Calcium in the oxygen-evolving complex: Structural and mechanistic role determined by X-ray spectroscopy

Journal of Photochemistry and Photobiology B: Biology

Volumn 104, Issue 1-2, 2011, Pages 51-59

  Yachandra, Vittal K ^a   Yano, Junko ^a  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Calcium; Manganese; Oxygen evolving complex; Photosystem II; X ray Absorption Spectroscopy

Indexed keywords

CALCIUM; MANGANESE;

BIOSYNTHESIS; CALCIUM ABSORPTION; CHEMICAL STRUCTURE; ELECTRON TRANSPORT; HETERONUCLEAR MULTIPLE BOND CORRELATION; LINEAR ENERGY TRANSFER; OXIDATION KINETICS; PHOTOSYNTHESIS; PHOTOSYSTEM II; PRIORITY JOURNAL; REVIEW; ROENTGEN SPECTROSCOPY;

CALCIUM; CATALYTIC DOMAIN; OXYGEN; PHOTOSYSTEM II PROTEIN COMPLEX; X-RAY ABSORPTION SPECTROSCOPY;

EID: 79957989328     PISSN: 10111344     EISSN: 18732682     Source Type: Journal    
DOI: 10.1016/j.jphotobiol.2011.02.019     Document Type: Review

References (70)

