S1-state Mn4Ca complex of Photosystem II exists in equilibrium between the two most-stable isomeric substates: XRD and EXAFS evidence

Journal of Photochemistry and Photobiology B: Biology

Volumn 104, Issue 1-2, 2011, Pages 100-110

  Kusunoki, Masami ^a  

^a MEIJI UNIVERSITY   (Japan)

Author keywords

DFT B3LYP method; Extended range EXAFS; Isomer; Manganese cluster; Photosystem II; Statistical dynamical X ray diffraction effect

Indexed keywords

ISOMER; MASS SPECTROMETRY; NONHUMAN; PHOTOCATALYSIS; PHOTOOXIDATION; PHOTOSYSTEM II; PHYTOCHEMISTRY; PRIORITY JOURNAL; REVIEW; SYNECHOCOCCUS; THERMOSYNECHOCOCCUS VULCANUS; CHEMISTRY; ENZYME ACTIVE SITE; ISOMERISM; METABOLISM; X RAY ABSORPTION SPECTROSCOPY;

THERMOSYNECHOCOCCUS VULCANUS;

CALCIUM; MANGANESE; WATER;

CALCIUM; CATALYTIC DOMAIN; ISOMERISM; MANGANESE; PHOTOSYSTEM II PROTEIN COMPLEX; WATER; X-RAY ABSORPTION SPECTROSCOPY;

EID: 79958012085     PISSN: 10111344     EISSN: 18732682     Source Type: Journal    
DOI: 10.1016/j.jphotobiol.2011.03.002     Document Type: Review

References (73)

