A metalloradical mechanism for the generation of oxygen from water in photosynthesis

Science

Volumn 277, Issue 5334, 1997, Pages 1953-1956

  Hoganson, Curtis W ^a   Babcock, Gerald T ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OXYGEN; WATER;

ARTICLE; ENZYME MECHANISM; NONHUMAN; OXIDATION; OXYGEN SUPPLY; PHOTOSYNTHESIS; PHOTOSYSTEM II; PHYTOCHEMISTRY; PRIORITY JOURNAL; PROTON TRANSPORT;

ALGAE; ELECTRONS; HYDROGEN; KINETICS; LIGANDS; MANGANESE; MODELS, CHEMICAL; OXIDATION-REDUCTION; OXYGEN; PHOTOSYNTHESIS; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PHOTOSYSTEM II PROTEIN COMPLEX; PLANTS; TYROSINE; WATER;

EID: 0030854151     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.277.5334.1953     Document Type: Article

References (86)

1. B. A. Diner and G. T. Babcock, in Oxygenic Photosynthesis: The Light Reactions, D. R. Ort and C. F. Yocum, Eds. (Kluwer, Dordrecht, Netherlands, 1996), pp. 213-247.
2. R. J. Debus, Biochim. Biophys. Acta 1102, 269 (1992); H. T. Witt, Ber. Bunsenges. Phys. Chem. 100, 1923 (1996).
3. R. J. Debus, Biochim. Biophys. Acta 1102, 269 (1992); H. T. Witt, Ber. Bunsenges. Phys. Chem. 100, 1923 (1996).
4. R. D. Britt, in Oxygenic Photosynthesis: The Light Reactions, D. R. Ort and C. F. Yocum, Eds. (Kluwer, Dordrecht, Netherlands, 1996), pp. 137-164.
5. V. K. Yachandra, K. Sauer, M. P. Klein, Chem. Rev. 96, 2927 (1996).
6. B. Kok, B. Forbush, M. McGloin, Photochem. Photobiol. 11, 457 (1970).
7. B. A. Barry and G. T. Babcock, Proc. Natl. Acad. Sci. U.S.A. 84, 7099 (1987); R. J. Debus, B. A. Barry, I. Sithole, G. T. Babcock, L. McIntosh, Biochemistry 27, 9071 (1988).
8. B. A. Barry and G. T. Babcock, Proc. Natl. Acad. Sci. U.S.A. 84, 7099 (1987); R. J. Debus, B. A. Barry, I. Sithole, G. T. Babcock, L. McIntosh, Biochemistry 27, 9071 (1988).
9. A. Chu, A. P. Nguyen, R. J. Debus, Biochemistry 34, 5839 (1995).
10. C. Tommos et al., J. Am. Chem. Soc. 117, 10325 (1995); G. T. Babcock et al., Acta Chem. Scand. 51, 533 (1997).
11. C. Tommos et al., J. Am. Chem. Soc. 117, 10325 (1995); G. T. Babcock et al., Acta Chem. Scand. 51, 533 (1997).
12. M. L. Gilchrist Jr., J. A. Ball, D. W. Randall, R. D. Britt, Proc. Natl. Acad. Sci. U.S.A. 92, 9545 (1995); X.-S. Tang, D. W. Randall, D. A. Force, B. A. Diner, R. D. Britt, J. Am. Chem. Soc. 118, 7638 (1996).
13. M. L. Gilchrist Jr., J. A. Ball, D. W. Randall, R. D. Britt, Proc. Natl. Acad. Sci. U.S.A. 92, 9545 (1995); X.-S. Tang, D. W. Randall, D. A. Force, B. A. Diner, R. D. Britt, J. Am. Chem. Soc. 118, 7638 (1996).
14. V. K. Yachandra, et al., Science 260, 675 (1993).
15. H. Dau et al., Biochemistry 34, 5274 (1995).
16. M. Haumann and W. Junge, Biochemistry 33, 864 (1994).
17. _, in Oxygenic Photosynthesis: The Light Reactions, D. R. Ort and C. F. Yocum, Eds. (Kluwer, Dordrecht, Netherlands, 1996), pp. 165-192.
