Quantum mechanics/molecular mechanics study of the catalytic cycle of water splitting in photosystem II

Journal of the American Chemical Society

Volumn 130, Issue 11, 2008, Pages 3428-3442

  Sproviero, Eduardo M ^a   Gascón, José A ^a,b   McEvoy, James P ^a,c   Brudvig, Gary W ^a   Batista, Victor S ^a  

^a YALE UNIVERSITY   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

^c REGIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CATALYSIS; MOLECULAR MECHANICS; PROTEINS; SOLAR CELLS; SOLAR ENERGY; X RAY DIFFRACTION;

CATALYTIC CYCLE; OXYGEN-EVOLVING COMPLEX (OEC); PHOTOSYSTEM; WATER SPLITTING;

QUANTUM THEORY;

CALCIUM; MANGANESE; OXYGEN; WATER;

ARTICLE; BIOFUEL PRODUCTION; CATALYSIS; ENGINEERING; MOLECULAR MECHANICS; MOLECULAR MODEL; OXIDATION; PHOTOSYNTHESIS; PHOTOSYSTEM II; PROTON TRANSPORT; QUANTUM MECHANICS; SOLAR ENERGY; SPECTROSCOPY; X RAY DIFFRACTION;

CALCIUM; CATALYSIS; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; CYANOBACTERIA; MANGANESE; MODELS, CHEMICAL; MODELS, MOLECULAR; OXYGEN; PHOTOSYSTEM II PROTEIN COMPLEX; QUANTUM THEORY; WATER;

EID: 41449116568     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja076130q     Document Type: Article

References (123)

