Mechanism of proton-coupled electron transfer for quinone (Q(B) reduction in reaction centers of Rb. Sphaeroides

Journal of the American Chemical Society

Volumn 118, Issue 38, 1996, Pages 9005-9016

  Graige, M S ^a   Paddock, M L ^a   Bruce, J M ^b   Feher, G ^a   Okamura, M Y ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ELECTRON TRANSPORT; MUTANT; PH; PHOTOSYNTHESIS; PHOTOTROPHIC BACTERIUM;

EID: 0029844155     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja960056m     Document Type: Article

References (90)

1. Cramer, W. A.; Knaff, D. B. In Energy Transduction in Biological Membranes; Springer-Verlag: New York, 1990.
2. Okamura, M. Y.; Feher, G. Annu. Rev. Biochim. 1992, 61, 861-896.
3. General review given by: Parson, W. W. In Photosynthesis: Amesz, J., Ed.; Elsevier: New York, 1987; pp 43-61.
4. Feher, G,; Allen, J. P.; Okamura, M. Y.; Rees, D. C. Nature 1989, 339, 111-116.
5. Verméglio, A.; Clayton, R. K. Biochim. Biophys. Acta 1977, 461, 159-165.
6. Wraight, C. A. Biochim. Biophys. Acta 1979, 548, 309-327.
7. Kleinfeld, D.; Okamura, M. Y.; Feher, G. Biochim. Biophys. Acta 1984, 766, 126-140.
8. Kleinfeld, D.; Okamura, M. Y.; Feher, G. Biochim. Biophys. Acta 1985, 809, 291-310.
9. Maróti, P.; Wraight, C. A. Biochim. Biophys. Acta 1988, 934, 314-328.
10. Maróti, P.; Wraight, C. A. Biochim. Biophys. Acta 1988, 934, 329-347.
11. Maróti, P.; Wraight, C. A. In Current Research in Photosynthesis; Baltscheffsky, M., Ed.: Kluwer: Dordrecht. The Netherlands, 1990; Vol. 1, pp 1.165-1.168.
12. McPherson, P. H.; Okamura, M. Y.: Feher, G. Biochim. Biophys. Acta 1988, 934, 348-368.
13. McPherson, P. H.; Okamura, M. Y.; Feher, G. Biochim. Biophys. Acta 1993, 1144, 309-324.
14. Paddock, M. L.; Rongey, S. H.; Feher, G.; Okamura, M. Y. Proc. Natl. Acad. Sci. U.S.A. 1989, 86, 6602-6606.
15. Paddock, M. L.; Rongey, S. H.: McPherson, P. H.; Juth, A.; Feher, G.; Okamura, M. Y. Biochemistry 1994, 33 (3), 734-745.
16. Takahashi, E.; Wraight, C. A. Biochemistry 1991, 31, 855-866.
17. Paddock, M. L.; McPherson, P. H.; Feher, G.; Okamura, M. Y. Proc. Natl. Acad. Sci. U.S.A. 1990, 87, 6803-6807.
18. Takahashi, E.; Wraight, C. A. Biochim. Biophys. Acta 1992, 1020, 107-111.
19. Takahashi, E.; Wraight, C. A. Biochemistry 1992, 31, 855-866.
20. McPherson, P. H.; Schönfeld, M.: Paddock, M. L.; Okamura, M. Y.; Feher, G. Biochemistry 1994, 33 (5), 1181-1193.
21. Okamura, M. Y.; Feher, G. In Anoxygenic Photosynthetic Bacteria; Blankenship, R. E., Madigan, M. T., Bauer, C. E., Eds. Kluwer Academic Publishers: Dordrecht, The Netherlands, 1995; pp 577-594.
22. Takahashi, E.: Maróti. P.; Wraight, C. A. In Electron and Proton Transfer in Chemistry and Biology, Diemann, E., Junge, W., Muller, Ratajezak, Hs., Eds. Elsevier: Amsterdam, Bielefeld, 1992; pp 219-236.
23. Verméglio, A. Biochim. Biophys. Acta 1977, 459, 516-524.
24. Land, E. J.; Simic, M.; Swallow, A. J. Biochim. Biophys. Acta 1971, 226, 239-240.
25. Hales, B. J.; Case, E. E. Biochim. Biophys. Acta 1981, 637, 291-302.
26. Lubitz, W.; Abresch, E. A.; Debus, R. J.; Isaacson, R. A.; Okamura, M. Y.; Feher, G. Biochim. Biophys. Acta 1985, 808, 464-469.
27. Feher, G.: Isaacson, R. A.; Okamura, M. Y.; Lubitz, W. In Antennas and Reaction Centers of Photosynthetic Bacteria; Michel-Beyerle, M. E., Ed.; Springer-Verlag: Berlin, 1985; pp 174-189.
28. O'Malley, P. J.; Chandrashekar, T. K.; Babcock, G. T. In Antennas and Reaction Centers of Photosynthetic Bacteria; Michel-Beyerle, M. E., Ed.; Springer-Verlag: New York, 1985; pp 339-344.