18. C. W. Hoganson et al., Photosyn. Res. 46, 177 (1995).
19. G. T. Babcock, in Photosynthesis: From Light to Biosphere, P. Mathis, Ed. (Kluwer, Dordrecht, Netherlands, 1995), vol. 2, pp. 209-215.
20. _, et al., Biochemistry 28, 9557 (1989).
21. G. W. Brudvig and R. H. Crabtree, Proc. Natl. Acad. Sci. U.S.A. 83, 4586 (1986); J. B. Vincent and G. Christou, Inorg. Chim. Acta 136, L41 (1987); V. L. Pecoraro, in Manganese Redox Enzymes, V. L. Pecoraro, Ed. (VCH, New York, 1992), pp. 197-231.
22. G. W. Brudvig and R. H. Crabtree, Proc. Natl. Acad. Sci. U.S.A. 83, 4586 (1986); J. B. Vincent and G. Christou, Inorg. Chim. Acta 136, L41 (1987); V. L. Pecoraro, in Manganese Redox Enzymes, V. L. Pecoraro, Ed. (VCH, New York, 1992), pp. 197-231.
23. G. W. Brudvig and R. H. Crabtree, Proc. Natl. Acad. Sci. U.S.A. 83, 4586 (1986); J. B. Vincent and G. Christou, Inorg. Chim. Acta 136, L41 (1987); V. L. Pecoraro, in Manganese Redox Enzymes, V. L. Pecoraro, Ed. (VCH, New York, 1992), pp. 197-231.
24. J. A. Gilbert et al., J. Am. Chem. Soc. 107, 3855 (1985); F. P. Rotzinger et al., ibid. 109, 6619 (1987); Y. Naruta, M. Sasayama, T. Sasaki, Angew. Chem. Int. Ed. 33, 1839 (1994).
25. J. A. Gilbert et al., J. Am. Chem. Soc. 107, 3855 (1985); F. P. Rotzinger et al., ibid. 109, 6619 (1987); Y. Naruta, M. Sasayama, T. Sasaki, Angew. Chem. Int. Ed. 33, 1839 (1994).
26. J. A. Gilbert et al., J. Am. Chem. Soc. 107, 3855 (1985); F. P. Rotzinger et al., ibid. 109, 6619 (1987); Y. Naruta, M. Sasayama, T. Sasaki, Angew. Chem. Int. Ed. 33, 1839 (1994).
27. J. Messinger, M. Badger, T. Wydrzynski, Proc. Natl. Acad. Sci. U.S.A. 92, 3209 (1995); J. Messinger, M. Hillier, M. Badger, T. Wydrzynski, in Photosynthesis: From Light to Biosphere, P. Mathis, Ed. (Kluwer, Dordrecht, Netherlands, 1995), vol. 2, pp. 283-286.
28. J. Messinger, M. Badger, T. Wydrzynski, Proc. Natl. Acad. Sci. U.S.A. 92, 3209 (1995); J. Messinger, M. Hillier, M. Badger, T. Wydrzynski, in Photosynthesis: From Light to Biosphere, P. Mathis, Ed. (Kluwer, Dordrecht, Netherlands, 1995), vol. 2, pp. 283-286.
29. 2 in superoxidized manganese catalase has been suggested as the basis for inactivity of this oxidation state; G. S. Waldo, S. Yu, J. E. Penner-Hahn, J. Am. Chem. Soc. 114, 5869 (1992); S. Khangulov, M. Sivaraja, V. V. Barynin, G. C. Dismukes, Biochemistry 32, 4912 (1993); M. Shank, V. Barynin, G. C. Dismukes, ibid. 33, 15433 (1994).
30. 2 in superoxidized manganese catalase has been suggested as the basis for inactivity of this oxidation state; G. S. Waldo, S. Yu, J. E. Penner-Hahn, J. Am. Chem. Soc. 114, 5869 (1992); S. Khangulov, M. Sivaraja, V. V. Barynin, G. C. Dismukes, Biochemistry 32, 4912 (1993); M. Shank, V. Barynin, G. C. Dismukes, ibid. 33, 15433 (1994).
