Light-harvesting complex 1 stabilizes P+QB - charge separation in reaction centers of Rhodobacter sphaeroides

Biochemistry

Volumn 43, Issue 44, 2004, Pages 14199-14210

  Francia, Francesco ^a   Dezi, Manuela ^a   Rebecchi, Alberto ^a   Mallardi, Antonia ^b   Palazzo, Gerardo ^c   Melandri, Bruno Andrea ^a   Venturoli, Giovanni ^a,d  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF BARI   (Italy)

^d INFM   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CONCENTRATION (PROCESS); LIGHT; PHOTOSYNTHESIS; PURIFICATION; REACTION KINETICS;

CHARGE RECOMBINATION; LIGHT EXCITATION; LIGHT HARVESTING;

BACTERIA;

1,4 BENZOQUINONE; CYTOCHROME C; PROTEIN REACTION CENTER LIGHT HARVESTING COMPLEX 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UBIDECARENONE; UNCLASSIFIED DRUG;

AEROBIC CAPACITY; ANTENNA; ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; CHEMICAL REACTION KINETICS; COMPLEX FORMATION; ELECTRON TRANSPORT; ENERGY RESOURCE; LASER; NONHUMAN; PHOTOOXIDATION; PHOTOSYNTHESIS; PHOTOTROPHIC BACTERIUM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN ISOLATION; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; REACTION ANALYSIS; RHODOBACTER SPHAEROIDES; STRAIN DIFFERENCE;

BACTERIAL PROTEINS; BINDING SITES; ELECTROCHEMISTRY; ELECTRON TRANSPORT; FREE RADICALS; KINETICS; LASERS; LIGHT-HARVESTING PROTEIN COMPLEXES; PHOTOLYSIS; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; RHODOBACTER SPHAEROIDES; UBIQUINONE;

ACTINOBACTERIA (CLASS); BACTERIA (MICROORGANISMS); PHOTOBACTERIA; RHODOBACTER; RHODOBACTER SPHAEROIDES; RHODOPSEUDOMONAS; UNCULTURED ACTINOMYCETE;

EID: 8344267912     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048629s     Document Type: Article

References (69)