1. Diner, B. A.; Babcock, G. T. Oxygenic Photosynthesis; The Light Reactions; Kluwer Academic Publishers: Dordrecht, The Netherlands, 1996.
2. Debus, R. J. Biochim. Biophys. Acta 1992, 1102, 269-352.
3. Witt, H. T. Ber. Bunsen-Ges. Phys. Chem. 1996, 100, 1923-1942.
4. Britt, R. D. Oxygenic Photosynthesis: The Light Reactions; Kluwer Academic Publishers: Dordrecht, The Netherlands, 1996.
5. McEvoy, J. P.; Brudvig, G. W. Chem. Rev. 2006, 106, 4455-4483.
6. Joliot, P.; Barbieri, G.; Chabaud, R. Photochem. Photobiol. 1969, 10, 309-329.
7. Kok, B.; Forbush, B.; McGloin, M. Photochem. Photobiol. 1970, 11, 457-475.
8. McEvoy, J. P.; Gascón, J. A.; Sproviero, E. M.; Batista, V. S.; Brudvig, G. W. Photosynthesis; Fundamental Aspects to Global Perspectives; Allen Press, Inc.: Lawrence, KS, 2005; Vol. 1.
9. Sproviero, E. M.; McEvoy, J. P.; Gascón, J. A.; Brudvig, G. W.; Batista, V. S. J. Chem. Theory Comput. 2006, 4, 1119-1134.
10. Sproviero, E. M.; Gascón, J. A.; McEvoy, J.; Brudvig, G. W.; Batista, V. S. Curr. Opin. Struct. Biol. 2007, 17, 173-180.
11. McEvoy, J. P.; Gascón, J. A.; Batista, V. S.; Brudvig, G. W. Photochem. Photobiol. 2005, 4, 940-949.
12. Sproviero, E. M.; Shinopolous, K.; Gascón, J. A.; McEvoy, J.; Brudvig, G. W.; Batista, V. S. Phil Trans. R. Soc. London, Ser. B 2008, 363, 1149-1156.
13. Debus, R. J.; Barry, B. A.; Sithole, I.; Babcock, G. T.; McIntosh, L. Biochemistry 1988, 27, 9071-9074.
14. Metz, J. G.; Nixon, P. J.; Rogner, M.; Brudvig, G. W.; Diner, B. A. Biochemistry 1989, 28, 6960-6969.
15. Ferreira, K. N.; Iverson, T. M.; Maghlaoui, K.; Barber, J.; Iwata, S. Science 2004, 303, 1831-1838.
16. Dau, H.; Liebisch, P.; Haumann, M. Phys. Chem. Chem. Phys. 2004, 6, 4781-4792.
17. Haumann, M.; Muller, C.; Liebisch, P.; Iuzzolino, L.; Dittmer, J.; Grabolle, M.; Neisius, T.; Meyer-Klaucke, W.; Dau, H. Biochemistry 2005, 4, 1894-1908.
18. Dau H., private communication.
19. Yano, J.; Pushkar, Y.; Glatzel, P.; Lewis, A.; Sauer, K.; Messinger, J.; Bergmann, U.; Yachandra, V. J. Am. Chem. Soc. 2005, 127, 14974-14975.
20. Messinger, J. Phys. Chem. Chem. Phys. 2004, 6, 4764-4771.
21. Vrettos, J. S.; Limburg, J.; Brudvig, G. W. Biochim. Biophys. Acta 2001, 1503, 229-245.
22. McEvoy, J. P.; Brudvig, G. W. Phys. Chem. Chem. Phys. 2004, 6, 4754-4763.
23. Robblee, J. H.; Cinco, R. M.; Yachandra, V. K. Biochim. Biophys. Acta 2001, 1503, 7-23.
24. Pecoraro, V. L.; Baldwin, M. J.; Caudle, M. T.; Hsieh, W. Y.; Law, N. A. Pure Appl. Chem. 1998, 70, 925-929.
25. Barber, J.; Ferreira, K. N.; Maghlaoui, K.; Iwata, S. Phys. Chem. Chem. Phys. 2004, 6, 4737-4742.
26. Britt, R. D.; Campbell, K. A.; Peloquin, J. M.; Gilchrist, M. L.; Aznar, C. P.; Dicus, M. M.; Robblee, J.; Messinger, J. Biochim. Biophys. Acta 2004, 1655, 158-171.
27. Lundberg, M.; Siegbahn, P. E. M. Phys. Chem. Chem. Phys. 2004, 6, 4772-4780.
28. Siegbahn, P. E. M.; Lundberg, M. Photochem. Photobiol. 2005, 4, 1035-1043.
29. Biesiadka, J.; Loll, B.; Kern, J.; Irrgang, K. D.; Zouni, A. Phys. Chem. Chem. Phys. 2004, 6, 4733-4736.
30. Loll, B.; Kern, J.; Saenger, W.; Zouni, A.; Biesiadka, J. Nature 2005, 438, 1040-1044.