31. 2 in superoxidized manganese catalase has been suggested as the basis for inactivity of this oxidation state; G. S. Waldo, S. Yu, J. E. Penner-Hahn, J. Am. Chem. Soc. 114, 5869 (1992); S. Khangulov, M. Sivaraja, V. V. Barynin, G. C. Dismukes, Biochemistry 32, 4912 (1993); M. Shank, V. Barynin, G. C. Dismukes, ibid. 33, 15433 (1994).
32. J. Lind, X. Shen, T. E. Eriksen, G. Merenyi, J. Am. Chem. Soc. 112, 479 (1990); J. A. Kerr, in Handbook of Chemistry and Physics (Chemical Rubber, Cleveland, OH, ed. 77, 1996), pp. 9-51.
33. J. Lind, X. Shen, T. E. Eriksen, G. Merenyi, J. Am. Chem. Soc. 112, 479 (1990); J. A. Kerr, in Handbook of Chemistry and Physics (Chemical Rubber, Cleveland, OH, ed. 77, 1996), pp. 9-51.
34. K. A. Gardner and J. M. Mayer, Science 269, 1849 (1995).
35. M. Baldwin and V. L. Pecoraro, J. Am. Chem. Soc. 118, 11325 (1996).
36. M. T. Caudle and V. L. Pecoraro, ibid. 119, 3415 (1997).
37. M. R. A. Blomberg et al., ibid., in press.
38. C. K. Ingold, Structure and Mechanism in Organic Chemistry (Cornell Univ. Press, Ithaca, NY, ed. 2, 1969), pp. 457-463 and 681-686; A. Pross, Theoretical and Physical Principles of Organic Reactivity (Wiley, New York, 1995).
39. C. K. Ingold, Structure and Mechanism in Organic Chemistry (Cornell Univ. Press, Ithaca, NY, ed. 2, 1969), pp. 457-463 and 681-686; A. Pross, Theoretical and Physical Principles of Organic Reactivity (Wiley, New York, 1995).
40. H. Koike, B. Hanssum, Y. Inoue, G. Renger, Biochim. Biophys. Acta 893, 524 (1987); G. Renger and B. Hanssum, FEBS Lett. 299, 28 (1992).
41. H. Koike, B. Hanssum, Y. Inoue, G. Renger, Biochim. Biophys. Acta 893, 524 (1987); G. Renger and B. Hanssum, FEBS Lett. 299, 28 (1992).
42. N. Lydakis-Simantiris, C. W. Hoganson, D. F. Ghanotakis, G. T. Babcock, in Photosynthesis: From Light to Biosphere, P. Mathis, Ed. (Kluwer, Dordrecht, Netherlands, 1995), vol. 2, pp. 279-282; N. Lydakis-Simantiris, D. F. Ghanotakis, G. T. Babcock, Biochim. Biophys. Acta, in press.
43. N. Lydakis-Simantiris, C. W. Hoganson, D. F. Ghanotakis, G. T. Babcock, in Photosynthesis: From Light to Biosphere, P. Mathis, Ed. (Kluwer, Dordrecht, Netherlands, 1995), vol. 2, pp. 279-282; N. Lydakis-Simantiris, D. F. Ghanotakis, G. T. Babcock, Biochim. Biophys. Acta, in press.
44. O. Bögershausen, M. Haumann, W. Junge, Ber. Bunsenges. Phys. Chem. 100, 1987 (1996); M. Karge, K.-D. Irrgang, G. Renger, Biochemistry 36, 8904 (1997).
45. O. Bögershausen, M. Haumann, W. Junge, Ber. Bunsenges. Phys. Chem. 100, 1987 (1996); M. Karge, K.-D. Irrgang, G. Renger, Biochemistry 36, 8904 (1997).
46. M. Karge et al., FEBS Lett. 378, 140 (1996).
47. C. Tommos and G. T. Babcock, Acct. Chem. Res., in press.
48. J. P. Dekker, H. J. Van Gorkom, J. Wensink, L. Ouwehand, Biochim. Biophys. Acta 767, 1 (1984); J. Lavergne, ibid. 1060, 175 (1991); M. Haumann, W. Drevenstedt, M. Hundelt, W. Junge, ibid. 1273, 237 (1996); H. Kretschmann, E. Schlodder, H. T. Witt, ibid. 1274, 1 (1996).
