Formation of a Semiquinone at the QB Site by A- or B-Branch Electron Transfer in the Reaction Center from Rhodobacter sphaeroides

Biochemistry

Volumn 43, Issue 16, 2004, Pages 4755-4763

  Wakeham, Marion C ^a   Breton, Jacques ^b   Nabedryk, Eliane ^b   Jones, Michael R ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b CEA SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPHAGES; CONFORMATIONS; CRYOGENICS; ELECTRON TRANSITIONS; FOURIER TRANSFORM INFRARED SPECTROSCOPY; MUTAGENESIS; PHOTOACOUSTIC EFFECT; PHOTOOXIDATION; RHODIUM COMPOUNDS;

COFACTORS; CRYOGENIC TEMPERATURE; RHODOBACTER SPHAEROIDES; TRANSMEMBRANE;

BIOCHEMISTRY;

SEMIQUINONE; ALANINE; ANTIINFECTIVE AGENT; BENZOQUINONE DERIVATIVE; POLYENE; SEMIQUINONE RADICALS; STIGMATELLIN; TRYPTOPHAN; UBIQUINONE;

ARTICLE; BACTERIAL METABOLISM; BACTERIAL MUTATION; BIOACCUMULATION; CONTROLLED STUDY; ELECTRON TRANSPORT; MOLECULAR INTERACTION; NONHUMAN; PHOTOREACTIVITY; PRIORITY JOURNAL; QUANTUM YIELD; RHODOBACTER SPHAEROIDES; TRANSPORT KINETICS; BINDING SITE; CHEMISTRY; COMPARATIVE STUDY; DRUG ANTAGONISM; FREEZING; GENETICS; INFRARED SPECTROSCOPY; LIGHT; METABOLISM; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; SITE DIRECTED MUTAGENESIS;

BACTERIA (MICROORGANISMS); JONES; RHODOBACTER; RHODOBACTER SPHAEROIDES; RHODOPSEUDOMONAS; UNIDENTIFIED BACTERIOPHAGE;

ALANINE; ANTI-BACTERIAL AGENTS; BENZOQUINONES; BINDING SITES; ELECTRON TRANSPORT; FREEZING; LIGHT; MUTAGENESIS, SITE-DIRECTED; OXIDATION-REDUCTION; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; POLYENES; RHODOBACTER SPHAEROIDES; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; TRYPTOPHAN; UBIQUINONE;

EID: 1942502803     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi035726x     Document Type: Article

References (64)

