Protein/lipid interaction in the bacterial photosynthetic reaction center: Phosphatidylcholine and phosphatidylglycerol modify the free energy levels of the quinones

Biochemistry

Volumn 43, Issue 40, 2004, Pages 12913-12923

  Nagy, László ^a   Milano, Francesco ^b   Dorogi, Márta ^a   Agostiano, Angela ^c   Laczkó, Gábor ^a   Szebényi, Kornélia ^a   Váró, György ^d   Trotta, Massimo ^b   Maróti, Péter ^a  

^a UNIVERSITY OF SZEGED   (Hungary)

^b CNR   (Italy)

^c UNIVERSITY OF BARI   (Italy)

^d INSTITUTE OF BIOCHEMISTRY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; DETERGENTS; FREE ENERGY; LIPIDS; MICELLES; PH EFFECTS; PROTEINS; REDOX REACTIONS;

ELECTRON TRANSFER; LIPID MEMBRANES; PHOTOSYNTHETIC REACTION; RHODOBACTER SPHAEROIDES;

PHOTOSYNTHESIS;

CARDIOLIPIN; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLGLYCEROL; QUINONE DERIVATIVE;

ARTICLE; CELL VACUOLE; ELECTRON TRANSPORT; ENERGY TRANSFER; HYDROGEN BOND; LIPID BILAYER; LUMINESCENCE; MICELLE; NONHUMAN; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; RHODOBACTER SPHAEROIDES;

AMINO ACIDS; CYTOCHROMES; ELECTRON TRANSPORT; KINETICS; LIPID BILAYERS; MEMBRANES, ARTIFICIAL; MOLECULAR CONFORMATION; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLGLYCEROLS; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PROTEINS; QUINONES; RHODOBACTER SPHAEROIDES; SPECTRUM ANALYSIS; THERMODYNAMICS; WATER;

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

EID: 4944251055     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0489356     Document Type: Article

References (84)