31. Yano, J.; Kern, J.; Irrgang, K.; Latimer, M. J.; Bergmann, U.; Glatzel, P.; Pushkar, Y.; Biesiadka, J.; Loll, B.; Sauer, K.; Messinger, J.; Zouni, A.; Yachandra, V. K. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 12047-12052.
32. Lavergne, J.; Junge, W. Photosynth. Res. 1993, 38, 279-296.
33. Noodleman, L. J. Chem. Phys. 1981, 74, 5737-5743.
34. Noodleman, L.; Davidson, E. R. Chem. Phys. 1981, 109, 131-143.
35. Dapprich, S.; Komaromi, K.; Byun, K.; Morokuma, K.; Frisch, M. J. Mol. Str. (THEOCHEM) 1999, 461, 1-21.
36. Frisch, M. J. et al. Gaussian 03, revision A1; Gaussian, Inc.: Pittsburgh, PA, 2003.
37. Gascón, J. A.; Batista, V. S. Biophys. J. 2004, 87, 2931-2941.
38. Gascón, J. A.; Sproviero, E. M.; Batista, V. S. J. Chem. Theory Comput. 2005, 1, 674-685.
39. Gascón, J. A.; Leung, S. S. F.; Batista, E. R.; Batista, V. S. J. Chem. Theory Comput. 2006, 2, 175-186.
40. Gascón, J. A.; Sproviero, E. M.; Batista, V. S. Acc. Chem. Res. 2005, 39, 184-193.
41. Vacek, G.; Perry, J. K.; Langlois, J. M. Chem. Phys. Lett. 1999, 310, 189-194.
42. Jaguar 5.5; Schroedinger, LLC: Portland, OR, 1991-2003.
43. Note that all amino acid residues are from the D1 protein subunit, unless otherwise indicated.
44. Cornell, W. D.; Cieplak, P.; Bayly, C. I.; Gould, I. R.; Merz, K. M.; Ferguson, D. M.; Spellmeyer, D. C.; Fox, T.; Caldwell, J. W.; Kollman, P. A. J. Am. Chem. Soc. 1995, 117, 5179-5197.
45. Sproviero, E. M.; Gascón, J. A.; McEvoy, J. P.; Brudvig, G. W.; Batista, V. S. J. Inorg. Biochem. 2005, 100, 786-800.
46. Noodleman, L. J. Chem. Phys. 1981, 74, 5737-5743.
47. Noodleman, L.; Davidson, E. R. Chem. Phys. 1986, 109, 131-143.
48. Noodleman, L.; Case, D. A. Adv. Inorg. Chem. 1992, 38, 423-470.
49. Noodleman, L.; Peng, C. Y.; Case, D. A.; Mouesca, J. M. Coord. Chem. Rev. 1995, 144, 199-244.
50. Gonis, A. Green Functions for Ordered and Disordered Systems; North Holland: Amsterdam, 1992.
51. Ankudinov, A. L.; Bouldin, C.; Rehr, J. J.; Sims, J.; Hung, H. Phys. Rev. B: Condens. Matter Mater. Phys. 2002, 65, 104107-104118.
52. Dau, H.; Liebisch, P.; Haumann, M. Anal. Bioanal. Chem. 2003, 376, 562-583.
53. Kronig, R. Z. Phys. 1931, 70, 317-323.
54. Kronig, R. Z. Phys. 1932, 75, 190-210.
55. Sayers, D. E.; Stern, E. A.; Lytle, F. W. Phys. Rev. Lett. 1971, 27, 1204-1207.
56. Stern, E. Phys. Rev. B: Condens. Matter Mater. Phys. 1974, 10, 3027-3027.
57. Pendry, J. Low Energy Electron Diffraction; Academic Press: New York, 1974.
58. Lee, P.; Pendry, J. Phys. Rev. B: Condens. Matter Mater. Phys. 1975, 11, 2795-2811.
59. Ashley, C.; Doniach, S. Phys. Rev. B: Condens. Matter Mater. Phys. 1975, 11, 1279-1288.
60. Dau, H.; Iuzzolino, L.; Dittmer, J. Biochim. Biophys. Acta 2001, 1503, 24-39.
61. Ono, T. A.; Noguchi, T.; Inoue, Y.; Kusunoki, M.; Matsushita, T.; Oyanagi, H. Science 1992, 258, 1335-1337.
62. Yachandra, V. K.; DeRose, V. J.; Latimer, M. J.; Mukerji, L.; Sauer, K.; Klein, M. P. Science 1993, 260, 675-679.
63. Roelofs, T. A.; Liang, W. C.; Latimer, M. J.; Cinco, R. M.; Rompel, A.; Andrews, J. C.; Sauer, K.; Yachandra, V. K.; Klein, M. P. Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 3335-3340.