49. J. P. Dekker, H. J. Van Gorkom, J. Wensink, L. Ouwehand, Biochim. Biophys. Acta 767, 1 (1984); J. Lavergne, ibid. 1060, 175 (1991); M. Haumann, W. Drevenstedt, M. Hundelt, W. Junge, ibid. 1273, 237 (1996); H. Kretschmann, E. Schlodder, H. T. Witt, ibid. 1274, 1 (1996).
50. J. P. Dekker, H. J. Van Gorkom, J. Wensink, L. Ouwehand, Biochim. Biophys. Acta 767, 1 (1984); J. Lavergne, ibid. 1060, 175 (1991); M. Haumann, W. Drevenstedt, M. Hundelt, W. Junge, ibid. 1273, 237 (1996); H. Kretschmann, E. Schlodder, H. T. Witt, ibid. 1274, 1 (1996).
51. J. P. Dekker, H. J. Van Gorkom, J. Wensink, L. Ouwehand, Biochim. Biophys. Acta 767, 1 (1984); J. Lavergne, ibid. 1060, 175 (1991); M. Haumann, W. Drevenstedt, M. Hundelt, W. Junge, ibid. 1273, 237 (1996); H. Kretschmann, E. Schlodder, H. T. Witt, ibid. 1274, 1 (1996).
52. G. C. Dismukes and Y. Siderer, Proc. Natl. Acad. Sci. U.S.A. 78, 274 (1981); A. Haddy, W. R. Dunham, R. H. Sands, R. Aasa, Biochim. Biophys. Acta 1099, 25 (1992).
53. G. C. Dismukes and Y. Siderer, Proc. Natl. Acad. Sci. U.S.A. 78, 274 (1981); A. Haddy, W. R. Dunham, R. H. Sands, R. Aasa, Biochim. Biophys. Acta 1099, 25 (1992).
54. T. Ono et al., Science 258, 1335 (1992).
55. P. J. Riggs, C. F. Yocum, J. E. Penner-Hahn, R. Mei, J. Am. Chem. Soc. 114, 10650 (1992).
56. T. A. Roelofs et al., Proc. Natl. Acad. Sci. U.S.A. 93, 3335 (1996).
57. 3.
58. P. J. Riggs-Gelasco, R. Mei, C. F. Yocum, J. E. Penner-Hahn, J. Am. Chem. Soc. 118, 2387 (1996); see also, J. Messinger, J. H. A. Nugent, M. C. W. Evans, Biochemistry, in press.
59. P. J. Riggs-Gelasco, R. Mei, C. F. Yocum, J. E. Penner-Hahn, J. Am. Chem. Soc. 118, 2387 (1996); see also, J. Messinger, J. H. A. Nugent, M. C. W. Evans, Biochemistry, in press.
60. J.-J. Girerd, in Photosynthesis: From Light to Biosphere, P. Mathis, Ed. (Kluwer, Dordrecht, Netherlands, 1995), vol. 2, pp. 217-222.
61. I. Vass and S. Styring, Biochemistry 30, 830 (1991).
62. X.-S. Tang et al., Proc. Natl. Acad. Sci. U.S.A. 91, 704 (1994).
63. K. Lindberg, T. Vänngård, L.-E. Andréasson, Photosyn. Res. 38, 401 (1993).
64. K. W. Kramarz and J. R. Norton, Prog. Inorg. Chem. 42, 1 (1994).
65. V. L. Pecoraro, Photochem. Photobiol. 48, 249 (1988).
66. D. W. Randall et al., J. Am. Chem. Soc. 117, 11780 (1995).
67. F. A. Cotton and G. Wilkinson, Advanced Inorganic Chemistry (Wiley, New York, ed. 5, 1988), p. 707; N. N. Greenwood and A. Earnshaw, Chemistry of the Elements (Pergamon, Oxford, 1984), p. 1228; R. Manchandra, G. W. Brudvig, R. H. Crabtree, Coord. Chem. Rev. 144, 1 (1995).