1. Heathcote, P., Fyfe, P. K., and Jones, M. R. (2002) Reaction centres: structure and mechanism in biological solar power, Trends Biochem. Sci. 27, 79-87.
2. Hoff, A. J., and Deisenhofer, J. (1997) Photophysics of photosynthesis: Structure and spectroscopy of reaction centres of purple bacteria, Phys. Rep. 287, 2-247.
3. Allen, J. P., Feher, G., Yeates, T. O., Komiya, H., and Rees, D. C. (1987) Structure of the reaction center from Rhodobacter sphaeroides R-26-the cofactors, Proc. Natl. Acad. Sci. U.S.A. 84, 5730-5734.
4. Allen, J. P., Feher, G., Yeates, T. O., Komiya, H., and Rees, D. C. (1987) Structure of the reaction center from Rhodobacter sphaeroides R-26-the protein subunits, Proc. Natl. Acad. Sci. U.S.A. 84, 6162-6166.
5. Chang, C. H., El Kabbani, O., Tiede, D., Norris, J., and Schiffer, M. (1991) Structure of the membrane-bound protein photosynthetic reaction center from Rhodobacter sphaeroides, Biochemistry 30, 5352-5360.
6. Ermler, U., Fritzsch, G., Buchanan, S. K., and Michel, H. (1994) Structure of the photosynthetic reaction center from Rhodobacter sphaeroides at 2.65-angstrom resolution-cofactors and protein-cofactor interactions, Structure 2, 925-936.
7. Ermler, U., Michel, H., and Schiffer, M. (1994) Structure and function of the photosynthetic reaction center from Rhodobacter sphaeroides, J. Bioenerg. Biomembr. 26, 5-15.
8. Stowell, M. H. B., McPhillips, T. M., Rees, D. C., Soltis, S. M., Abresch, E., and Feher, G. (1997) Light-induced structural changes in photosynthetic reaction center: Implications for mechanism of electron-proton transfer, Science 276, 812-816.
9. Fyfe, P. K., and Jones, M. R. (2000) Reemerging structures: continuing crystallography of the bacterial reaction centre, Biochim. Biophys. Acta 1459, 413-421.
10. Parson, W. W. (1991) Reaction centers, in Chlorophylls (Scheer, H., Ed.) pp 1153-1180, CRC Press, Boca Raton, FL.
11. Fleming, G. R., and Van Grondelle, R. (1994) The primary steps of photosynthesis, Phys. Today 47, 48-55.
12. Woodbury, N. W., and Allen, J. P. (1995) The pathway, kinetics and thermodynamics of electron transfer in wild type and mutant bacterial reaction centers of purple nonsulfur bacteria, in Anoxygenic Photosynthetic Bacteria (Blankenship, R. E., Madigan, M. T., and Bauer, C. E., Eds.) pp 527-557, Kluwer Academic Publishers, Dordrecht, The Netherlands.
13. Parson, W. W. (1996) Photosynthetic bacterial reaction centers, in Protein Electron Transfer (Bendall, D. S., Ed.) pp 125-160, BIOS Scientific Publishers, Oxford, U.K.
14. Van Brederode, M. E., and Jones, M. R. (2000) Reaction Centres of Purple Bacteria, in Enzyme-Catalysed Electron and Radical Transfer (Scrutton, N. S., and Holzenburg, A., Eds.) pp 621-676, Kluwer Academic/Plenum Publishers, New York.
15. B in reaction centers from photosynthetic bacteria, in Anoxygenic Photosynthetic Bacteria (Blankenship, R. E., Madigan, M. T., and Bauer, C. E., Eds.) pp 577-594, Kluwer Academic Publishers, Dordrecht, The Netherlands.
16. Okamura, M. Y., Paddock, M. L., Graige, M. S., and Feher, G. (2000) Proton and electron transfer in bacterial reaction centers. Biochim. Biophys. Acta 1458, 148-163.
17. Kirmaier, C., Gaul, D., Debey, R., Holten, D., and Schenck, C. C. (1991) Charge separation in a reaction center incorporating bacteriochlorophyll for photoactive bacteriopheophytin, Science 251, 922-927.
18. Heller, B. A., Holten, D., and Kirmaier, C. (1995) Control of electron-transfer between the L-side and M-side of photosynthetic reaction centers, Science 269, 940-945.
19. - via B-branch electron transfer in mutant reaction centres, in Photosynthesis: Mechanisms and Effects (Garab, G., Ed.) pp 849-852, Kluwer, Dordrecht, The Netherlands.
20. Katilius, E., Turanchik, T., Lin, S., Taguchi, A. K. W., and Woodbury, N. W. (1999) B-side electron transfer in a Rhodobacter sphaeroides reaction center mutant in which the B-side monomer bacteriochlorophyll is replaced with bacteriopheophytin, J. Phys. Chem. B. 103, 7386-7389.
21. Kirmaier, C., Weems, D., and Holten, D. (1999) M-side electron transfer in reaction center mutants with a lysine near the nonphotoactive B bacteriochlorophyll, Biochemistry 38, 11516-11530.
22. Kirmaier, C., He, C. Y., and Holten, D. (2001) Manipulating the direction of electron transfer in the bacterial reaction center by swapping Phe for Tyr near BCh1(M) (L181) and Tyr for Phe near BCh1(L) (M208), Biochemistry 40, 12132-12139.