64. Bergmann, U.; Grush, M. M.; Horne, C. R.; DeMarois, P.; Penner-Hahn, J. E.; Yocum, C. F.; Wright, D. W.; Dube, C. E.; Armstrong, W. H.; Christou, G.; Eppley, H. J.; Cramer, S. P. J. Phys. Chem. B 1998, 102, 8350-8352.
65. Iuzzolino, L.; Dittmer, J.; Dau, H. Biochemistry 1998, 37, 17112-17119.
66. Messinger, J.; Robblee, J. H.; Bergmann, U.; Fernandez, C.; Glatzel, P.; Visser, H.; Cinco, R. M.; McFarlane, K. L.; Bellacchio, E.; Pizarro, S. A.; Cramer, S. P.; Sauer, K.; Klein, M. P.; Yachandra, V. K. J. Am. Chem. Soc. 2001, 123, 7804-7820.
67. Zheng, M.; Dismukes, G. C. Inorg. Chem. 1996, 35, 3307-3319.
68. Kuzek, D.; Pace, R. J. Biochim. Biophys. Acta 2001, 1503, 123-137.
69. Force, D. A.; Randall, D. W.; Britt, R. D. Biochemistry 1997, 36, 12062-12070.
70. Haumann, M.; Barra, M.; Loja, P.; Löscher, S.; Krivanek, R.; Grundmeier, A.; Dau, L. E. A. H. Biochemistry 2006, 45, 13101-13107.
71. Yano, J.; Kern, J.; Sauer, K.; Latimer, M. J.; Pushkar, Y.; Biesiadka, J.; Loll, B.; Saenger, W.; Messinger, J.; Zouni, A.; Yachandra, V. K. Science 2006, 314, 821-225.
72. Debus, R. J.; Strickler, M. A.; Walker, L. M.; Hillier, W. Biochemistry 2005, 44, 1367-1374.
73. Chu, H.; Debus, R. J.; Babcock, G. T. Biochemistry 2001, 40, 2312-2316.
74. Strickler, M. A.; Hillier, W.; Debus, R. J. Biochemistry 2006, 45, 8801-8811.
75. Strickler, M. A.; Walker, L. M.; Hillier, W.; Britt, D.; Debus, R. J. Biochemistry 2007, 46, 3151-3160.
76. Kimura, Y.; Mizusawa, N.; Yamanari, T.; Ishii, A.; Ono, T. J. Biol. Chem. 2005, 280, 2078-2083.
77. McGrady, J. E.; Stranger, R. J. Am. Chem. Soc. 1997, 119, 8512-8522.
78. Zhao, X. G.; Richardson, W. H.; Chen, J. L.; Li, J.; Noodleman, L.; Tsai, H. L.; Hendrickson, D. N. Inorg. Chem. 1997, 36, 1198-1217.
79. Delfs, C. D.; Stranger, R. Inorg. Chem. 2001, 40, 3061-3076.
80. Barone, V.; Bencini, A.; Gatteschi, D.; Totti, F. Chem. - Eur. J. 2002, 8, 5019-5027.
81. Glatzel, P.; Bergmann, U.; Yano, J.; Visser, H.; Robblee, J. H.; Gu, W.; Groot, F. D.; Christou, G.; Pecoraro, V. L.; Cramer, S. P.; Yachandra, V. K. J. Am. Chem. Soc. 2004, 126, 9946-9959.
82. Law, N. A.; Hillier, W.; Chu, H.; Hsieh, W.; Haymond, S.; Cerda, J.; Pecoraro, V.; Babcock, G. J. Inorg. Biochem. 2001, 86, 310-320.
83. Kretschmann, H.; Witt, H. T. Biochim. Biophys. Acta 1993, 1144, 331-345.
84. Kretschmann, H.; Schlodder, E.; Witt, H. T. Biochim. Biophys. Acta 1996, 1274, 1-8.
85. Haumann, M.; Boesershausen, O.; Junge, W. FEBS Lett. 1994, 355, 101-105.
86. Pospisil, P.; Haumann, M.; Dittmer, J.; Sole, V. A.; Dau, H. Biophys. J. 2003, 84, 1370-1386.
87. Dau, H.; Liebisch, P.; Haumann, M. Anal. Bioanal. Chem. 2003, 376, 562-583.
88. Robblee, J. H.; Messinger, J.; Cinco, R. M.; McFarlane, K. L.; Fernandez, C.; Pizarro, S. A.; Sauer, K.; Yachandra, V. K. J. Am. Chem. Soc. 2002, 124, 7459-7471.
89. Fowler, C. F. Biochim. Biophys. Acta 1977, 462, 414-421.
90. Wille, B.; Lavergne, J. Photobiochem. Photobiophys. 1982, 4, 131-144.
91. Saphon, S.; Crofts, A. R. Z. Naturforsch 1977, 32C, 617-626.
92. Rappaport, F.; Blanchard-Desce, M.; Lavergne, J. Biochim. Biophys. Acta 1994, 1184, 178-192.