1. Sebban, P., Maróti, P., and Hanson, D. K. (1995) Electron and proton transfer to the quinones in bacterial photosynthetic reaction centers: Insight from combined approaches of molecular genetics and biophysics, Biochimie 77, 677-694.
2. Allen, J. P., and Williams, J. C. (1998) Photosynthetic reaction centers, FEBS Lett. 438, 5-9.
3. 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.
4. Paddock, M. L., Feher, G., and Okamura, M. Y. (2003) Proton transfer pathways and mechanism in bacterial reaction centers, FEBS Lett. 555, 45-50.
5. Wraight, C. A. (2004) Proton and electron transfer in the acceptor quinone complex of photosynthetic reaction centers from Rhodobacter sphaeroides, Frontiers Biosci. 9, 309-337.
6. Wraight, C. A., and Clayton, R. (1974) The absolute quantum efficiency of bacteriochlorophyll photooxidation in reaction centers of Rhodopseudomonas sphaeroides, Biochim. Biophys. Acta 333, 246-260.
7. 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.
8. Muh, F., Rautter, J., and Lubitz, W. (1997) Two distinct conformations of the primary electron donor in reaction centers from Rhodobacter sphaeroides revealed by ENDOR/TRIPLE-spectroscopy, Biochemistry 36, 4155-4162.
9. B leaves the reaction center, Biochim. Biophys. Acta 1016, 289-292.
10. Fathir, I., Mori, T., Nogi, T., Kobayashi, M., Miki, K., and Nozawa, T. (2001) Structure of the H subunit of the photosynthetic reaction center from the thermophilic purple bacterium, Thermochromatium tepidum - Implications for the specific binding of the lipid molecule to the membrane protein complex, Eur. J. Biochem. 268, 2652-2657.
11. McAuley, K. E., Fyfe, P. K., Ridge, J. P., Isaacs, N. W., Cogdell, R. J., and Jones, M. R. (1999) Structural details of interaction between cardiolipin and an integral membrane protein, Proc. Natl. Acad. Sci. U.S.A. 96, 14706-14711.
12. Ermler, U., Fritzsch, G., Buchanan, S. K., and Michel, H. (1994) Structure of the photosynthetic reaction-center from Rhodobacter-sphaeroides at 2.65 Å resolution-cofactors and protein-cofactor interactions, Structure 2, 925-936.
13. 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.
14. Stowell, M. H. B., McPhillips, T. M., Rees, D. C., Soltis, S. M., Abresh, E., and Feher, G. (1997) Light induced structural changes in photosynthetic reaction center: implications for mechanism of electron-proton transfer, Science 276, 812-816.
15. Tiede, D. M., Vázquez, J., Córdova, J., and Marone, P. (1996) Time-resolved electrochromism associated with the formation of quinone anions in the Rhodobacter sphaeroides R26 reaction center, Biochemistry 35, 10763-10775.
16. B, Biochemistry 38, 4542-4552.
17. - recombination kinetics in reaction centers from Rhodopseudomonas viridis: the effects of pH and temperature, Biochim. Biophys. Acta 974, 54-65.
18. Nagy, L., Fodor, E., Tandori, J., Rinyu, L., and Farkas, T. (1999) Lipids affect the charge stabilization in wild type and mutant reaction centers of Rhodobacter sphaeroides, Aust. J. Plant Physiol. 25, 465-473.
19. Taly, A., Baciou, L., and Sebban, P. (2002) The DMPC lipid phase transition influences differently the first and the second electron transfer reactions in bacterial reaction centers, FEBS Lett. 532, 91-96.
20. Donohue, T. J., Cain, B. D., and Kaplan, S. (1982) Alteration in the phospholipid composition of Rhodopseudomonas sphaeroides and other bacteria induced by Tris, J. Bacteriol. 152, 595-606.
21. Wood, B. J. B., Nichols, B. W., and James, A. T. (1965) The lipids and fatty acid metabolism of photosynthetic bacteria, Biochim. Biophys. Acta 106, 261-273.
22. Steiner, S., Sojka, G. A., Conti, S. F., Gest, H., and Lester, R. L. (1970) Modification of membrane composition in growing photosynthetic bacteria, Biochim. Biophys. Acta 203, 571-574.
23. Onishi, J. C., and Niederman, R. (1982) Rhodopseudomonas sphaeroides membranes: Alterations in phospholipid composition in aerobically and phototrophically grown cells, J. Bacteriol. 149, 831-839.
24. Fyfe, P. K., Isaacs, N. W., Cogdell, R., and Jones, M. (2004) Disruption of a specific molecular interaction with a bound lipid affects the thermal stability of the purple bacterial reaction centre, Biochim. Biophys. Acta 1608, 11-22.
