Water oxidation chemistry of photosystem II

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 363, Issue 1494, 2008, Pages 1211-1219

  Brudvig, Gary W ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

Calcium; Manganese; Oxygen evolving complex; Photosystem II; Water oxidation

Indexed keywords

AMINO ACID; BIOPHYSICS; CALCIUM; CATALYST; CRYSTALLOGRAPHY; CYANOBACTERIUM; ELECTRON; MANGANESE; OXIDATION; OXYGEN; PHOTOSYNTHESIS; WATER; X-RAY SPECTROSCOPY;

CYANOBACTERIA;

EID: 38949151612     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2007.2217     Document Type: Article

References (64)

1. Bouckaert, J., Loris, R. & Wyns, L. 2000 Zinc/calcium- and cadmium/cadmium-substituted concanavalin A: interplay of metal binding, pH and molecular packing. Acta Cryst. D 56, 1569-1576. (doi:10.1107/S0907444900013342)
2. 2 evolution. Proc. Natl Acad. Sci. USA 83, 4586-4588. (doi:10.1073/pnas.83.13.4586)
3. Brudvig, G. W., Casey, J. L. & Sauer, K. 1983 The effect of temperature on the formation and decay of the multiline EPR signal species associated with photosynthetic oxygen evolution. Biochim. Biophys. Acta 723, 366-371. (doi:10.1016/0005-2728(83)90042-7)
4. -. Inorg. Chem. 46, 34-43. (doi:10.1021/ic060499j)
5. Clausen, J. & Junge, W. 2004 Detection of an intermediate of photosynthetic water oxidation. Nature 430, 480-483. (doi:10.1038/nature02676)
6. Collins, T. J. & Gordon-Wylie, S. W. 1989 A manganese(V)-oxo complex. J. Am. Chem. Soc. 111, 4511-4513. (doi:10.1021/ja00194a063)
7. Collins, T. J., Powell, R. D., Slebodnick, C. & Uffelman, E. S. 1990 A water-stable manganese(V)-oxo complex - efinitive assignment of a ν(Mn(V)O) infrared vibration. J. Am. Chem. Soc. 112, 899-901. (doi:10.1021/ja00158a077)
8. Cooper, S. R. & Calvin, M. 1977 Mixed-valence interactions in di-μ-oxo bridged manganese complexes. J. Am. Chem. Soc. 99, 6623-6630. (doi:10.1021/ja00462a025)
9. Cooper, S. R., Dismukes, G. C., Klein, M. P. & Calvin, M. 1978 Mixed valence interactions in di-μ-oxo bridged manganese complexes. Electron paramagnetic resonance and magnetic susceptibility studies. J. Am. Chem. Soc. 100, 7248-7252. (doi:10.1021/ja00491a021)
10. Dasgupta, J., van Willigen, R. T. & Dismukes, G. C. 2004 Consequences of structural and biophysical studies for the molecular mechanism of photosynthetic oxygen evolution: functional roles for calcium and bicarbonate. Phys. Chem. Chem. Phys. 6, 4793-4802. (doi:10.1039/b408270b)
11. Dau, H., Iuzzolino, L. & Dittmer, J. 2001 The tetramanganese complex of photosystem II during its redox cycle - X-ray absorption results and mechanistic implications. Biochim. Biophys. Acta 1503, 24-39. (doi:10.1016/S0005-2728(00)00230-9)
12. Dean, J. A. (ed.) 1985 Lange's handbook of chemistry. New York, NY: McGraw-Hill.
13. Debus, R. J. 2001 Amino acid residues that modulate the properties of tyrosine YZ 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)
14. 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)
15. 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)
16. Fleischer, E. B., Palmer, J. M., Srivastava, T. S. & Chatterjee, A. 1971 Thermodyamic and kinetic properties of an ironporphyrin system. J. Am. Chem. Soc. 93, 3162-3167. (doi:10.1021/ja00742a012)
17. 2 formation tracked by time-resolved X-ray experiments. Science 310, 1019-1021. (doi:10.1126/science.1117551)
18. 2 state of photosystem II. Biochemistry 41, 13 328-13 334. (doi:10.1021/bi026246t)
19. 18O isotope exchange measurements reveal that calcium is involved in the binding of one substrate-water molecule to the oxygen-evolving complex in photosystem II. Biochemistry 42, 6209-6217. (doi:10.1021/bi034279i)
