1021/bi00401a001)
36. 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. Chem. Commun. (Camb.), 54-56. (doi:10.1039/b413680b)
37. Miyashita, H., Ikemoto, H., Kurano, N., Adachi, K., Chihara, M. & Miyachi, S. 1996 A niche for cyanobacteria containing chlorophyll d. Nature 383, 402. (doi:10.1038/383402a0)
38. Morris, E. P., Hankamer, B., Zheleva, D., Friso, G. & Barber, J. 1997 The 3-D structure of a photosystem II core complex determined by electron crystallography. Structure 5, 837-849. (doi:10.1016/S0969-2126(97) 00237-2)
39. Murray, J. W. & Barber, J. 2006 Identification of a calcium-binding site in the PsbO protein of photosystem II. Biochemistry 45, 4128-4130. (doi:10.1021/bi052503t)
40. Murray, J. W. & Barber, J. 2007 Structural characteristics of channels and pathways in photosystem II including the identification of an oxygen channel. J. Struct. Biol. 159, 228-237. (doi:10.1016/j.jsb.2007.01.016)
41. Murray, J. W., Duncan, J. & Barber, J. 2006 CP43-like chlorophyll binding proteins: structural and evolutionary implications. Trends Plant Sci. 11, 152-158. (doi:10.1016/j.tplants.2006.01.007)
42. Nield, J. & Barber, J. 2006 Refinement of the structural model of the photosystem II supercomplex of higher plants. Biochim. Biophys. Acta 1757, 353-361. (doi:10.1016/j.bbabio.2006.03.019)
43. Nield, J., Orlova, E., Morris, E., Gowen, B., van Heel, M. & Barber, J. 2000a 3D map of the plant photosystem two supercomplex obtained by cryoelectron microscopy and single particle analysis. Nat. Struct. Biol. 7, 44-47. (doi:10.1038/71242)
44. Nield, J., Kruse, O., Ruprecht, J., Da Fonseca, P., Büchel, C. & Barber, J. 2000b 3D structure of Chlamydomonas reinhardtii and Synechococcus elongatus photosystem II complexes allow for comparison of their OEC organisation. J. Biol. Chem. 275, 27 940-27 946.
45. Nield, J., Balsera, M., De Las Rivas, J. & Barber, J. 2002 3D cryo-EM study of the extrinsic domains of the oxygen evolving complex of spinach. Assignment of the PsbO protein. J. Biol. Chem. 277, 15 006-15 012. (doi:10.1074/jbc.M110549200)
46. 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 Appl. Chem. 70, 925-929. (doi:10.1351/pac199870040925)
47. 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. J. Am. Chem. Soc. 122, 10 926-10 942. (doi:10.1021/ja002104f)
48. Rhee, K.-H., Morris, E. P., Zheleva, D., Hankamer, B., Kühlbrandt, W. & Barber, J. 1997 Two-dimensional structure of plant photosystem II at 8 Å resolution. Nature 389, 522-526. (doi:10.1038/39103)
49. Rhee, K.-H., Morris, E. P., Barber, J. & Kühlbrandt, W. 1998 Three-dimensional structure of the photosystem II reaction centre at 8 Å resolution. Nature 396, 283-286. (doi:10.1038/24421)
50. 2. In Sixth Int. Congress on Carbon Dioxide Utilization, 9-14 September 2001, Breckenridge, Colorado, abstr. p. 49.
51. 2 precipitates in the early oceans. Proc. Natl Acad. Sci. USA 99, 8631-8636. (doi:10.1073/pnas.132266199)
52. Schubert et al. 1998 A common ancestor for oxygenic and anoxygenic photosynthetic systems: a comparison based on the structural model of photosystem I. J. Mol. Biol. 280, 297-341. (doi:10.1006/jmbi.1998. 1824)
53. 4-state of the oxygen evolving complex in photosystem II. Chem. A Eur. J. 12, 9217-9237. (doi:10.1002/chem.200600774)
54. Siegbahn, P. E. M. & Lundberg, M. 2005 The mechanism for dioxygen formation in PSII studied by quantum chemical methods. Photochem. Photobiol. Sci. 4, 1035-1043. (doi:10.1039/b506746b)
55. Sleep, N. H. & Bird, D. K. 2007 Niches of the prephotosynthetic biosphere and geologic preservation of Earth's earliest ecology. Geobiology 5, 101-117. (doi:10.1111/j.1472-4669.2007.00105.x)
56. 2-evolving complex of photosystem II. J. Chem. Theory Comput. 2, 1119-1134. (doi:10.1021/ct0600181)
57. 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. Curr. Opin. Struct. Biol. 17, 173-180. (doi:10.1016/j.sbi.2007.03.015)
58. 559 of photosystem II. Biochim. Biophys. Acta 1367, 63-87. (doi:10.1016/S0005-2728(98)00139-X)
59. Telfer, A. 2002 What is β-carotene doing in the photosystem two reaction centre. Phil. Trans. R. Soc. B 357, 1431-1440. (doi:10.1098/rstb.2002.1139)
60. Tracewell, C. A. & Brudvig, G. W. 2003 Two redox active β-carotene molecules in photosystem II. Biochemistry 42, 9127-9136. (doi:10.1021/bi0345844)
61. Williams, J. C., Steiner, L. A. & Feher, G. 1986 Primary structures of the reaction center from Rhodopseudomonas spheroids. Proteins 1, 312-325. (doi:10.1002/prot.340010405)
62. Wydrzynski, T. J. & Satoh, K. 2005 Photosystem II: the light-driven water: plastoquinone oxidoreductase Advances in photosynthesis and respiration, pp. 1-786. Dordrecht, The Netherlands: Springer.
63. Yachandra, V. K. 2002 Structure of the Mn complex in photosystem II: insights from X-ray spectroscopy. Phil. Trans. R. Soc. B 357, 1347-1358. (doi:10.1098/rstb.2002.1133)
64. 4Ca complex in photosystem II crystals: a case study for metallo-protein X-ray crystallography. Proc. Natl Acad. Sci. USA. 102, 12 047-12 052. (doi:10.1073/pnas.0505207102)
65. 4Ca cluster. Science 314, 821-825. (doi:10.1126/science.1128186)
66. Youvan, D. C., Bylina, E. J., Alberti, M., Begusch, H. & Hearst, J. E. 1984 Nucleotide and deduced polypeptide sequences of the photosynthetic reaction center, B870 antennae and flanking polypeptides from R. capsulate. Cell 37, 949-957. (doi:10.1016/0092-8674(84)90429-X)
67. 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. (doi:10.1038/35055589)