1. T. Wydrzynski, and S. Satoh Photosystem II: the light-driven water:plastoquinone oxidoreductase Govindjee Advances in Photosynthesis and Respiration 2005 Springer Dordrecht
2. 2 evolution Photochem. Photobiol. 11 1970 457 476
3. 2 evolving complex Coord. Chem. Rev. 252 2008 296 305
4. D.F. Ghanotakis, G.T. Babcock, and C.F. Yocum Calcium reconstitutes high rates of oxygen evolution in polypeptide depleted Photosystem II preparations FEBS Lett. 167 1984 127 130
5. C.J. Lockett, C. Demetriou, S.J. Bowden, and J.H.A. Nugent Studies on calcium depletion of PS II by pH 8.3 treatment Biochim. Biophys. Acta 1016 1990 213 218
6. M. Miqyass, M.A. Marosvolgyi, Z. Nagel, C.F. Yocum, and H.J. van Gorkom S-state dependence of the calcium requirement and binding characteristics in the oxygen-evolving complex of photosystem II Biochemistry 47 2008 7915 7924
7. 2+ Biochemistry 27 1988 3476 3483
8. 87Sr ESEEM spectroscopy J. Am. Chem. Soc. 126 2004 7228 7237 (Pubitemid 38747773)
9. 113Cd NMR Biochemistry 39 2000 6751 6755 (Pubitemid 30390365)
10. B. Loll, J. Kern, W. Saenger, A. Zouni, and J. Biesiadka Towards complete cofactor arrangement in the 3.0 resolution structure of photosystem II Nature 438 2005 1040 1044 (Pubitemid 43093979)
11. K.N. Ferreira, T.M. Iverson, K. Maghlaoui, J. Barber, and S. Iwata Architecture of the photosynthetic oxygen-evolving center Science 303 2004 1831 1838 (Pubitemid 38374869)
12. N. Kamiya, and J.R. Shen Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7 resolution Proc. Natl. Acad. Sci. USA 100 2003 98 103 (Pubitemid 36078036)
13. J. Kargul, K. Maghlaoul, J.W. Murray, Z. Deak, A. Boussac, A.W. Rutherford, I. Vass, and J. Barber Purification, crystallization and X-ray diffraction analyses of the T-elongatus PSII core dimer with strontium replacing calcium in the oxygen-evolving complex Biochim. Biophys. Acta - Bioenerg. 1767 2007 404 413 (Pubitemid 46855740)
14. A. Guskov, J. Kern, A. Gabdulkhakov, M. Broser, A. Zouni, and W. Saenger Cyanobacterial photosystem II at 2.9-angstrom resolution and the role of quinones, lipids, channels and chloride Nat. Struct. Mol. Biol. 16 2009 334 342
15. M.J. Latimer, V.J. DeRose, I. Mukerji, V.K. Yachandra, K. Sauer, and M.P. Klein Evidence for the proximity of calcium to the manganese cluster of photosystem II: determination by X-ray absorption spectroscopy Biochemistry 34 1995 10898 10909
16. M.J. Latimer, V.J. DeRose, V.K. Yachandra, K. Sauer, and M.P. Klein Structural effects of calcium depletion on the manganese cluster of photosystem II: determination by X-ray absorption spectroscopy J. Phys. Chem. B 102 1998 8257 8265 (Pubitemid 128611767)
17. R.M. Cinco, J.H. Robblee, A. Rompel, C. Fernandez, V.K. Yachandra, K. Sauer, and M.P. Klein Strontium EXAFS reveals the proximity of calcium to the manganese cluster of oxygen-evolving photosystem II J. Phys. Chem. B 102 1998 8248 8256 (Pubitemid 128611766)
18. R.M. Cinco, K.L.M. Holman, J.H. Robblee, J. Yano, S.A. Pizarro, E. Bellacchio, K. Sauer, and V.K. Yachandra Calcium EXAFS establishes the Mn-Ca cluster in the oxygen-evolving complex of photosystem II Biochemistry 41 2002 12928 12933 (Pubitemid 35215775)
19. 4Ca cluster of the oxygen-evolving complex determined using polarized strontium EXAFS of photosystem II membranes Biochemistry 43 2004 13271 13282 (Pubitemid 39391128)
20. 4Ca cluster from X-ray spectroscopy Inorg. Chem. 47 2008 1711 1726
21. 4Ca cluster J. Am. Chem. Soc. 127 2005 14974 14975 (Pubitemid 41547334)
22. 4Ca cluster in plant photosystem II membranes studied by polarized range-extended X-ray absorption spectroscopy J. Biol. Chem. 282 2007 7198 7208 (Pubitemid 47093654)
23. 4Ca cluster and the mechanism of photosynthetic water splitting Proc. Natl. Acad. Sci. USA 105 2008 1879 1884 (Pubitemid 351439433)