93. Junge, W.; Haumann, M.; Ahbrink, R.; Mulkidjanian, A.; Clausen, J. Philos. Trans. R. Soc. London, Ser. B 2002, 357, 1407-1418.
94. Schlodder, E.; Witt, H. T. J. Biol. Chem. 1999, 274, 30877-30392.
95. Haumann, M.; Junge, W. Oxygenic Photosynthesis: The Light Reactions; Kluwer Academic Publishers: Dordrecht, The Netherlands, 1996.
96. Haumann, M.; Bögershausen, O.; Cherepanov, D.; Ahlbrink, R.; Junge, W. Photosynth. Res. 1997, 51, 193-208.
97. Liang, W. C.; Roelofs, T. A.; Cinco, R. M.; Rompel, A.; Latimer, M. J.; Yu, W. O.; Sauer, K.; Klein, M. P.; Yachandra, V. K. J. Am. Chem. Soc. 2000, 122, 3399-3412.
98. Haumann, M.; Junge, W. Biochemistry 1994, 33, 864-872.
99. Haumann, M.; Liebisch, P.; Muller, C.; Barra, M.; Grabolle, M.; Dau, H. Science 2005, 310, 1019-1021.
100. Lundberg, M.; Blomberg, M. R. A.; Siegbahn, P. E. M. Inorg. Chem. 2004, 43, 264-274.
101. Sauer, K.; Yachandra, V. K. Biochim. Biophys. Acta 2004, 1655, 140-148.
102. Knoepfle, N.; Bricker, T. M.; Putnam-Evans, C. Biochemistry 1999, 38, 1582-1588.
103. Puustinen, A.; Wikstrom, M. Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 35-37.
104. Qian, J.; Mills, D. A.; Geren, L.; Wang, K.; Hoganson, C. W.; Schmidt, B.; Hiser, C.; Babcock, G. T.; Durham, B.; Millett, F.; Ferguson-Miller, S. Biochemistry 2004, 43, 5748-5756.
105. Roffey, R. A.; Kramer, D. M.; Govindjee,; Sayre, R. T. Biochim. Biophys. Acta 1994, 1185, 257-270.
106. Hays, A. M. A.; Vassiliev, I. R.; Golbeck, J. H.; Debus, R. J. Biochemistry 1998, 37, 11352-11365.
107. Hays, A. M. A.; Vassiliev, I. R.; Golbeck, J. H.; Debus, R. J. Biochemistry 1998, 38, 11851-11865.
108. Ishikita, H.; Saenger, W.; Loll, B.; Biesiadka, J.; Knapp, E. W. Biochemistry 2006, 45, 2063-2071.
109. Hoganson, C. W.; Lydakis-Simantiris, N.; Tang, X. S.; Tommos, C.; Warncke, K.; Babcock, G. T.; Diner, B. A.; McCracken, J.; Styring, S. Photosynth. Res. 1995, 46, 177-184.
110. Hoganson, C. W.; Babcock, G. T. Science 1997, 277, 1953-1956.
111. Szalai, V. A.; Brudvig, G. W. Biochemistry 1996, 35, 15080-1507.
112. Wincencjusz, H.; van Gorkom, H. J.; Yocum, C. F. Biochemistry 1997, 36, 3663-3670.
113. Kühne, H.; Szalai, V. A.; Brudvig, G. W. Biochemistry 1999, 38, 6604-6613.
114. Brettel, K.; Schlodder, E.; Witt, H. T. Biochim. Biophys. Acta 1984, 766, 403-415.
115. Renger, G.; Christen, G.; Karge, M.; Eckert, H. J.; Irrgang, K. D. J. Biol. Inorg. Chem. 1998, 3, 360-366.
116. Jeans, C.; Schilstra, M. J.; Klug, D. R. Biochemistry 2002, 41, 5015-5023.
117. Bacon, K. In Photosynthesis-Photobiochemistry and Photobiophysics; Kluwer Academic Publishers: Dordretcht, The Netherlands, 2001.
118. Siegbahn, P. E. M. Chem. - Eur. J. 2006, 12, 9217-9227.
119. Siegbahn, P. E. M.; Crabtree, R. H. J. Am. Chem. Soc. 1999, 121, 117-127.
120. Siegbahn, P. E. M. Curr. Opin. Chem. Biol. 2002, 6, 227-235.
121. Yachandra, V. K. Philos. Trans. R. Soc. London, Ser. B2002, 357, 1347-1357.
122. Brudvig, G. W.; Crabtree, R. H. Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 4586-4588.
123. Yachandra, V. K.; Sauer, K.; Klein, M. P. Chem. Rev. 1996, 96, 2927-2950.