23. Roberts, J. A., Holten, D., and Kirmaier, C. (2001) Primary events in photosynthetic reaction centers with multiple mutations near the photoactive electron carriers, J. Phys. Chem. B 105, 5575-5584.
24. de Boer, A. L., Neerken, S., de Wijn, R., Permentier, H. P., Gast, P., Vögenboom, E., and Hoff, A. J. (2002) High yield of B-branch electron transfer in a quadruple reaction center mutant of the photosynthetic bacterium Rhodobacter sphaeroides, Biochemistry 41, 3081-3088.
25. de Boer, A. L., Neerken, S., de Wijn, R., Permentier, H. P., Gast, P., Vögenboom, E., and Hoff, A. J. (2002) B-branch electron transfer in reaction centers of Rhodobacter sphaeroides assessed with site-directed mutagenesis, Photosynth. Res. 71, 221-239.
26. Kirmaier, C., Laible, P. D., Czarnecki, K., Hata, A. N., Hanson, D. K., Bocian, D. F., and Holten, D. (2002) Comparison of M-side electron transfer in Rb. sphaeroides and Rb. capsulatus reaction centers, J. Phys Chem. B 106, 1799-1808.
27. Katilius, E., Katiliene, Z., Lin, S., Taguchi, A. K. W., and Woodbury, N. W. (2002) B side electron transfer in a Rhodobacter sphaeroides reaction center mutant in which the B side monomer bacteriochlorophyll is replaced with bacteriopheophytin: Low-temperature study and energetics of charge-separated states, J. Phys Chem. B 106, 1471-1475.
28. Kirmaier, C., Cua, A., He, C. Y., Holten, D., and Bocian, D. F. (2002) Probing M-branch electron transfer and cofactor environment in the bacterial photosynthetic reaction center by addition of a hydrogen bond to the M-side bacteriopheophytin, J. Phys. Chem. B 106, 495-503.
29. Laible, P. D., Kirmaier, C., Udawatte, C. S. M., Hofman, S. J., Holten, D., and Hanson, D. K. (2003) Quinone reduction via secondary B-branch electron transfer in mutant bacterial reaction centers, Biochemistry 42, 1718-1730.
30. B, Biochemistry 42, 2016-2024.
31. A ubiquinone, FEBS Lett. 540, 234-240.
32. A ubiquinone and carotenoid in the reaction center from Rhodobacter sphaeroides, Photosynth. Res. 59, 9-26.
33. McAuley, K. E., Fyfe, P. K., Ridge, J. P., Cogdell, R. J., Isaacs, N. W., and Jones, M. R. (2000) Ubiquinone binding, ubiquinone exclusion, and detailed cofactor conformation in a mutant bacterial reaction center, Biochemistry 39, 15032-15043.
34. Hanson, D. K., Baciou, L., Tiede, D. M., Nance, S. L., Schiffer, M., and Sebban, P. (1992) In bacterial reaction centers protons can diffuse to the secondary quinone by alternative pathways, Biochim. Biophys. Acta 1102, 260-265.
35. B binding-site of the photosynthetic reaction-center, Proc. Natl. Acad. Sci. U.S.A. 90, 8929-8933.
36. Maróti, P., Hanson, D. K., Baciou, L., Schiffer, M., and Sebban, P. (1994) Proton conduction within the reaction centers of Rhodobacter capsulatus-the electrostatic role of the protein, Proc. Natl. Acad. Sci. U.S.A. 91, 5617-5621.
37. Nabedryk, E., Bagley, K. A., Thibodeau, D. L., Bauscher, M., Mäntele, W., and Breton, J. (1990) A protein conformational change associated with the photoreduction of the primary and secondary quinones in the bacterial reaction center, FEBS Lett. 266, 59-62.
38. - states in reaction centers from Rb. sphaeroides, in Current Research in Photosynthesis (Baltscheffsky, M., Ed.) pp 75-85, Springer, Berlin, Germany.
39. A in Rhodobacter sphaeroides using site-specific C-13-labeled ubiquinone, Biochemistry 33, 14378-14386.
40. B vibrations in Rhodobacter sphaeroides and Rhodopseudomonas viridis probed by isotope labeling, Biochemistry 34, 11606-11616.
41. Breton, J., and Nabedryk, E. (1996) Protein-quinone interactions in the bacterial photosynthetic reaction center: Light-induced FTIR difference spectroscopy of the quinone vibrations, Biochim. Biophys. Acta 1275, 84-90.
42. Jones, M. R., Fowler, G. J. S., Gibson, L. C. D., Grief, G. G., Olsen, J. D., Crielaard, W., and Hunter, C. N. (1992) Construction of mutants of Rhodobacter sphaeroides lacking one or more pigment-protein complexes and complementation with reaction-centre, LH1, and LH2 genes, Mol. Microbiol. 6, 1173-1184.
43. Jones, M. R., Heer-Dawson, M., Mattioli, T. A., Hunter, C. N., and Robert, B. (1994) Site-specific mutagenesis of the reaction centre from Rhodobacter sphaeroides studied by Fourier transform Raman spectroscopy: Mutations at tyrosine M210 do not affect the electronic structure of the primary donor, FEBS Lett. 339, 18-24.