1. 2 evolution-I. A linear four step mechanism Photochem. Photobiol. 11 1970 457 475
2. P. Joliot, and B. Kok Oxygen Evolution in Photosynthesis 1975 Academic Press New York
3. G. Renger, and T. Renger Photosystem II: the machinery of photosynthetic water splitting Photosynth. Res. 98 2008 53 80 (Pubitemid 50289510)
4. B. Velthuys, and B. Kok Photosynthetic oxygen evolution from hydrogen peroxide Biochim. Biophys. Acta 502 1978 211 221 (Pubitemid 8326464)
5. -3 state of the water oxidase in photosystem II Biochemistry 36 1997 6862 6873 (Pubitemid 27258098)
6. -1 to the state characterized by the Mn(II)-Mn(III) multiline EPR signal Biochemistry 37 1998 16445 16451 (Pubitemid 28543901)
7. -2 of the water oxidase in isolated spinach thylakoids Biochemistry 32 1993 9379 9386 (Pubitemid 23292057)
8. -2 state in the oxygen-evolving complex of photosystem II from Synechococcus elongatus Biochemistry 42 2003 1016 1023 (Pubitemid 36159535)
9. -1 state in spinach thylakoids Biochim. Biophys. Acta 1708 2005 35 41 (Pubitemid 40798528)
10. H. Dau, and M. Haumann Reaction cycle of photosynthetic water oxidation in plants and cyanobacteria Science 312 2006 1471 1472
11. 2 formation tracked by time-resolved X-ray experiments Science 310 2005 1019 1021 (Pubitemid 41611914)
12. D.R.J. Kolling, T.S. Brown, G. Ananyev, and G.C. Dismukes Photosynthetic oxygen evolution is not reversed at high oxygen pressures: mechanistic consequences for the water-oxidizing complex Biochemistry 48 2009 1381 1389
13. D. Shevela, K. Beckmann, J. Clausen, W. Junge, and J. Messinger Membrane-inlet mass spectrometry reveals a high driving force for oxygen production by photosystem II Proc. Natl. Acad. Sci. USA 108 2011 3602 3607
14. J. Clausen, and W. Junge Search for intermediates of photosynthetic water oxidation Photosynth. Res. 84 2005 339 345 (Pubitemid 41110667)
15. G. Renger, and W. Weiss Studies on the nature of the water-oxidizing enzyme: III. Spectral characterization of the intermediary redox states in the water-oxidizing enzyme system Y Biochim. Biophys. Acta 850 1986 184 196
16. J.P. Dekker, H.J. van Gorkom, J. Wensink, and L. Ouwenand Absorbance difference spectra of the successive redox states of the oxygen-evolving apparatus of photosynthesis Biochim. Biophys. Acta 767 1984 1 9
17. J. Lavergne Improved UV-visible spectra of the S-transitions in the photosynthetic oxygen-evolving system Biochim. Biophys. Acta 1060 1991 175 188
18. T. Ono, T. Noguchi, Y. Inoue, M. Kusunoki, T. Matsushita, and H. Oyanagi X-ray detection of the period-four cycling of the manganese cluster in photosynthetic water oxidizing enzyme Science 258 1992 1335 1337 (Pubitemid 23007782)
19. T.A. Roelofs, W. Liang, M.J. Latimer, R.M. Cinco, A. Rompel, J.C. Andrews, K. Sauer, V.K. Yachandra, and M.P. Klein Oxidation states of the manganese cluster during the flash-induced S-state cycle of the photosynthetic oxygen-evolving complex Proc. Natl. Acad. Sci. USA 93 1996 3335 3340
20. M. Haumann, and W. Junge Extent and rate of proton release by photosynthetic water oxidation in thylakoids: electrostatic relaxation versus chemical production Biochemistry 33 1994 864 872 (Pubitemid 24058423)
21. M. Haumann, A. Mulkidjanian, and W. Junge Electrogenicity of electron and proton transfer at the oxidizing side of photosystem II Biochemistry 36 1997 9304 9315 (Pubitemid 27346967)
22. E. Schlodder, and H.T. Witt Stoichiometry of proton release from the catalytic center in photosynthetic water cleavages in photosynthetic water oxidation. Re-examination by a glass electrode study at pH 5.5-7.2 J. Biol. Chem. 274 1999 30387 30392
23. 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
24. G.C. Dismukes, and Y. Siderer Intermediates of a polynuclear manganese center involved in photosynthetic oxidation of water Proc. Natl. Acad. Sci. USA 78 1981 274 278
25. J.L. Casey, and K. Sauer EPR detection of a cryogenically photogenerated intermediate in photosynthetic oxygen evolution Biochim. Biophys. Acta 767 1984 21 28
26. J.-L. Zimmermann, and A.W. Rutherford EPR studies of the oxygen-evolving enzyme of photosystem II Biochim. Biophys. Acta 767 1984 160 167
27. A. Boussac, J.J. Girerd, and A.W. Rutherford Conversion of the spin state of the manganese complex in photosystem II induced by near-infrared light Biochemistry 35 1996 6984 6989 (Pubitemid 26182086)
28. 2 state of photosystem II Biochim Biophys Acta 1457 2000 145 156 (Pubitemid 30201478)
29. 2 state of photosystem II confirms an S = 5/2 origin of the X-band g = 4.1 signal Biophys. J. 87 2004 2885 2896
30. J. Messinger, J.H.A. Nugent, and M.C.W. Evans Detection of an EPR multiline signal for the S 0 state in photosystem II Biochemistry 36 1997 11055 11060 (Pubitemid 27398424)
31. 0 state of the oxygen evolving complex in photosystem II Biochemistry 36 1997 13148 13152 (Pubitemid 27473358)
32. 1-state manganese cluster in the photosynthetic oxygen-evolving system Biochemistry 36 1997 7520 7526 (Pubitemid 27262377)
33. 1-state 'multiline' EPR signal in photosystem II particles from Synechocystis sp. PCC 6803, J. Am. Chem. Soc. 120 (1998) 447-448. (Pubitemid 28062540)
34. 3-state of oxygen-evolving complex in photosystem II Biochemistry 38 1999 4072 4077
35. 3-state of the oxygen-evolving photosystem II J. Am. Chem. Soc. 131 2009 5050 5051
36. 2 state of a photosynthetic water-splitting enzyme Chem. Phys. Lett. 197 1992 108 116
37. 2-state multiline EPR signal in oriented photosystem II membranes: structural implications for the manganese cluster in an oxygen-evolving complex Biochemistry 37 1998 9457 9465 (Pubitemid 28307702)
38. 2-state manganese tetramer in photosynthetic oxygen-evolving complex deduced from g = 2 multiline EPR signal Chem. Phys. Lett. 300 1999 9 19 (Pubitemid 129335019)