25. Sebban, P., Parot, P., Baciou, L., Mathis, P., and Verméglio, A. (1991) Effects of low temperature and lipid rigidity on the charge recombination process in Rps. viridis and Rb. sphaeroides reaction centers, Biochim. Biophys. Acta 1057, 109-114.
26. 2 by bacterial photosynthetic reaction centers in phospholipid vesicles: 1. Studies with natural membranes, Biochemistry 19, 3322-3327.
27. 2 by bacterial photosynthetic reaction centers in phospholipid vesicles: 2. Studies with negative membranes, Biochemistry 19, 3328-3334.
28. Linscheid, M. L., Diehl, B. W., Övermöhle, M., Riedl, I., and Heinz, E. (1997) Membrane lipids of Rhodopseudomonas viridis, Biochim. Biophys. Acta 1347, 151-163.
29. B, Structure 5, 1339-1359.
30. Agostiano, A., Milano, F., and Trotta, M. (1999) Investigation on the detergent role in the function of secondary quinone in bacterial reaction centers, Eur. J. Biochem. 262, 358-364.
31. Wakeham, M. C., Sessions, R. B., Jones, M. R., and Fyfe, P. K. (2001) Is there conserved interaction between cardiolipin and the type II bacterial reaction center, Biophys. J. 80, 1395-1405.
32. Camara-Artigas, A., Brune, D., and Allen, J. (2002) Interactions between lipids and bacterial reaction centers determined by protein crystallography, Proc. Natl. Acad. Sci. U.S.A. 99, 11055-11060.
33. Nogi, T., Fathir, I., Kobayashi, M., Nozawa, T., and Miki, K. (2000) Crystal structures of photosynthetic reaction centers and high potential iron-sulfur protein from Thermochromatium tepidum; thermostability and electron transfer, Proc. Natl. Acad. Sci. U.S.A. 97, 13561-13566.
34. Kruse, O., and Schmid, G. H. (1995) The role of phosphatidyl-glycerol as a functional effector and membrane anchor of the D1-core peptide from photosystem II-particles of the cyanobacterium Oscillatoria chalybea, Z. Naturforsch. 50c, 380-390.
35. Hagio, M., Gombos, Z., Várkonyi, Zs., Masamoto, K., Sato, N., Tsuzuki, M., and Wada, H. (2000) Direct evidence for requirement of phosphatidylglycerol in photosystem II of photosynthesis, Plant Physiol. 124, 795-804.
36. Sato, N., Hagio, M., Wada, H., and Tsuzuki, M. (2000) Requirement of phosphatidylglycerol for photosynthetic function in thylakoid membranes, Proc. Natl. Acad. Sci. U.S.A. 97, 10655-10660.
37. B in the photosystem II reaction center, Biochemistry 41, 3796-3802.
38. Aro, E. M., Virgin, L., and Andersson, B. (1993) Photoinhibition of photosystem-2-inactivation, protein damage and turnover, Biochim. Biophys. Acta 1143, 113-134.
39. -. in bacterial reaction centers of Rhodobacter sphaeroides determined by driving force assay, Proc. Natl. Acad. Sci. U.S.A. 95, 11679-11684.
40. B in bacterial photosynthetic reaction centers, Biochemistry 43, 3318-3326.
41. Baxter, R. H. G., Ponomarenko, N., Srajer, V., Pahl, R., Moffat, K., and Norris, J. R. (2004) Time-resolved crystallographic studies of light-induced structural changes in the photosynthetic reaction center, Proc. Natl. Acad. Sci. U.S.A. 101, 5982-5987.
42. Kuglstatter, A., Ermler, U., Michel, H., Baciou, L., and Fritsch, 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.
43. Ormerod, J. G., Ormerod, K. S., and Gest, H. (1961) Light-dependent utilization of organic compounds and photoproduction of molecular hydrogen by photosynthetic bacteria; relationships with nitrogen metabolism, Arch. Biochem. Biophys. 94, 449-463.
44. B-pocket in reaction centers of Rhodobacter sphaeroides, Photosynth. Res. 45, 135-146.
45. Ollivon, M., Lesieur, S., Grabielle-Madelmont, C., and Patemostre, M. (2000) Vesicle reconstitution from lipid-detergent mixed micelles, Biochim. Biophys. Acta 1508, 34-50.
46. Trotta, M., Milano, F., Nagy, L., and Agostiano, A. (2002) Response of membrane protein to the environment: the case of photosynthetic reaction centre, Mater. Sci. Eng., C 22, 263-267.
47. Tandori, J., Nagy, L., and Maróti, P. (1991) Semiquinone oscillation as a probe of quinone/herbicide binding in bacterial reaction centers, Photosynthetica 25, 159-166.
48. Lakatos, M., Groma, G. I., Ganea, C., Lanyi, J. K., and Váró, G. (2002) Characterization of the azide-dependent bacteriorhodopsin-like photocycle of salinarum halorhodopsin Biophys. J. 82, 1687-1695.
49. Wraight, C. A., and Stein, R. R. (1983) Redox equilibrium in the acceptor quinone complex of isolated reaction centers and the mode of action of orthophenantroline, FEBS Lett. 113, 73-77.
50. -, Biochim. Biophys. Acta 766, 126-140.