1. Hu, X., Damianovic, A., Ritz, T., and Schulten, K. (1998) Architecture and mechanism of the light-harvesting apparatus of purple bacteria, Proc. Natl. Acad. Sci. U.S.A. 95, 5935-5941.
2. Sundström, V., Pullerits, T., and van Grondelle, R. (1999) Photosynthetic light-harvesting: reconciling dynamics and structure of purple bacterial LH2 reveals function of photosynthetic unit, J. Phys. Chem. B 103, 2327-2346.
3. Isaacs, N. W., Cogdell, R. J., Freer, A. A., and Prince, S. M. (1995) Light-harvesting mechanisms in purple photosynthetic bacteria, Curr. Opin. Struct. Biol. 5, 794-797.
4. Walz, T., Jamieson, S. J., Bowers, C. M., Bullough, P. A., and Hunter, C. N. (1998) Projection structures of three photosynthetic complexes from Rhodobacter sphaeroides: LH2 at 6 Å, LH1 and RC-LH1 at 25 Å, J. Mol. Biol. 282, 833-845.
5. Farchaus, J. W., Barz, W. P., Grünberg, H., and Oesterhelt, D. (1992) Studies on the expression of the PufX polypeptide and its requirement for photoheterotrophic growth in Rhodobacter sphaeroides, EMBO J. 11, 2779-2788.
6. McGlynn, P., Hunter, C. N., and Jones, M. R. (1994) The Rhodobacter sphaeroides PufX protein is not required for photosynthetic competence in the absence of a light harvesting system, FEBS Lett. 349, 349-353.
7. Francia, F., Wang, J., Venturoli, G., Melandri, B. A., Barz, W. P., and Oesterhelt, D. (1999) The reaction center-LH1 antenna complex of Rhodobacter sphaeroides contains one PufX molecule which is involved in dimerization of this complex, Biochemistry 38, 6834-6845.
8. Jungas, C., Ranck, J. L., Rigaud, J. L., Joliot, P., and Vermeglio, A. (1999) Supramolecular organization of the photosynthetic apparatus of Rhodobacter sphaeroides, EMBO J. 18, 534-542.
9. Scheuring, S., Francia, F., Busselez, J., Melandri, B. A., Rigaud, J. L., and Levy, D. (2004) Structural role of PufX in the dimerization of the photosynthetic core complex of Rhodobacter sphaeroides, J. Biol. Chem. 279, 3620-3626.
10. Siebert, C. A., Qian, P., Fotiadis, D., Engel, A., Hunter, C. N., and Bullough, P. A. (2004) Molecular architecture of photosynthetic membranes in Rhodobacter sphaeroides: the role of PufX, EMBO J. 23, 690-700.
11. Feher, G., Allen, J. P., Okamura, M. Y., and Rees, D. C. (1989) Structure and function of bacterial photosynthetic reaction centres, Nature 339, 111-116.
12. Crofts, A. R., and Wraight, C. A. (1983) The electrochemical domain of photosynthesis, Biochim. Biophys. Acta 726, 149-185.
13. 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.
14. Allen, J. P., Feher, G., Yeates, T. O., Rees, D. C., Deisenhofer, J., Michel, H., and Huber, R. (1986) Structural homology of reaction centers from Rhodopseudomonas sphaeroides and Rhodopseudomonas viridis as determined by X-ray diffraction, Proc. Natl. Acad. Sci. U.S.A. 83, 8589-8593.
15. 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.
16. 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.
17. 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.
18. 1 complex, Biochemistry 34, 15248-15258.
19. -, Biochim. Biophys. Acta 766, 126-140.
20. Arata, H. (1985) Free-energy change accompanying the reduction of the reaction center secondary quinone in Rhodopseudomonas sphaeroides chromatophores, Biochim. Biophys. Acta 809, 284-287.
21. 2 from Rhodopseudomonas sphaeroides: in vivo and solution studies, FEBS Lett. 105, 137-142.
22. 2 to the primary donor of Rhodobacter spaheroides reaction centers. A temperature dependent study, Biochemistry 32, 13245-13253.
23. Roszak, A. W., Howard, T. D., Southall, J., Gardiner, A. T., Law, C. J., Isaacs, N. W., and Cogdell, R. J. (2003) Crystal structure of the RC-LH1 core complex from Rhodopseudomonas palustris, Science 302, 1969-1972.
24. - reaction in isolated reaction centers from the photosynthetic bacterium Rhodopseudomonas sphaeroides, Biochim. Biophys. Acta 764, 46-54.
25. Palazzo, G., Mallardi, A., Giustini, M., Berti, D., and Venturoli, G. (2000) Cumulant analysis of charge recombination kinetics in bacterial reaction centers reconstituted into lipid vesicles, Biophys. J. 79, 1171-1179.