68. F. A. Cotton and G. Wilkinson, Advanced Inorganic Chemistry (Wiley, New York, ed. 5, 1988), p. 707; N. N. Greenwood and A. Earnshaw, Chemistry of the Elements (Pergamon, Oxford, 1984), p. 1228; R. Manchandra, G. W. Brudvig, R. H. Crabtree, Coord. Chem. Rev. 144, 1 (1995).
69. F. A. Cotton and G. Wilkinson, Advanced Inorganic Chemistry (Wiley, New York, ed. 5, 1988), p. 707; N. N. Greenwood and A. Earnshaw, Chemistry of the Elements (Pergamon, Oxford, 1984), p. 1228; R. Manchandra, G. W. Brudvig, R. H. Crabtree, Coord. Chem. Rev. 144, 1 (1995).
70. T. J. Collins, R. D. Powell, C. Slebodnick, E. S. Uffelman, J. Am. Chem. Soc. 112, 899 (1990); M. K. Stern and J. T. Groves, in Manganese Redox Enzymes, V. L. Pecoraro, Ed. (VCH, New York, 1992), pp. 233-259.
71. T. J. Collins, R. D. Powell, C. Slebodnick, E. S. Uffelman, J. Am. Chem. Soc. 112, 899 (1990); M. K. Stern and J. T. Groves, in Manganese Redox Enzymes, V. L. Pecoraro, Ed. (VCH, New York, 1992), pp. 233-259.
72. D. T. Sawyer, Oxygen Chemistry, (Oxford Univ. Press, New York, 1991).
73. A. Chu, A. P. Nguyen, R. J. Debus, Biochemistry 34, 5859 (1995).
74. C. W. Hoganson and G. T. Babcock, in Metal Ions in Biological Systems, vol. 30, Metalloenzymes Involving Amino Acid-Residue and Related Radicals, H. Sigel and A. Sigel, Eds., (Dekker, New York, 1994), pp. 77-107.
75. W. H. Saunders Jr. and A. F. Cockerill, Mechanisms of Elimination Reactions (Wiley, New York, 1973).
76. G. T. Babcock, R. E. Blankenship, K. Sauer, FEBS Lett. 61, 286 (1976); M. R. Razeghifarad, C. Klughammer, R. J. Pace, Biochemistry 36, 86 (1997).
77. G. T. Babcock, R. E. Blankenship, K. Sauer, FEBS Lett. 61, 286 (1976); M. R. Razeghifarad, C. Klughammer, R. J. Pace, Biochemistry 36, 86 (1997).
78. A. Boussac, P. Sétif, A. W. Rutherford, Biochemistry 31, 1224 (1992).
79. L. I. Krishtalik, Bioelectrochem. Bioenerg. 23, 249 (1990).
80. G. Tian, J. A. Berry, J. P. Klinman, Biochemistry 33, 226 (1994); J. P. Klinman, Chem. Rev. 96, 2541 (1996).
81. G. Tian, J. A. Berry, J. P. Klinman, Biochemistry 33, 226 (1994); J. P. Klinman, Chem. Rev. 96, 2541 (1996).
82. R. M. Wachter and B. P. Branchaud, J. Am. Chem. Soc. 118, 2782 (1996).
83. C. F. Yocum, Biochim. Biophys. Acta 1059, 1 (1991); H. Wincencjusz, H. J. van Gorkom, C. F. Yocum, Biochemistry 36, 3663 (1997).
84. C. F. Yocum, Biochim. Biophys. Acta 1059, 1 (1991); H. Wincencjusz, H. J. van Gorkom, C. F. Yocum, Biochemistry 36, 3663 (1997).
85. B. E. Sturgeon et al., J. Am. Chem. Soc. 118, 7551 (1996).
86. Supported by NIH grant GM-37300 and the USDA Competitive Grants Office. We thank C. F. Yocum, C. Tommos, K. Warncke, N. Lydakis-Simantiris and M. Gardner for useful discussions.