Identification of a novel protonation pattern for carboxylic acids upon QB photoreduction in Rhodobacter sphaeroides reaction center mutants at Asp-L213 and Glu-L212 sites

Biochemistry

Volumn 43, Issue 23, 2004, Pages 7236-7243

  Nabedryk, Eliane ^a   Breton, Jacques ^a   Okamura, Melvin Y ^b   Paddock, Mark L ^b  

^a CEA SACLAY   (France)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABSORPTION; AMINES; CARBOXYLIC ACIDS; ISOTOPES; MUTAGENESIS; PHOTOSYNTHESIS; REDUCTION;

CHEMICAL ENERGY; ELECTRON-PROTON TRANSFER; PHOTOREDUCTION; PROTONATION PATTERNS;

BIOCHEMISTRY;

1,4 BENZOQUINONE; AMINE; ASPARTIC ACID; CARBOXYLIC ACID; GLUTAMIC ACID;

ABSORPTION; ARTICLE; BACTERIUM MUTANT; ELECTRICITY; ELECTRON TRANSPORT; ENERGY; INFRARED SPECTROSCOPY; MUTATION; NONHUMAN; PHOTOSYNTHESIS; PRIORITY JOURNAL; PROTON TRANSPORT; RHODOBACTER SPHAEROIDES; VIBRATION;

AMINO ACID SUBSTITUTION; ASPARTIC ACID; BENZOQUINONES; CARBOXYLIC ACIDS; GLUTAMIC ACID; LIGHT; MOLECULAR STRUCTURE; MUTATION; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PROTEIN STRUCTURE, TERTIARY; PROTONS; RHODOBACTER SPHAEROIDES; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

BACTERIA (MICROORGANISMS); RHODOBACTER; RHODOBACTER SPHAEROIDES; RHODOPSEUDOMONAS;

EID: 2942555096     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049342y     Document Type: Article

References (67)