29. McPherson, P. H.; Okamura, M. Y.; Feher, G. Biochim. Biophys. Acta 1990, 1016, 289-292.
30. (a) Perrin, C. L. J. Phys. Chem. 1984, 88, 3611-3615.
31. (b) Zhao, X. G.; Cukier, R. I. J. Phys. Chem. 1995, 99 (3), 945-954.
32. (c) Cukier, R. I. J. Phys. Chem. 1994, 98, 2377-2381.
33. (a) Savéant, J. M. In Advances in Physical Organic Chemistry; Bethel, D., Ed.; Academic Press: New York, 1990; pp 1-130.
34. (b) Gauduel, Y.; Pommeret, S.; Antonetti, A. J. Phys. Chem. 1993, 97, 134-142.
35. (c) Gauduel, Y.; Pommeret, S.; Migus, A.; Antonetti, A. J. Phys. Chem. 1991, 95, 533-539.
36. Labahn, A.; Bruce, J. M.; Okamura, M. Y.; Feher, G. Chem. Phys. 1995, 197, 355-366.
37. Gunner M. R.; Tiede, D. M.; Prince, R. C., Dutton, P. L. In Functions of Quinones in Energy Conserving Systems; Trumpower, B. L., Ed.; Academic Press: New York, 1982; pp 265-269.
38. Mashraqui, S.; Keehn, P. Synth. Commun. 1982, 12, 637.
39. Paddock, M. L.; Rongey, S. H.; Abresch, E. C.; Feher, G.; Okamura, M. Y. Photosynth. Res. 1988, 17, 75-96.
40. Okamura, M. Y.; Isaacson, R. A.; Feher, G. Proc. Natl. Acad. Sci. U.S.A. 1975, 72, 3491-3495.
41. Okamura, M. Y.; Debus, R. J.; Kleinfeld, D.; Feher, G. In Functions of Quinones in Energy Conserving Systems; Trumpower, B. L., Ed.; Academic Press: New York, 1982; pp 299-317.
42. (a) Stein, R. R.; Castellvi, A. L.; Bogacz, J. P.; Wraight, C. A. In Biosynthesis of the Photosynthetic Appralus: Molecular Development, and Regulation; Hallick, R., Staehlin, L. A., Thornber, J. P., Eds.; Alan R. Liss: New York, 1984; pp 167-183.
43. (b) Okamura, M. Y. ref 38a. pp 381-390.
44. This observation was elaborated on previously by: Giangiacomo, K. M.; Dutton, P. L. Proc. Natl. Acad. Sci. U.S.A. 1989, 86, 2658-2662.
45. (a) Bibikov, S. I.; Bloch, D. A.; Cherepanov, D. A.: Oesterhelt. D.: Semenov, A. Y. FEBS Lett. 1994, 341, 10-14.
46. (b) Lancaster, C. R. D.: Michel, H. In Reaction Centers of Photosynthetic Bacteria. Structure and Dynamics Michel-Beyerle, M. E., Ed.; Springer-Verlag: New York. 1996; pp 1-13.
47. B in native RCs when added in an approximately stoichiometric amount.
48. Warncke, K.; Gunner, M. R.; Braun, B. S.; Gu, L.; Yu, C.; Bruce, J. M.; Dutton, P. L. Biochemistry 1994, 33, 7830-7841.
49. Woodbury, N. W.; Parson, W. W.; Gunner, M. R.; Prince, R. C.; Dutton, P. L. Biochim. Biophys. Acta 1986, 851, 6-22.
50. Gunner, M. R.; Dutton, P. L. J Am. Chem. Soc: 1989, 111, 3400-3412.
51. For a complete discussion of this point see: Feher, G.; Arno, T. R.; Okamura, M. Y. In The Photosynthetic Bacterial Reaction Center; Breton, J., Verméglio, A., Eds.; Plenum Publishing: New York, 1988; pp 271-287.
52. Wraight, C. A,; Stein, R. R. FEBS Lett. 1980, 113, 73-77.
53. Verméglio, A. In Functions of Quinones in Energy Conserving Systems, Trumpower, B. L., Ed.: Academic Press: New York, 1982; pp 169-180.
54. (a) Marcus, R. A. J. Chem. Phys. 1956, 24, 966-978.
55. (b) Marcus, R. A.; Sutin, N. Biochim. Biophys. Acta 1985, 811, 265-322.
56. (c) Reviewed by: Albery, J. W. Annu. Rev. Phys. Chem. 1980, 31, 227-263.
57. (d) Reviewed by: Yates, K. J. Phys. Org. Chem. 1989, 2, 300-322.
58. For electron transfer in RCs, the entropy term in the free energy is often neglected. We, therefore, use the term exothermic (endothermic) to refer to reactions in which the free energy is less than zero (greater than zero).
59. (a) Sutin, N. In Inorganic Biochemistry; Eichhorn, G. L., Ed.; Eisevier: Amsterdam, The Netherlands, 1973; Vol. 2, pp 611-653.
