An isotope-edited FTIR investigation of the role of Ser-L223 in binding quinone (QB) and semiquinone (QB-) in the reaction center from Rhodobacter sphaeroides

Biochemistry

Volumn 44, Issue 44, 2005, Pages 14519-14527

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

^a CEA SACLAY   (France)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; FOURIER TRANSFORM INFRARED SPECTROSCOPY; HYDROGEN BONDS; KETONES; MUTAGENESIS; PHOTOSYNTHESIS; PROTONS; REDOX REACTIONS;

BINDING QUINONE; ELECTRON TRANSFER REACTIONS; FINGERPRINT SPECTRA; REDOX CHEMISTRY;

PROTEINS;

ALANINE; ASPARTIC ACID; CARBON; ISOTOPE; LEUCINE; OXYGEN; PROTON; QUINOL; QUINONE DERIVATIVE; SEMIQUINONE; SERINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; ELECTRON RADIATION; HYDROGEN BOND; INFRARED SPECTROSCOPY; LIGHT; NONHUMAN; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PRIORITY JOURNAL; PROTON TRANSPORT; RHODOBACTER SPHAEROIDES; SEQUENCE ANALYSIS;

AMINO ACID SUBSTITUTION; BINDING SITES; ELECTRON TRANSPORT; HYDROGEN BONDING; LIGHT; MUTAGENESIS, SITE-DIRECTED; OXIDATION-REDUCTION; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PROTEIN CONFORMATION; PROTONS; QUINONES; RHODOBACTER SPHAEROIDES; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

BACTERIA (MICROORGANISMS); RHODOBACTER SPHAEROIDES;

EID: 27644458594     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi051328d     Document Type: Article

References (68)