1. 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.
2. Paddock, M. L., Feher, G., and Okamura, M. Y. (2003) Proton-transfer pathways and mechanism in bacterial reaction centers, FEBS Lett. 555, 45-50.
3. Wraight, C. A. (2004) Proton and electron transfer in the acceptor quinone complex of photosynthetic reaction centers from Rhodobacter sphaeroides, Front. Biosci. 9, 309-337.
4. Feher, G., Allen, J. P., Okamura, M. Y., and Rees, D. C. (1989) Structure and function of bacterial photosynthetic reaction centers, Nature 339, 111-116.
5. + binding by bacterial photosynthetic reaction centers: Influences of the redox states of the acceptor quinones and primary donor, Biochim. Biophys. Acta 934, 329-347.
6. -, Biochim. Biophys. Acta 934, 348-368.
7. Miksovska, J., Schiffer, M., Hanson, D. K., and Sebban, P. (1999) Proton uptake by bacterial reaction centers: The protein complex responds in a manner similar to the reduction of either quinone acceptor, Proc. Natl. Acad. Sci. U.S.A. 96, 14348-14353.
8. Ermler, U., Fritzsch, G., Buchanan, S. K., and Michel, H. (1994) Structure of the photosynthetic reaction centre from Rhodobacter sphaeroides at 2.65 Å resolution: Cofactors and protein-cofactor interactions, Structure 2, 925-936.
9. Lancaster, C. R. D., Ermler, U., and Michel, H. (1995) The structures of photosynthetic reaction centres from purple bacteria as revealed by X-ray crystallography, in Anoxygenic Photosynthetic Bacteria (Blankenship, R. E., Madigan, M. T., and Bauer, C. E., Eds.) pp 503-525, Kluwer Academic Publishers, Dordrecht, The Netherlands.
10. 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.
11. Abresch, E. C., Paddock, M. L., Stowell, M. H. B., McPhillips, T. M., Axelrod, H. L., Soltis, S. M., Rees, D. C., Okamura, M. Y., and Feher, G. (1998) Identification of proton-transfer pathways in the X-ray structure of the bacterial reaction center from Rhodobacter sphaeroides, Photosynth. Res. 55, 119-125.
12. Fritzsch, G., Kampmann, L., Kapaun, G., and Michel, H. (1998) Water clusters in the reaction center of Rhodobacter sphaeroides, Photosynth. Res. 55, 127-132.
13. 2+, Proc. Natl. Acad. Sci. U.S.A. 96, 6183-6188.
14. 2+ in bacterial reaction centers, Proc. Natl. Acad. Sci. U.S.A. 97, 1542-1547.
15. B) in Rhodobacter sphaeroides chromatophores, Biochemistry 40, 429-439.
16. a of functionally important histidine residues, Biochemistry 42, 9626-9632.
17. L213 in the proton-transfer pathway to the secondary quinone of reaction centers from Rhodobacter sphaeroides, Biochim. Biophys. Acta 1020, 107-111.
18. B binding site, Biochemistry 31, 855-866.
19. Paddock, M. L., Rongey, S. H., McPherson, P. H., Juth, A., Feher, G., and Okamura, M. Y. (1994) Pathway of proton transfer in bacterial reaction centers: Role of aspartate-L213 in proton transfers associated with reduction of quinone to hydroquinone, Biochemistry 33, 734-745.
20. Paddock, M. L., McPherson, P. H., Feher, G., and Okamura, M. Y. (1990) Pathway of proton transfer in bacterial reaction centers: Replacement of serine-L223 by alanine inhibits electron and proton transfers associated with reduction of quinone to hydroquinone, Proc. Natl. Acad. Sci. U.S.A. 87, 6803-6807.
21. Paddock, M. L., Feher, G., and Okamura, M. Y. (1995) Pathway of proton transfer in bacterial reaction centers: Further investigations on the role of Ser-L223 studied by site-directed mutagenesis, Biochemistry 34, 15742-15750.
22. Paddock, M. L., Rongey, S. H., Feher, G., and Okamura, M. Y. (1989) Pathway of proton transfer in bacterial reaction centers: Replacement of glutamic acid 212 in the L subunit by glutamine inhibits quinone (secondary acceptor) turnover, Proc. Natl. Acad. Sci. U.S.A. 86, 6602-6606.
23. 2 in native and Glu-L212 → Gln mutant reaction centers from Rhodobacter sphaeroides, Biochemistry 33, 1181-1193.
24. 2 share a common entry point, Proc. Natl. Acad. Sci. U.S.A. 97, 13086-13091.
25. Ädelroth, P., Paddock, M. L., Tehrani, A., Beatty, J. T., Feher, G., and Okamura, M. Y. (2001) Identification of the proton pathway in bacterial reaction centers: Decrease of proton-transfer rate by mutation of surface histidine at H126 and H128 and chemical rescue by imidazole identifies the initial proton donors, Biochemistry 40, 14538-14546.
26. 2+, Proc. Natl. Acad. Sci. U.S.A. 97, 1548-1553.
27. B), Biochemistry 40, 6893-6902.
28. Maróti, P., Hanson, D. K., Schiffer, M., and Sebban, P. (1995) Long-range electrostatic interaction in the bacterial photosynthetic reaction centre, Nature Struct. Biol. 2, 1057-1059.
29. B can be achieved in the absence of Glu-L212, Biochemistry 36, 12216-12226.
30. - in bacterial wild-type and mutant reaction centers, Biochim. Biophys. Acta 1321, 149-156.
31. Gunner, M. R., and Honig, B. (1992) Calculations of proton uptake in Rhodobacter sphaeroides reaction centers, in The Photosynthetic Bacterial Reaction Center II (Breton, J., and Verméglio, A., Eds.) pp 403-410, Plenum Press, New York.
32. -, in the reaction center, Biophys. J. 68, 2233-2250.
33. B in bacterial photosynthetic reaction centers, Biochemistry 38, 8253-8270.
34. Cherepanov, D. A., Bibikov, S. I., Bibikova, M. V., Bloch, D. A., Drachev, L. A., Gopta, O. A., Oesterhelt, D., Semenov, A. Y., and Mulkidjanian, A. Y. (2000) Reduction and protonation of the secondary quinone acceptor of Rhodobacter sphaeroides photosynthetic reaction center: Kinetic model based on a comparison of wild-type chromatophores with mutants carrying Arg → Ile substitution at sites 207 and 217 in the L-subunit, Biochim. Biophys. Acta 1459, 10-34.