20. Hillier, W. & Messinger, J. 2005 Mechanism of photosynthetic oxygen production. In Photosystem II: the light-driven water : plastoquinone oxidoreductase (eds T. J. Wydrzynski & K. Satoh), pp. 567-608. Dordrecht, The Netherlands: Springer.
21. 2 evolving complex of photosystem II vary independently during S-state turnover. Biochemistry 39, 4399-4405. (doi:10.1021/bi992318d)
22. 2 evolving mechanism of photosystem II. Biochim. Biophys. Acta 1503, 197-209. (doi:10.1016/S0005-2728(00) 00225-5)
23. Hillier, W. & Wydrzynski, T. 2004 Substrate water interactions within the photosystem II oxygen evolving complex. Phys. Chem. Chem. Phys. 6, 4882-4889. (doi:10.1039/b407269c)
24. 3 state of photosystem II. Biochemistry 37, 16 908-16 914. (doi:10.1021/bi980756z)
25. 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)
26. Ishikita, H., Saenger, W., Loll, B., Biesiadka, J. & Knapp, E. W. 2006 Energetics of a possible proton exit pathway for water oxidation in photosystem II. Biochemistry 45, 2063-2071. (doi:10.1021/ bi051615h)
27. Isobe, H., Shoji, M., Koizumi, K., Kitagawa, Y., Yamanaka, S., Kuramitsu, S. & Yamaguchi, K. 2005 Electronic and spin structures of manganese clusters in the photosynthesis II system. Polyhedron 24, 2767-2777. (doi:10.1016/j.poly.2005.08.049)
28. Junge, W., Haumann, M., Ahlbrink, R., Mulkidjanian, A. & Clausen, J. 2002 Electrostatics and proton transfer in photosynthetic water oxidation. Phil. Trans. R. Soc. B 357, 1407-1417. (doi:10.1098/rstb.2002. 1137)
29. Kamiya, N. & Shen, J. R. 2003 Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7 angstrom resolution. Proc. Natl Acad. Sci. USA 100, 98-103. (doi:10.1073/pnas.0135651100)
30. 2 evolution - I. A linear four step mechanism. Photochem. Photobiol. 11, 457-475.
31. 2+ in the oxygen-evolving complex of photosystem II by metal ion inhibition. Biochemistry 46, 3211-3223. (doi:10.1021/bi062033i)
32. V=O species in photosynthetic water oxidation. J. Chem. Soc. Dalton Trans. 1353-1362. (doi:10.1039/a807583b)
33. 2-evolving complex in photosystem II. Science 283, 1524-1527. (doi:10.1126/science.283.5407.1524)
34. 2 (terpy=2,2′-6,2″-terpyridine). J. Am. Chem. Soc. 123, 423-430. (doi:10.1021/ja001090a)
35. 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)
36. Lundberg, M. & Siegbahn, P. E. M. 2005 Agreement between experiment and hybrid DFT calculations for O-H bond dissociation enthalpies in manganese complexes. J. Comput. Chem. 26, 661-667. (doi:10.1002/jcc.20206)
37. MacDonnell, F. M., Fackler, N. L. P., Stern, C. & O'Halloran, T. V. 1994 Air oxidation of a 5-coordinate Mn(III ) dimer to a high-valent oxomanganese(V) complex. J. Am. Chem. Soc. 116, 7431-7432. (doi:10.1021/ja00095a066)
38. 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)
39. McEvoy, J. P. & Brudvig, G. W. 2006 Water-splitting chemistry of photosystem II. Chem. Rev. 106, 4455-4483. (doi:10.1021/cr0204294)
40. McPhalen, C. A., Strynadka, N. C. J. & James, M. N. G. 1991 Calcium-binding sites in proteins: a structural perspective. Adv. Protein Chem. 42, 77-144.
41. xCa structures for the catalytic site and spectroscopic data. Phys. Chem. Chem. Phys. 6, 4764-4771. (doi:10.1039/b406437b)
42. Messinger, J., Badger, M. & Wydrzynski, T. 1995 Detection of one slowly exchanging substrate water molecule in the S3 state of photosystem II. Proc. Natl Acad. Sci. USA 92, 3209-3213. (doi:10.1073/pnas.92.8. 3209)
43. Nugent, J. H. A., Rich, A. M. & Evans, M. C. W. 2001 Photosynthetic water oxidation: towards a mechanism. Biochim. Biophys. Acta 1503, 138-146. (doi:10.1016/S0005-2728(00)00223-1)