44. McAuley-Hecht, K. E., Fyfe, P. K., Ridge, J. P., Prince, S. M., Hunter, C. N., Isaacs, N. W., Cogdell, R. J., and Jones, M. R. (1998) Structural studies of wild type and mutant reaction centres from an antenna-deficient strain of Rhodobacter sphaeroides: monitoring the optical properties of the complex from cell to crystal, Biochemistry 37, 4740-4750.
45. Nabedryk, E. (1996) Light-induced Fourier transform infrared difference spectroscopy of the primary electron donor in photosynthetic reaction centers, in Infrared Spectroscopy of Biomolecules (Mantsch, H. H., and Chapman, D., Eds.) pp 39-81, Wiley-Liss, New York.
46. B, Structure 5, 1339-1359.
47. Kleinfeld, D., Feher, G., and Okamura, M. Y. (1984) Electron-transfer kinetics in photosynthetic reaction centers cooled to cryogenic temperatures in the charge-separated state-evidence for light-induced structural-changes, Biochemistry 23, 5780-5786.
48. - in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay, Proc. Natl. Acad. Sci. U.S.A. 95, 11679-11684.
49. - in Rhodobacter sphaeroides reaction centers, Biochemistry 39, 7445-7454.
50. McElroy, J. D., Feher, G., and Mauzerall, D. C. (1969) On the nature of the free radical formed during the primary process of bacterial photosynthesis, Biochim. Biophys. Acta 172, 180-183.
51. Fritzsch, G., Koepke, J., Diem, R., Kuglstatter, A., and Baciou, L. (2002) Charge separation induces conformational changes in the photosynthetic reaction centre of purple bacteria, Acta Crystallogr. Sect. D 58, 1660-1663.
52. Pokkuluri, P. R., Laible, P. D., Deng, Y.-L., Wong, T. N., Hanson, D. K., and Schiffer, M. (2002) The structure of a mutant photosynthetic reaction center shows unexpected changes in main chain orientations and quinone position, Biochemistry 41, 5998-6007.
53. Kuglstatter, A., Ermler, U., Michel, H., Baciou, L., and Fritzsch, G. (2001) X-ray structure analyses of photosynthetic reaction center variants from Rhodobacter sphaeroides: Structural changes induced by point mutations at position L209 modulate electron and proton transfer, Biochemistry 40, 4253-4260.
54. Spiedel, D., Roszak, A. W., McKendrick, K., McAuley, K. E., Fyfe, P. K., Nabedryk, E., Breton, J., Robert, B., Cogdell, R. J., Isaacs, N. W., and Jones, M. R. (2002) Tuning of the optical and electrochemical properties of the primary donor bacteriochlorophylls in the reaction center from Rhodobacter sphaeroides: spectroscopy and structure, Biochim. Biophys. Acta, 1554, 75-93.
55. B binding site at the proximal position in wild-type reaction centers and in the Pro-L209 → Tyr mutant from Rhodobacter sphaeroides, Biochemistry 41, 12921-12927.
56. B) binding site and protein structural changes in photosynthetic reaction center mutants at Pro-L209 revealed by vibrational spectroscopy, Biochemistry 42, 5819-5827.
57. B electron transfer in bacterial photosynthetic reaction centers: Effect of substrate position and tail length on the conformational gating step, Biochemistry 41, 10021-10025.
58. B in Rhodospeudomonas viridis photosynthetic reaction centers, Biochim. Biophys. Acta 1505, 280-290.
59. - with the protein in native and Ser-223 → Ala Rb. sphaeroides reaction centers probed by light-induced FTIR difference spectroscopy, Biophys. J. 72, A7.
60. B binding-site, Biochemistry 31, 855-866.
61. Xu, Q., and Gunner, M. R. (2001) Trapping conformational intermediate states in the reaction center protein from photosynthetic bacteria, Biochemistry, 40, 3232-3241.
62. Joliot, P., and Joliot, A. (1999) In vivo analysis of the electron transfer within Photosystem-1: are the two phylloquinones involved? Biochemistry 38, 11130-11136.
63. Guergova-Kuras, M., Boudreaux, B., Joliot, A., Joliot, P., and Redding, K. (2001) Evidence for two active branches for electron transfer in Photosystem-I, Proc. Natl. Acad. Sci U.S.A. 98, 4437-4442.
64. Purton, S., Stevens, D. R., Muhiuddin, I. P., Evans, M. C. W., Carter, S., Rigby, S. E. J., and Heathcote, P. (2001) Site-directed mutagenesis of PsaA residue W693 affects phylloquinone binding and function in the Photosystem I reaction center of Chlamydomonas reinhardtii, Biochemistry 40, 2167-2175.