26. Shinkarev, V. P., and Wraight, C. A. (1997) The interaction of quinone and detergent with reaction centers of purple bacteria. I. Slow quinone exchange between reaction center micelles and pure detergent micelles, Biophys. J. 72, 2304-2319.
27. Mallardi, A., Palazzo, G., and Venturoli, G. (1997) Binding of ubiquinone to photosynthetic reaction center: determination of enthalpy and entropy changes of the binding process in reverse micelles, J. Phys. Chem. B 101, 7850-7857.
28. Baccarini-Melandri, A., and Melandri, B. A. (1971) Partial resolution of the photophosphorylating system of Rhodopseudomonas capsulata, Methods Enzymol. 23, 556-561.
29. Gray, K. A., Farchaus, J. W., Wachtveitl, J., Breton, J., and Oesterhelt, D. (1990) Initial characterization of site-directed mutants of tyrosine M210 in the reaction centre of Rhodobacter sphaeroides, EMBO J. 9, 2061-2070.
30. Piazza, R., Pierno, M., Vignati, E., Venturoli, G., Francia, F., Mallardi, A., and Palazzo, G. (2003) Liquid - liquid phase separation of a surfactant-solubilized membrane protein, Phys. Rev. Lett. 90, 208101.
31. Bartsch, R. G. (1971) Cytochromes: bacterial, Methods Enzymol. 23, 344-363.
32. Palazzo, G., Mallardi, A., Francia, F., Dezi, M., Venturoli, G., Pierno, M., Vignati, E., and Piazza, R. (2004) Spontaneous emulsification of detergent solubilized reaction center: protein conformational changes precede droplet growth, Phys. Chem. Chem. Phys. 6, 1439-1445.
33. 2 oxidoreductase complex in chromatophores from Rhodobacter sphaeroides, Biochim. Biophys. Acta 851, 340-352.
34. Straley, S. C., Parson, W. W., Mauzerall, D. C., and Clayton, R. K. (1973) Pigment content and molar extinction coefficients of photochemical reaction centers from Rhodopseudomonas sphaeroides, Biochim. Biophys. Acta 305, 597-609.
35. 2 and reaction center of Rhodospeudomonas spheroides Ga membranes. Extinction coefficients, content, half-reduction potentials, kinetics and electric field alterations, Biochim. Biophys. Acta 387, 536-556.
36. Bowyer, J. R., Meinhardt, S. W., Tierney, G. V., and Crofts, A. R. (1981) Resolved difference spectra of redox centers involved in photosynthetic electron flow in Rhodopseudomonas capsulata and Rhodopseudomonas sphaeroides, Biochim. Biophys. Acta 635, 167-186.
37. B electron transfer in bacterial reaction centers embedded in trehalose amorphous matrices, Biophys. J. 85, 2760-2775.
38. Clayton, R. K. (1966) Spectroscopic analysis of bacteriochlorophylls in vitro and in vivo, Photochem. Photobiol. 5, 669-677.
39. McDermott, G., Prince, S. M., Freer, A. A., Hawthornthwaite-Lawless, A. M., Papiz, M. Z., Cogdell, R. J., and Isaacs, N. W. (1995) Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria, Nature 374, 517-521.
40. Vermeglio, A. (1977) Secondary electron transfer in reaction centers of Rhodopseudomonas sphaeroides. Out-of-phase periodicity of two for the formation of ubisemiquinone and fully reduced ubiquinone, Biochim. Biophys. Acta 459, 516-524.
41. Wraight, C. A. (1977) Electron acceptors of photosynthetic bacterial reaction centers. Direct observation of oscillatory behaviour suggesting two closely equivalent ubiquinones, Biochim. Biophys. Acta 459, 525-531.
42. Palazzo, G., Mallardi, A., Hochkoeppler, A., Cordone, L., and Venturoli, G. (2002) Electron transfer kinetics in photosynthetic reaction centers embedded in trehalose glasses: trapping of conformational substates at room temperature, Biophys. J. 82, 558-568.
43. Kleinfeld, D., Okamura, M. Y., and Feher, G. (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.
44. Wraight, C. A., Cogdell, R. J., and Clayton, R. K. (1975) Some experiments on the primary electron acceptor in reaction centres from Rhodopseudomonas spaheroides, Biochim. Biophys. Acta 396, 242-249.
45. Shinkarev, V. P., and Wraight, C. A. (1993) Electron and proton transfer in the acceptor quinone complex of reaction centers of phototrophic bacteria, in The Photosynthetic Reaction Center (Deisenhofer, J., and Norris, J. R., Eds.) Vol. 1, pp 193-255, Academic Press, San Diego.
46. Okamura, M. Y., Isaacson, R. A., and Feher, G. (1975) Primary acceptor in bacterial photosynthesis: obligatory role of ubiquinone in photoactive reaction centers of Rhodopseudomonas spheroides, Proc. Natl. Acad. Sci. U.S.A. 72, 3491-3495.