39. 2-state multiline EPR signal of photosystem II: implications on the structure of the tetranuclear Mn cluster J. Am. Chem. Soc. 122 2000 10926 10942
40. 2 state through quantum chemical calculation of its magnetic properties Phys. Chem. Chem. Phys. 11 2009 6788 6798
41. 2 states of the oxygen-evolving complex in photosystem II J. Am. Chem. Soc. 127 2005 2392 2393 (Pubitemid 40327794)
42. J. Yano, and V.K. Yachandra X-ray absorption spectroscopy Photosynth. Res. 102 2009 241 254
43. 4Ca cluster. J. Am. Chem. Soc. 127 2005 14974 14975 (Pubitemid 41547334)
44. H. Dau, L. Iuzzolino, and J. Dittmer The tetra-manganese complex of photosystem II during its redox cycle - X-ray absorption results and mechanistic implications Biochim. Biophys. Acta 1503 2001 24 39
45. H. Dau, A. Grundmeier, P. Loja, and M. Haumann On the structure of the manganese complex of photosystem II: extended-range EXAFS data and specific atomic-resolution models for four S-states Philos. Trans. Roy. Soc. Lond. B: Biol. Sci. 363 2008 1237 1243 discussion 1243-1234 (Pubitemid 351225978)
46. G. Hendry, and T. Wydrzynski (18)O 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)
47. W. Hillier, and T. Wydrzynski Substrate water interactions within the photosystem II oxygen evolving complex Phys. Chem. Chem. Phys. 6 2004
48. S. Singh, R.J. Debus, T. Wydrzynski, and W. Hillier Investigation of substrate water interactions at the high-affinity Mn site in the photosystem II oxygen-evolving complex Philos. Trans. Roy. Soc. Lond. B: Biol. Sci. 363 2008 1229 1234 discussion 1234-1225 (Pubitemid 351225972)
49. 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 A resolution Nature 409 2001 739 743 (Pubitemid 32144521)
50. N. Kamiya, and J.R. Shen Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-A resolution Proc. Natl. Acad. Sci. USA 100 2003 98 103 (Pubitemid 36078036)
51. 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)
52. J. Kern, B. Loll, A. Zouni, W. Saenger, K.D. Irrgang, and J. Biesiadka Cyanobacterial photosystem II at 3.2 A resolution - the plastoquinone binding pockets Photosynth. Res. 84 2005 153 159 (Pubitemid 41110641)
53. B. Loll, J. Kern, W. Saenger, A. Zouni, and J. Biesiadka Towards complete cofactor arrangement in the 3.0 A resolution structure of photosystem II Nature 438 2005 1040 1044 (Pubitemid 43093979)
54. A. Guskov, J. Kern, A. Gabdulkhakov, M. Broser, A. Zouni, and W. Saenger Cyanobacterial photosystem II at 2.9-A resolution and the role of quinones, lipids, channels and chloride Nat. Struct. Mol. Biol. 16 2009 334 342
55. J.-R. Shen, Y. Umena, K. Kawakami, N. Kamiya, Crystal structure of oxygen evolving photosystem II at an atomic resolution, in: Photosynthesis: Research for Food, Fuel and the Future; Abstracts of the 15th International Congress of Photosynthesis, Beijing, 2010, pp. 87-88.
56. 4Ca complex in single crystals of photosystem II: a case study for metalloprotein crystallography Proc. Natl. Acad. Sci. USA 102 2005 12047 12052 (Pubitemid 41291126)
57. 2- evolving center by replacement of chloride with other anions Arch. Biochem. Biophys. 256 1987 618 624
58. P. van Vliet, and A.W. Rutherford Properties of the chloride-depleted oxygen-evolving complex of photosystem II studied by electron paramagnetic resonance Biochemistry 35 1996 1829 1839 (Pubitemid 26062632)
59. 4Ca cluster Biochim. Biophys. Acta 1767 2007 484 492 Corregendom, Biochim. Biophys. Acta 1777 (2008) 477 (Pubitemid 46860311)
60. M. Lundberg, and P.E.M. Siegbahn Theoretical investigations of structure and mechanism of the oxygen-evolving complex in PSII Phys. Chem. Chem. Phys. 6 2004
61. J.P. McEvoy, J.A. Gascon, V.S. Batista, and G.W. Brudvig The mechanism of photosynthetic water splitting Photochem. Photobiol. Sci. 4 2005 940 949 (Pubitemid 41818863)
62. E.M. Sproviero, J.A. Gascon, J.P. McEvoy, G.W. Brudvig, and V.S. Batista Quantum mechanics/molecular mechanics study of the catalytic cycle of water splitting in photosystem II J. Am. Chem. Soc. 130 2008 3428 3442 (Pubitemid 351456044)
63. 2 formation in photosystem II Acc. Chem. Res. 42 2009 1871 1880
64. M. Kusunoki, Catalytic cooperativity of mono-manganese and tri-manganese clusters for water-splitting and oxygen-evolving reaction in photosystem II: chemical mechanistic insight, in: Photosynthesis: Research for Food, Fuel and the Future; Abstracts of the 15th International Congress of Photosynthesis at Beijing, 2010, PS6.22, pp. 97-99.
65. J.J. Rehr, J. Mustre de Leon, S.I. Zabinsky, and R.C. Albers Theoretical X-ray absorption fine structure standards J. Am. Chem. Soc. 113 1991 5135 5140
66. A.L. Ankudinov, B. Ravel, J.J. Rehr, and S.D. Conradson Real-space multiple-scattering calculation and interpretaion of X-ray-absorption near-edge structure Phys. Rev. B 58 1998 7565 7576 (Pubitemid 128486524)
67. Jaguar7.6, vol. Schrodinger, L.L.C., Portland, OR, 1991-2009.
68. 2-evolving complex in photosystem II: evaluation of the DFT/B3LYP level of theory J. Inorg. Biochem. 100 2006 786 800
69. D.E. Sayers, E.A. Stern, and F.W. Lytle New technique for investigating noncrystalline structures: Fourier analysis of the extended X-ray absorption fine structure Phys. Rev. Lett. 27 1971 1204 1207
70. A.V. Poiarkova, and J.J. Rehr Multiple-scattering X-ray-absorption fine-structure Debye-Waller factor calculations Phys. Rev. B 59 1999 948 957
71. P.E. Siegbahn An energetic comparison of different models for the oxygen evolving complex of photosystem II J. Am. Chem. Soc. 131 2009 18238 18239
72. 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)
73. 1-state MnCaCl cluster in photosystem II, in: Proc. 12th Int. Congr. Photosynthesis, CSIRO Publishing, Collingwood, Australia, 2001, pp. S13-012.