35. Rabenstein, B., Ullmann, G. M., and Knapp, E.-W. (2000) Electron transfer between the quinones in the photosynthetic reaction center and its coupling to conformational changes, Biochemistry 39, 10487-10496.
36. Ishikita, H., Morra, G., and Knapp, E.-W. (2003) Redox potential of quinones in photosynthetic reaction centers from Rhodobacter sphaeroides: Dependence on protonation of Glu-L212 and Asp-L213, Biochemistry 42, 3882-3892.
37. Grafton, A. K., and Wheeler, R. A. (1999) Amino acid protonation states determine binding sites of the secondary ubiquinone and its anion in the Rhodobacter sphaeroides photosynthetic reaction center, J. Phys. Chem. B 103, 5380-5387.
38. Walden, S. E., and Wheeler, R. A. (2002) Protein conformational gate controlling binding site preference and migration for ubiquinone-B in the photosynthetic reaction center of Rhodobacter sphaeroides, J. Phys. Chem. B 106, 3001-3006.
39. B reduction, Biophys. J. 84, 2090-2098.
40. Mäntele, W. (1993) Reaction-induced infrared difference spectroscopy for the study of protein function and reaction mechanisms, Trends Biochem. Sci. 18, 197-202.
41. Vogel, R., and Siebert, F. (2000) Vibrational spectroscopy as a tool for probing protein function, Curr. Opin. Chem. Biol. 4, 518-523.
42. Siebert, F. (1993) Infrared spectroscopic investigations of retinal proteins, in Biomolecular Spectroscopy, (Clark, R. J. H., and Hester, R. E., Eds.) Part A, pp 1-54, John Wiley & Sons, New York.
43. Nabedryk, E., Breton, J., Hienerwadel, R., Fogel, C., Mäntele, W., Paddock, M. L., and Okamura, M. Y. (1995) Fourier transform infrared difference spectroscopy of secondary quinone acceptor photoreduction in proton-transfer mutants of Rhodobacter sphaeroides, Biochemistry 34, 14722-14732.
44. - formation in the photosynthetic reaction center of Rhodobacter sphaeroides: Evidence from time-resolved infrared spectroscopy, Biochemistry 34, 2832-2843.
45. B in the photosynthetic reaction center from Rhodobacter capsulatus with FTIR spectroscopy, Biochim. Biophys. Acta 1411, 206-213.
46. B in the photosynthetic reaction center from Rhodobacter capsulatus, Biochemistry 39, 14654-14663.
47. B in reaction centers from Rhodobacter sphaeroides, Biochemistry 40, 13826-13832.
48. 2H exchange, in Photosynthesis: From Light to Biosphere (Mathis, P., Ed.) Vol. I, pp 875-878, Kluwer Academic Publishers, Dordrecht, The Netherlands.
49. B) in bacterial reaction centers from Rhodobacter sphaeroides: FTIR studies on the effects of replacing Glu H173, Biochemistry 37, 14457-14462.
50. B in Rhodobacter sphaeroides reaction centers, Biochim. Biophys. Acta 1553, 320-330.
51. B by interchanging Asp and Glu at the L212 and L213 sites, Biochemistry 36, 14238-14249.
52. B reduction: Effect of interchanging Glu and Asp at the L213 and L212 sites, in Photosynthesis: Mechanisms and Effects (Garab, G., Ed.) Vol. 2, pp 845-848, Kluwer Academic Publishers, Dordrecht, The Netherlands.
53. Paddock, M. L., Rongey, S. H., Abresch, E. C., Feher, G., and Okamura, M. Y. (1988) Reaction centers from three herbicide resistant mutants of Rhodobacter sphaeroides 2.4.1: Sequence analysis and preliminary characterization, Photosynth. Res. 17, 75-96.
54. B) in photosynthetic bacterial reaction centers by light-induced FTIR difference spectroscopy, FEBS Lett. 288, 109-113.
55. B vibrations in Rhodobacter sphaeroides and Rhodopseudomonas viridis probed by isotope labeling, Biochemistry 34, 11606-11616.
56. B carbonyl groups in Rhodobacter sphaeroides R26 reaction centers, FEBS Lett. 370, 88-92.
57. 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.
58. Krimm, S., and Bandekar, J. (1986) Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins, Adv. Protein Chem. 38, 181-364.
59. 2O) solutions. I. Spectral parameters of amino acid residue absorption bands, Biopolymers 30, 1243-1257.
60. Rahmelow, K., Hübner, W., and Ackermann, T. (1998) Infrared absorbance of protein side chains, Anal. Biochem. 257, 1-11.
61. Dioumaev, A. K., and Braiman, M. S. (1995) Modeling vibrational spectra of amino acid side chains in proteins: The carbonyl stretch frequency of buried carboxylic residues, J. Am. Chem. Soc. 117, 10572-10574.
62. A demonstrated by mutations at residues Glu L104 and Trp L100 in reaction centers from Rhodobacter sphaeroides, Biochemistry 36, 4515-4525.
63. Breton, J., and Nabedryk, E. (1998) Proton uptake upon quinone reduction in bacterial reaction centers: IR structure and possible participation of a highly polarizable hydrogen bond network, Photosynth. Res. 55, 301-307.
64. 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.
65. Lancaster, C. R. D., Michel, H., Honig, B., and Gunner, M. R. (1996) Calculated coupling of electron and proton transfer in the photosynthetic reaction center of Rhodopseudomonas viridis, Biophys. J. 70, 2469-2492.
66. Rabenstein, B., Ullmann, G. M., and Knapp, E.-W. (1998) Energetics of electron transfer and protonation reactions of the quinones in the photosynthetic reaction center of Rhodopseudomonas viridis, Biochemistry 37, 2488-2495.
67. Breton, J., Nabedryk, E., Mioskowski, C., and Boullais, C. (1996) Protein - quinone interactions in photosynthetic bacterial reaction centers investigated by light-induced FTIR difference spectroscopy, in The Reaction Center of Photosynthetic Bacteria, Structure, and Dynamics (Michel-Beyerle, M.-E., Ed.) pp 381-394, Springer-Verlag, New York.