47. Okamura, M. Y., Debus, R. J., Kleinfeld, D., and Feher, G. (1982) Quinone binding sites in reaction centers from photosynthetic bacteria, in Functions of Quinones in Energy Conserving Systems (Trumpower, B. L., Ed.) pp 299-317, Academic Press, New York.
48. Garcia, A. F., Venturoli, G., Gad'on, N., Fernández-Velasco, J. G., Melandri, B. A., and Drews, G. (1987) The adaptation of the electron transfer chain of Rhodopseudomonas capsulata to different light intensities, Biochim. Biophys. Acta 890, 335-345.
49. Takamiya, K.-I., and Dutton, P. L. (1979) Ubiquinone in Rhodopseudomonas sphaeroides. Some thermodynamic properties, Biochim. Biophys. Acta 546, 1-6.
50. 2 oxidoreductase act as independent enzymes in Rps. sphaeroides, J. Bioenerg. Biomembr. 18, 437-445.
51. Crofts, A. R., Meinhardt, S. W., Jones, K. R., and Snozzi, M. (1983) The role of the quinone pool in the cyclic electron transfer chain of Rps. sphaeroides: a modified Q-cycle mechanism, Biochim. Biophys. Acta 723, 202-218.
52. 2 oxidoreductase, and is delocalized, Biochem. Soc. Trans. 19, 588-593.
53. 1 complex, Biochim. Biophys. Acta 975, 336-345.
54. Lavergne, J., Joliot, P., and Vermeglio, A. (1989) Partial equilibration of photosynthetic carriers under weak illumination: a theoretical and experimental study, Biochim. Biophys. Acta 975, 347-355.
55. Lavergne, J., and Joliot, P. (1991) Restricted diffusion in photosynthetic membranes, Trends Biochem. Sci. 16, 129-134.
56. 2 photo-oxidation reflects the subcellular distribution of reaction centers in Rps. sphaeroides Ga cells, Biochim. Biophys. Acta 1183, 352-360.
57. 1 complex in Rhodobacter sphaeroides chromatophores under oxidizing conditions, FEBS Lett. 245, 43-46.
58. Crofts, A., Guergove-Kuras, M., and Hong, S. (1998) Chromatophores heterogeneity explains phenomena seen in Rhodobacter sphaeroides previously attributed to supercomplexes, Photosynth. Res. 55, 357-362.
59. Crofts, A. R. (2000) Photosynthesis in Rhodobacter sphaeroides, Trends Microbiol. 8, 105.
60. Vermeglio, A., and Joliot, P. (2000) Response from Vermeglio and Joliot, Trends Microbiol. 8, 106.
61. Crofts, A. R. (2000) Response from Crofts, Trends Microbiol. 8, 107-108.
62. Roth, M., Arnoux, B., Ducruix, A., and Reiss-Husson, F. (1991) Structure of the detergent phase and protein-detergent interactions in crystals of the wild-type (strain Y) Rhodobacter sphaeroides photochemical reaction center, Biochemistry 30, 9403-9413.
63. Roth, M., Lewit-Bentley, A., Michel, H., Deisenhofer, J., Huber, R., and Oesterhelt, D. (1989) Detergent structure in crystals of a bacterial photosynthetic reaction center, Nature 340, 659-661.
64. Gast, P., Hemelrijk, P., and Hoff, A. J. (1994) Determination of the number of detergent molecules associated with the reaction center protein isolated from the photosynthetic bacterium Rhodopseudomonas viridis. Effect of the amphiphilic molecule 1,2,3-heptanetriol, FEBS Lett. 337, 39-42.
65. McAuley, K. E., Fyfe, P. K., Ridge, J. P., Isaacs, N. W., Cogdell, R. J., and Jones, M. R. (1999) Structural details of an interaction between cardiolipin and an intergral membrane protein, Proc. Natl. Acad. Sci. U.S.A. 96, 14706-14711.
66. Fyfe, P. K., McAuley, K. E., Roszak, A. W., Isaacs, N. W., Cogdell, R. J., and Jones, R. J. (2001) Probing the interface between membrane proteins and membrane lipids by X-ray crystallography, Trends Biochem. Sci. 26, 106-112.
67. Camara-Artigas, A., Brune, D., and Allen, J. P. (2002) Interactions between lipids and bacterial reaction centers determined by protein crystallography, Proc. Natl. Acad. Sci. U.S.A. 99, 11055-11060.
68. Schmid, R., and Labahn, A. (2000) Temperature and free energy dependence of the direct charge recombination rate from the secondary quinone in bacterial reaction centers from Rhodobacter sphaeroides, J. Phys. Chem. B 104, 2928-2936.
69. Allen, J. P., Williams, J. C., Graige, M. S., Paddock, M. L., Feher, G., and Okamura, M. Y. (1998) Free energy dependence of the direct charge recombination from the primary and secondary quinones in reaction centers from Rhodobacter sphaeroides, Photosynth. Res. 55, 227-233.