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. - in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay, Proc. Natl. Acad. Sci. U.S.A. 95, 11679-11684.
3. B) reduction in reaction centers of Rb. sphaeroides, J. Am. Chem. Soc. 118, 9005-9016.
4. 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.
5. 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.
6. Paddock, M. L., Feher, G., and Okamura, M. Y. (2003) Proton transfer pathways and mechanism in bacterial reaction centers, FEBS Lett. 555, 45-50.
7. 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.
8. B in bacterial photosynthetic reaction centers, Biochemistry 38, 8253-8270.
9. B redox state in reaction centers from Rhodobacter sphaeroides, J. Am. Chem. Soc. 126, 8059-8064.
10. Zhu, Z., and Gunner, M. R. (2005) Energetics of quinone-dependent electron and proton transfers in Rhodobacter sphaeroides photosynthetic reaction centers, Biochemistry 44, 82-96.
11. 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.
12. 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.
13. 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.
14. B in the photosynthetic reaction center of Rhodopseudomonas viridis, Biochemistry 32, 1958-1964.
15. Deisenhofer, J., and Michel, H. (1989) The photosynthetic reaction centre from the purple bacterium Rhodopseudomonas viridis, EMBO J. 8, 2149-2170.
16. 2+) interactions, Proc. Natl. Acad. Sci. U.S.A. 85, 8487-8491.
17. El-Kabbani, O., Chang, C.-H., Tiede, D., Norris, J., and Schiffer, M. (1991) Comparison of reaction centers from Rhodobacter sphaeroides and Rhodopseudomonas viridis: Overall architecture and protein-pigment interactions, Biochemistry 30, 5361-5369.
18. Chirino, A. J., Lous, E. J., Huber, M., Allen, J. P., Schenck, C. C., Paddock, M. L., Feher, G., and Rees, D. C. (1994) Crystallographic analyses of site-directed mutants of the photosynthetic reaction center from Rhodobacter sphaeroides, Biochemistry 33, 4584-4593.
19. 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.
20. Arnoux, B., and Reiss-Husson, F. (1996) Pigment-protein interactions in Rhodobacter sphaeroides Y photochemical reaction center; Comparison with other reaction center structures, Eur. Biophys. J. 24, 233-242.
21. 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 503-526, Kluwer Academic Publishers, Dordrecht, The Netherlands.
22. 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. D 58, 1660-1663.
23. McAuley, K. E., Fyfe, P. K., Ridge, J. P., Cogdell, R. J., Isaacs, N. W., and Jones, M. (2000) Ubiquinone binding, ubiquinone exclusion, and detailed cofactor conformation in a mutant bacterial reaction center, Biochemistry 39, 15032-15043.
24. B) reduction by B-branch electron transfer in mutant bacterial reaction centers from Rhodobacter sphaeroides: Quantum efficiency and X-ray structure, Biochemistry 44, 6920-6928.
25. Pokkuluri, P. R., Laible, P. D., Crawford, A. E., Mayfield, J. F., Yousef, M. A., Ginell, S. L., Hanson, D. K., and Schiffer, M. (2004) Temperature and cryoprotectant influence secondary quinone binding position in bacterial reaction centers, FEBS Lett. 570, 171-174.
26. -. formed by B-branch electron transfer in reaction centers from Rhodobacter sphaeroides, in Photosynthesis: Fundamental Aspects to Global Perspectives (van der Est, A., and Bruce, D., Eds.), pp. 207-209, Alliance Communications Group, Lawrence, KA.
27. B reduction revealed by ENDOR spectroscopy in reaction centers from Rhodobacter sphaeroides, Biophys. J. 88, A204.
28. Bibikov, S. I., Bloch, D. A., Cherepanov, A., Oesterhelt, D., and Semenov, A. Yu. (1994) Flash-induced electrogenic reactions in the SA(L223) reaction center mutant in Rhodobacter sphaeroides chromatophores, FEBS Lett. 341, 10-14.
29. Nabedryk, E., Breton, J., Hienerwadel, R., Fogel, C., Man̈tele, 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.
30. 2H exchange, in Photosynthesis: from Light to Biosphere (Mathis, P., Ed.) Vol. I, pp 875-878, Kluwer Academic Publishers, Dordrecht, The Netherlands.
31. B vibrations in Rhodobacter sphaeroides and Rhodopseudomonas viridis probed by isotope labeling, Biochemistry 34, 11606-11616.
32. B carbonyl groups in Rhodobacter sphaeroides R26 reaction centers, FEBS Lett. 370, 88-92.
33. B in bacterial photosynthetic reaction centers, Biochemistry 43, 3318-3326.
34. 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.
35. B) binding site and protein structural changes in photosynthetic reaction center mutants at Pro-L209 revealed by vibrational spectroscopy, Biochemistry 42, 5819-5827.
36. B upon photoreduction via A-branch or B-branch electron transfer in mutant reaction centers from Rhodobacter sphaeroides, Biochim. Biophys. Acta 1656, 127-138.
37. - with the protein in native and Ser-L223→Ala Rb. sphaeroides reaction centers probed by light-induced FTIR difference spectroscopy, Biophys. J. 72, A7.
38. B) in photosynthetic bacterial reaction centers by light-induced FTIR difference spectroscopy, FEBS Lett. 288, 109-113.
39. Boullais, C., Nabedryk, E., Burie, J.-R., Nonella, M., Mioskowski, C., and Breton, J. (1998) Site-specific isotope-labeling demonstrates a large mesomeric resonance effect of the methoxy groups on the carbonyl frequencies in ubiquinones, Photosynth. Res. 55, 247-252.
40. B in reaction centers from Rhodobacter sphaeroides, Biochemistry 40, 13826-13832.