24. 4Ca complex in photosystem II crystals: a case study for metallo-protein X-ray crystallography Proc. Natl. Acad. Sci. USA 102 2005 12047 12052 (Pubitemid 41291126)
25. R.A. Scott X-ray absorption spectroscopy D.L. Rousseau, Structural and Resonance Techniques in Biological Research 1984 Academic Press Orlando 295 362
26. S.P. Cramer, Biochemical applications of X-ray absorption spectroscopy, in: D.C. Koningsberger, R. Prins (Eds.), X-ray Absorption: Principles, Applications and Techniques of EXAFS, SEXAFS, and XANES, Wiley-Interscience, New York, 1988, pp. 257-326.
27. V.K. Yachandra X-ray absorption spectroscopy and applications in structural biology Methods Enzymol. 246 1995 638 675
28. J. Yano, and V.K. Yachandra X-ray absorption spectroscopy Photosynth. Res. 102 2009 241 254
29. 4Ca cluster in photosystem II Photosynth. Res. 92 2007 289 303 (Pubitemid 47248572)
30. V.K. Yachandra, K. Sauer, and M.P. Klein Manganese cluster in photosynthesis: where plants oxidize water to dioxygen Chem. Rev. 96 1996 2927 2950 (Pubitemid 126641122)
31. 2 states Biochem. J. 285 1992 569 576
32. 2-evolving complex in spinach PS II: the S 1, S 2 and S 3 states and the role of the 17 kDa and 23 kDa extrinsic polypeptides Biochim. Biophys. Acta 1186 1994 186 200
33. P.J. Riggs-Gelasco, R. Mei, D.F. Ghanotakis, C.F. Yocum, and J.E. PennerHahn X-ray absorption spectroscopy of calcium-substituted derivatives of the oxygen-evolving complex of phostosystem II J. Am. Chem. Soc. 118 1996 2400 2410 (Pubitemid 26120921)
34. N. Tamura, and G. Cheniae Effects of photosystem-II extrinsic proteins on microstructure of the oxygen-evolving complex and its reactivity to water analogs Biochim. Biophys. Acta 809 1985 245 259
35. 4-clusters by preventing ligation of nonfunctional high-valency states of manganese Biochemistry 34 1995 13511 13526
36. VO species in photosynthetic water oxidation, J. Chem. Soc. Dalton Trans. (1999) 1353-1361.
37. G. Renger Mechanistic and structural aspects of photosynthetic water oxidation Physiol. Plant. 100 1997 828 841 (Pubitemid 27383530)
38. P.E.M. Siegbahn Theoretical models for the oxygen radical mechanism of water oxidation and of the water oxidizing complex of photosytem II Inorg. Chem. 39 2000 2923 2935
39. G.M. Ananyev, and G.C. Dismukes Calcium induces binding and formation of a spin-coupled dimanganese (II, II) center in the apo-water oxidation complex of photosystem II as precursor to the functional tetra-Mn/Ca Cluster Biochemistry 36 1997 11342 11350 (Pubitemid 27408616)
40. H. Dau, J.C. Andrews, T.A. Roelofs, M.J. Latimer, W. Liang, V.K. Yachandra, K. Sauer, and M.P. Klein Structural consequences of ammonia binding to the manganese cluster of the photosynthetic oxygen-evolving complex: an X-ray absorption study of isotropic and oriented photosystem II particles Biochemistry 34 1995 5274 5287
41. I. Mukerji, J.C. Andrews, V.J. DeRose, M.J. Latimer, V.K. Yachandra, K. Sauer, and M.P. Klein Orientation of the oxygen-evolving manganese complex in a photosystem II membrane preparation: an X-ray absorption spectroscopy study Biochemistry 33 1994 9712 9721 (Pubitemid 24272932)
42. U. Bergmann, S.P. Cramer, A high-resolution large-acceptance analyzer for X-ray fluorescence and Raman spectroscopy, in: SPIE Conference on Crystal and Multilayer Optics, SPIE, San Diego, CA, 1998, pp. 198-209.
43. 4Ca cluster in plant photosystem II membranes studied by polarized range-extended X-ray absorption spectroscopy J. Biol. Chem. 282 2007 7198 7208 (Pubitemid 47093654)
44. A. Zouni, H.T. Witt, J. Kern, P. Fromme, N. Krauss, W. Saenger, and P. Orth Crystal structure of photosystem II from Synechococcus elongatus at 3.8 resolution Nature 409 2001 739 743 (Pubitemid 32144521)