44. Pecoraro, V. L., Baldwin, M. J. & Gelasco, A. 1994 Interaction of manganese with dioxygen and its reduced derivatives. Chem. Rev. 94, 807-826. (doi:10.1021/cr00027a012)
45. Pecoraro, V. L., Baldwin, M. J., Caudle, M. T., Hsieh, W.-Y. & Law, N. A. 1998 A proposal for water oxidation in photosystem II. Pure Appl. Chem. 70, 925-929.
46. Riggs-Gelasco, P. J., Mei, R., Ghanotakis, D. F., Yocum, C. F. & Penner-Hahn, J. E. 1996 X-ray absorption spectroscopy of calcium-substituted derivatives of the oxygen-evolving complex of phostosystem II. J. Am. Chem. Soc. 118, 2400-2410. (doi:10.1021/ja9504505)
47. 6: a partial model for photosynthetic water binding and activation. Inorg. Chem. 39, 1021-1027. (doi:10.1021/ic9911421)
48. Siegbahn, P. E. M. 2000 Theoretical models for the oxygen radical mechanism of water oxidation and of the water oxidizing complex of photosystem II. Inorg. Chem. 39, 2923-2935. (doi:10.1021/ic9911872)
49. Siegbahn, P. E. M. & Crabtree, R. H. 1999 Manganese oxyl radical intermediates and O-O bond formation in photosynthetic oxygen evolution and a proposed role for the calcium cofactor in photosystem II. J. Am. Chem. Soc. 121, 117-127. (doi:10.1021/ja982290d)
50. Siegbahn, P. E. M. & Lundberg, M. 2005 The mechanism of dioxygen formation in PSII studied by quantum chemical methods. Photochem. Photobiol. Sci. 6, 4793-4802.
51. Sjoberg, B.-M., Loehr, T. M. & Sanders-Loehr, J. 1982 Raman spectral evidence for a μ-oxo bridge in the binuclear iron center of ribonucleotide reductase. Biochemistry 21, 96-102. (doi:10.1021/bi00530a017)
52. 2-evolving complex of photosystem II. J. Chem. Theory Comput. 2, 1119-1134. (doi:10.1021/ct060018l)
53. 2-evolving complex of photosystem II. In Photosynthesis: mechanisms and effects (ed. G. Garab), pp. 1403-1406. Dordrecht, The Netherlands: Kluwer Academic.
54. Tagore, R., Chen, H., Crabtree, R. H. & Brudvig, G. W. 2006 Determination of bridging-oxo exchange in di-μ-oxo dimanganese complexes by electrospray ionization mass spectrometry. J. Am. Chem Soc. 128, 9457-9465. (doi:10.1021/ja061348i)
55. 2-evolving complex of photosystem II. Inorg. Chem. 46, 2193-2203. (doi:10.1021/ic061968k)
56. Tagore, R., Crabtree, R. H. & Brudvig, G. W. In press. Oxygen evolution catalysis by a dimanganese complex and its relation to photosynthetic water oxidation. Inorg. Chem.
57. Vincent, J. B. & Christou, G. 1987 A molecular double-pivot mechanism for water oxidation. Inorg. Chim. Acta 136, L41-L43. (doi:10.1016/S0020-1693(00)81142-1)
58. Volkov, A. G. 1989 Oxygen evolution in the course of photosynthesis - molecular mechanisms. Bioelectrochem. Bioenerg. 21, 3-24. (doi:10.1016/0302-4598(89)87002-3)
59. Vrettos, J. S., Limburg, J. & Brudvig, G. W. 2001a Mechanism of photosynthetic water oxidation: combining biophysical studies of photosystem II with inorganic model chemistry. Biochim. Biophys. Acta 1503, 229-245. (doi:10.1016/S0005-2728(00)00214-0)
60. 2 formation. Biochemistry 40, 7937-7945. (doi:10.1021/bi010679z)
61. Weast, R. C. (ed.) 1978 CRC handbook of chemistry and physics, West Palm Beach, FL: CRC Press.
62. Wilkins, R. G. & Yelin, R. E. 1969 Kinetics of monomerdimer interconversion of iron(III ) ethylenediaminetetra-acetate and related chelates. Inorg. Chem. 8, 1470-1473. (doi:10.1021/ic50077a020)
63. Yachandra, V. K., Sauer, K. & Klein, M. P. 1996 Manganese cluster in photosynthesis: where plants oxidize water to dioxygen. Chem. Rev. 96, 2927-2950. (doi:10.1021/cr950052k)
64. 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 angstrom resolution. Nature 409, 739-743. (doi:10.1038/35055589)