60. (b) Scandola, F.; Balzani, V.; Schuster, G. B. J. Am. Chem. Soc: 1981, 103, 2519-2523.
61. (a) Klingler, R. J.; Kochi, J. K. J. Am. Chem. Soc: 1981, 103, 5839-5848.
62. (b) Klingler, R. J.; Kochi, J. K. J. Am. Chem. Soc: 1982, 104, 4186-4196.
63. Murphy, S. T.; Zou, C.; Miers, J. B.; Ballew, R. M.; Dlott, D. D.; Schuster, G. B. J. Phys. Chem. 1993, 97, 13152-13157.
64. 75
65. (2) reaction. Biexponential kinetics will be observed in many situations when intrinsic rates are similar.
66. a of the protonated semiquinone. The quinone substitution technique described here should be able to determine unambiguously whether proton transfer is the rate limiting step (i.e., mechanism 1). In this mechanism, the slope of the free energy dependence would be zero.
67. Albery, W. J. Faraday Discuss. Chem. Soc. 1982, 74, 245-256.
68. 31a Thus, 1.1 eV should be considered a lower limit for λ in mechanism 5.
69. 47d and work terms for electron transfer reactions in RCs are expected to be negligible since the redox centers are held at a constant separation by the protein matrix.
70. Rongey, S. H.; Paddock, M. L.; Feher, G.; Okamura, M. Y. Proc: Natl. Acad. Sci. U.S.A. 1993, 90, 1325-1329.
71. Paddock, M. L.; Feher, G.; Okamura, M. Y. Biophys. J. 1996, 70, All.
72. Paddock, M. L.; Feher, G.; Okamura, M. Y. Biochemistry 1995, 34, 15742-15750.
73. 69
74. 2 intermediate state ≃:470 meV above that of the initial state, consistent with the estimate of 490 meV based on solution redox potentials (see Appendix).
75. Baxendale, J. H.; Hardy, H. R. Trans. Farady Soc. 1953, 49, 1140-1144.
76. (a) Allen, J. P.; Feher, G.; Yeates, T. O.; Komiya, H.; Rees, D. C. Proc. Natl. Acad. Sci. U.S.A. 1988, 85, 8487-8491.
77. (b) Chirino, A. J.: Lous, E. J.; Huber, M.; Allen, J. P.; Schenck, C. C.; Paddock, M. L.; Feher, G.: Rees, D. C. Biochemistry 1994, 33, 4584-4593.
78. (a) Beroza, P.; Fredkin, D. R.; Okamura, M. Y.; Feher, G. In The Photosynthetic Bacterial Reaction Center II; Breton, J., Vermégleo, A., Eds.; Plenum Press: New York, 1992; pp 363-374.
79. (b) Gunner, M. R.; Honig, B. Proc. Natl. Acad. Sci. U.S.A. 1991, 88, 9151-9155.
80. (a) Lancaster, C. R. D.; Ermler, U.; Michel, H. In Anoxygenic Photosynthetic Bacteria; Blankenship, R. E., Madigan, M. T., Bauer, C. E., Eds.; Kluwer Academic Publishers: Dordrecht, The Netherlands, 1995; pp 503-526.
81. (b) Ermler, U.; Fritzsch, G.; Buchanan, S. K.; Michel, H. Structure 1994, 2, 925-936.
82. (c)Takahashi, E.; Wraight, C. A. Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 2640-2645.
83. B was observed (±5%).
84. Graige, M. S.; Paddock, M. L.; Feher, G.; Okamura, M. Y. Biophys. J. 1996, 70, A11.
85. Gennis, R. B.; Barquera, B.; Hacker, B.; Van Doren, S. R.; Arnaud, S.; Crofts, A. R., DAvidson, E.; Gray, K. A.; Daldal, A. J. Bioenerg. Biomembr. 1993, 25 (3), 195-209.
86. Discussed in: Falvins and Flamproteins, 1987: Proceedings of the Ninth International Symposium; Edmondson, D. E.; McCormick, D. B., Eds.; W. de Gruyten: Berlin, New York, 1987.
87. Wikström, M. Nature 1989, 338. 776-778.
88. Babcock, G. T.; Barry, B. A.; Debus, R. J.; Hoganson, C. W.; Atamian, M.; McIntosh, L.; Sithole, I.; Yocum, C. F. Biochemistry 1989, 28 (25), 9557-9565.
89. Swallow, A. J. In Functions of Quinones in Energy Conserving Systems: Trumpower, B. L., Ed.; Academic Press: New York, 1982: pp 59-72.
90. Morrison, L. E.; Schelhorn, J. E.; Cotton, T. M.; Bering, C. L.; Loach, P. A. In Functions of Qinones in Energy Conserving Systems; Trumpower, B. L., Ed.; Academic Press: New York, 1982; pp 35-57.