45. 2+ exchange in the photosystem II oxygen-evolving enzyme of Thermosynechococcus elongatus J. Biol. Chem. 279 2004 22809 22819 (Pubitemid 38685581)
46. A. Mishra, J. Yano, Y. Pushkar, V.K. Yachandra, K.A. Abboud, G. Christou, Heteronuclear MnCa/Sr Model Complexes, and Ca/Sr EXAFS spectral comparisons with the oxygen-evolving complex of photosystem II, Chem. Commun. (2007) 1538-1540. (Pubitemid 46570689)
47. 4Ca cluster Science 314 2006 821 825 (Pubitemid 44706649)
48. T. Kuntzleman, M. McCarrick, J. Penner-Hahn, and C. Yocum Probing reactive sites within the photosystem II manganese cluster: evidence for separate populations of manganese that differ in redox potential Phys. Chem. Chem. Phys. 6 2004 4897 4904
49. 3 state transition of the oxygen-evolving complex of photosystem II. Does it reflect the onset of water/substrate oxidation? Determination by Mn X-ray absorption spectroscopy J. Am. Chem. Soc. 122 2000 3399 3412 (Pubitemid 30211113)
50. 2+ binding to the oxygen evolving enzyme varies with the redox state of the Mn cluster FEBS Lett. 236 1988 432 436
51. 55Mn-ENDOR and EPR spectroscopy J. Am. Chem. Soc. 129 2007 13421 13435 (Pubitemid 350071770)
52. 2 formation in photosystem II Acc. Chem. Res. 42 2009 1871 1880
53. H. Suzuki, M. Sugiura, and T. Noguchi Monitoring proton release during photosynthetic water oxidation in photosystem II by means of isotope-edited infrared spectroscopy J. Am. Chem. Soc. 131 2009 7849 7857
54. F. Rappaport, and J. Lavergne Coupling of electron and proton transfer in the photosynthetic water oxidase Bichim. Biophys. Acta 1503 2001 246 259
55. M.J. Baldwin, T.L. Stemmler, P.J. Riggs-Gelasco, M.L. Kirk, J.E. Penner-Hahn, and V.L. Pecoraro Structural and magnetic effects of successive protonations of oxo bridges in high-valent manganese dimers J. Am. Chem. Soc. 116 1994 11349 11356 (Pubitemid 127657938)
56. 2 moieties in the tetranuclear Mn complex? J. Am. Chem. Soc. 124 2002 7459 7471 (Pubitemid 34685486)
57. 2 transition: an isotope-edited FTIR study Biochemistry 43 2004 3152 3166 (Pubitemid 38352265)
58. Y. Kimura, N. Mizusawa, T. Yamanari, A. Ishii, and T. Ono Structural changes of D1 C-terminal alpha-carboxylate during S-state cycling in photosynthetic oxygen evolution J. Biol. Chem. 280 2005 2078 2083
59. P.E.M. Siegbahn, and R.H. Crabtree 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 1999 117 127 (Pubitemid 29047129)
60. M. Lundberg, M.R.A. Blomberg, and P.E.M. Siegbahn Oxyl radical required for O-O bond formation in synthetic Mn-catalyst Inorg. Chem. 43 2004 264 274
61. J.P. McEvoy, and G.W. Brudvig Water-splitting chemistry of photosystem II Chem. Rev. 106 2006 4455 4483 (Pubitemid 44816649)
62. H.-A. Chu, W. Hillier, N.A. Law, and G.T. Babcock Vibrational spectroscopy of the oxygen-evolving complex and of manganese model compounds Biochim. Biophys. Acta 1503 2001 69 82
63. 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 2003 6209 6217 (Pubitemid 36605123)
64. 2 state of photosystem II? Appl. Mag. Res. 37 2010 123 136
65. J.S. Vrettos, J. Limburg, and G.W. Brudvig Mechanism of photosynthetic water oxidation: combining biophysical studies of photosystem II with inorganic model chemistry Biochim. Biophys. Acta 1503 2001 229 245
66. 4+ ion J. Am. Chem. Soc. 126 2004 9786 9795 (Pubitemid 39031061)
67. S. Romain, F. Bozoglian, X. Sala, and A. Llobet Oxygen-oxygen bond formation by the Ru-Hbpp water oxidation catalyst occurs solely via an intramolecular reaction pathway J. Am. Chem. Soc. 131 2009 2768 2769
68. J.J. Concepcion, J.W. Jurss, M.K. Brennaman, P.G. Hoertz, A.O.T. Patrocinio, N.Y.M. Iha, J.L. Templeton, and T.J. Meyer Making oxygen with ruthenium complexes Acc. Chem. Res. 42 2009 1954 1965
69. 2+ Scaffold: effects on catalytic water oxidation J. Am. Chem. Soc. 132 2010 16094 16106
70. IV-O J. Am. Chem. Soc. 128 2006 7476 7485 (Pubitemid 43877520)