41. Lutz, M., and Mäntele, W. (1991) Vibrational spectroscopy of chlorophylls in The Chlorophylls (Scheer, H., Ed.) pp 855-902, CRC Press, Boca Raton, FL.
42. Breton, J., and Nabedryk, E., (1996) Protein-interactions in the bacterial photosynthetic reaction center: Light-induced FTIR difference spectroscopy of the quinone vibrations, Biochim. Biophys. Acta 1275, 84-90.
43. Nabedryk, E., Allen, J. P., Taguchi, A. K. W., Williams, J. C., Woodbury, N. W., and Breton, J. (1993) Fourier transform infrared study of the primary electron donor in chromatophores of Rhodobacter sphaeroides with reaction centers genetically modified at residues M160 and L131, Biochemistry 32, 13879-13885.
44. Mattioli, T. A., Williams, J. C., Allen, J. P., and Robert B. (1994) Changes in primary donor hydrogen-bonding interactions in mutant reaction centers from Rhodobacter sphaeroides: Identification of the vibrational frequencies of all the conjugated carbonyl groups, Biochemistry 33, 1636-1643.
45. Mattioli, T. A., Lin, X., Allen, J. P., and Williams, J. C. (1995) Correlation between multiple hydrogen bonding and alteration of the oxidation potential of the bacteriochlorophyll dimer of reaction centers from Rhodobacter sphaeroides, Biochemistry 34, 6142-6152.
46. Robert, B. (1990) Resonance Raman studies of bacterial reaction centers, Biochim. Biophys. Acta 1017, 99-111.
47. Nabedryk, E., Andrianambinintsoa, S., Dejonghe, D., and Breton, J. (1995) FTIR spectroscopy of the photoreduction of the bacteriopheophytin electron acceptor in reaction centers of Rb. sphaeroides and Rps. viridis, Chem. Phys. 194, 371-378.
48. Palaniappan, V., and Bocian, D. F. (1995) Resonance Raman spectroscopic evidence for dielectric asymmetry in bacterial photosynthetic reaction centers, J. Am. Chem. Soc. 117, 3647-3648.
49. A in reaction centers from Rhodopseudomonas viridis revealed by Fourier transform infrared spectroscopy and site-directed mutagenesis, Biochemistry 38, 11541-11552.
50. Moenne-Loccoz, P., Robert, B., and Lutz, M. (1989) A resonance Raman characterization of the primary electron acceptor in photosystem II, Biochemistry 28, 3641-3645.
51. Nabedryk, E., Andrianambinintsoa, S., Berger, G., Leonhard, M., Mäntele, W., and Breton, J. (1990) Characterization of bonding interactions of the intermediary electron acceptor in the reaction center of photosystem II by FTIR spectroscopy, Biochim. Biophys. Acta 1016, 49-54.
52. +, Biochemistry 43, 8380-8390.
53. Breton, I., Chitnis, P. R., and Pantelidou, M. (2005) Evidence for hydrogen bond formation to the PsaB chlorophyll of P700 in photosystem I mutants of Synechocystis sp. PCC 6803, Biochemistry 44, 5402-5408.
54. Witt, H., Schlodder, E., Teutloff, C., Niklas, J., Bordignon, E., Carbonera, D., Kohler, S., Labahn, A., and Lubitz, W. (2002) Hydrogen bonding to P700: Site-directed mutagenesis of threonine A739 of photosystem I of Chlamydomonas reinhardtii, Biochemistry 41, 8557-8569.
55. Rautter, J., Lendzian, F., Schulz, C., Fetsch, A., Kuhn, M., Lin, X., Williams, J. C., Allen, J. P., and Lubitz, W. (1995) ENDOR studies of the primary donor cation radical in mutant reaction centers of Rhodobacter sphaeroides with altered hydrogen-bond interactions, Biochemistry 34, 8130-8143.
56. -. in reaction centers of Rps. viridis, in Current Research in Photosynthesis (Baltscheffsky, M., Ed.) Vol. I, pp 141-144, Kluwer Academic Publishers, Dordrecht, The Netherlands.
57. 13C-labeled ubiquinone, Biochemistry 33, 14378-14386.
58. A in Rhodobacter sphaeroides R26 reaction centers monitored by Fourier transform infra-red spectroscopy using site-specific isotopically labelled ubiquinone-10, EMBO J. 13, 5523-5530.
59. Feher, G., Isaacson, R. A., Okamura, M. Y., and Lubitz, W. (1985) ENDOR of semiquinones in RCs from Rhodopseudomonas sphaeroides, in Antennas and Reaction centers of Photosynthetic Bacteria-Structure, Interactions and Dynamics (Michel-Beyerle, M. E., Ed.) Springer Series in Chemical Physics, Vol. 42, pp 174-189, Springer, Berlin.
60. van der Brink, J. S., Spoyalov, A. P., Gast, P., van Liemt, W. B. S., Raap, J., Lugtenburg, J., and Hoff, A. J. (1994) Asymmetric binding of the primary quinone acceptor in reaction centers of the photosynthetic bacterium Rhodobacter sphaeroides R26, probed with Q-band (35 GHz) EPR spectroscopy, FEBS Lett. 353, 273-276.
61. -. by EPR and ENDOR, Appl. Magn. Reson. 17, 1-48.
62. Burie, J.-R., Boullais, C., Nonella, M., Mioskowski, C., Nabedryk, E., and Breton, J. (1997) Importance of the conformation of methoxy groups on the vibrational and electrochemical properties of ubiquinones, J. Phys. Chem. B 101, 6607-6617.
63. Badger, R. M., and Bauer, S. H. (1937) Spectroscopic studies of the hydrogen bond. II The shift of the O-H vibrational frequency in the formation of the hydrogen bond, J. Chem. Phys. 5, 839-851.
64. B photoreduction in Rhodobacter sphaeroides reaction center mutants at Asp-L213 and Glu-L212 sites, Biochemistry 43, 7236-7243.
65. 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.
66. 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.
67. Nagle, J. F., and Tristram-Nagle, S. (1983) Hydrogen bonded chain mechanisms for proton conduction and proton pumping, J. Membr. Biol. 74, 1-14.
68. Eigen, M. (1964). Proton transfer, acid-base catalysis, and enzymatic hydrolysis, Angew. Chem., Int. Ed. Engl. 3, 1-72.