51. Halmschlager, A., Tandori, J., Trotta, M., Rinyu, L., Pfeiffer, I., and Nagy, L. (2002) A mathematical model for the quinone-herbicide competition in the reaction centers of Rhodobacter sphaeroides, Funct. Plant Biol. 29, 1-7.
52. Turzo, K., Laczkó, G., Filus, Z., and Maróti, P. (2000) Quinone-dependent delayed fluorescence from the reaction center of photosynthetic bacteria, Biophys. J. 79, 14-25.
53. Tiede, D. M., Utschig, L., Hanson, D. K., and Gallo, D. M. (1998) Resolution of electron and proton transfer events in the electrochromism associated with quinone reduction in bacterial reaction centers, Photosynth. Res. 55, 267-273.
54. 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 sphaeroides, Proc. Natl. Acad. Sci. U.S.A. 72, 3491-3495.
55. Rinyu, L., Martin, E., Takahashi, E., Maróti, P., and Wraight, C. (2004) Modulation of the free energy of the primary quinone acceptor (QA) in reaction centers from Rhodobacter sphaeroides: contributions from the protein and protein-lipid (cardiolipin) Interaction, Biochim. Biophys. Acta 1655, 93-101.
56. Arata, H., and Parson, W. (1981) Delayed fluorescence from Rhodopseudomonas sphaeroides reaction centers; Enthalpy and free energy changes accompanying electron transfer from P-870 to quinones, Biochim. Biophys. Acta 638, 201-209.
57. Kleinfeld, D., Abresch, E. C., Okamura, M. Y., and Feher, G. (1984) Damping oscillations in the semiquinone absorption in reaction centers after successive flashes, Biochim. Biophys. Acta 756, 406-409.
58. Verkhovskii, M. I., Kaurov, B. S., Rubin, A. B., and Shinkarev, V. P. (1981) Kinetics of conversion of ubisemiquinone in primary reactions of bacterial photosynthesis, Mol. Biol. (Moscow) 15, 589-600.
59. Shinkarev, V. P., Verkhovskii, M. I., Kaurov, B. S., and Rubin, A. B. (1981) The kinetic model of two electron gate in photosynthetic reaction center of bacteria, Mol. Biol. (Moscow) 15, 743-844.
60. Maróti, P. (1991) Electron transfer and proton uptake of photosynthetic bacterial reaction centers reconstituted in phospholipid vesicles, J. Photochem. Photobiol., B 8, 263-277.
61. Palazzo, G., Mallardi, A., Giustini, M., Berti, D., and Venturolli, G. (2000) Cumulant analysis of charge recombination kinetics in bacterial reaction centers reconstituted into lipid vesicles, Biophys. J. 79, 1171-1179.
62. B site of reaction centers from the purple bacteria Rhodobacter sphaeroides reconstituted in liposomes, Eur. J. Biochem. 270, 4595-4605.
63. Wraight, C. A. (1981) Oxidation-reduction physical chemistry of the acceptor quinone complex in bacterial reaction centres: evidence for a new model of herbicide activity, Isr. J. Chem. 21, 348-354.
64. Dutton, P. L., Leigh, J. S., and Wraight, C. A. (1973) Direct measurement of the midpoint potential of the primary electron acceptor in Rhodopseudomonas sphaeroides in situ and in the isolated state: some relationships with pH and o-phenantroline, FEBS Lett. 36, 169-173.
65. Fritzsch, G., Koepke, J., Diem, R., Kuglstatter, A., and Baciou, L. (2002) Charge separation induces conformational changes in the photosynthetic reaction center of purple bacteria, Acta Crystallogr., Sect. D: Biol. Crystallogr. 58, 1661-1663.
66. Mauzerall, D. C., Gunner, M. R., and Zhang, J. W. (1995) Volume contraction on photoexcitation of the reaction center from Rhodobacter sphaeroides R-26: Internal probe of dielectrics, Biophys. J. 68, 275-280.
67. Brumfeld, V., Nagy, L., Kiss, V., and Malkin, S. (1999) Wide-frequency hydrophone detection of laser-induced photoacoustic signals in photosynthesis, Photochem. Photobiol. 70, 607-615.
68. Nagy, L., Kiss, V., Brumfeld, V., and Malkin, S. (2001) Thermal and structural changes of photosynthetic reaction centers characterized by photoacoustic detection with a broad frequency band hydrophone, Photochem. Photobiol. 74, 81-87.
69. Kálmán, L., and Maróti, P. (1997) Conformation-activated protonation in reaction centers of the photosynthetic bacterium Rhodobacter sphaeroides, Biochemistry 36, 15269-15276.
70. 2+-substituted reaction centers from Rhodobacter sphaeroides, Biochim. Biophys. Acta 1607, 45-52.
71. Filus, Z., Laczkó, G., Wraight, C. A., and Maróti, P. (2004) Delayed fluorescence from photosynthetic reaction center measured by electronic gating of the photomultiplier, Biopolymers 74, 92-95.
72. McMahon, B. H., Müller, J. D., Wraight, C. A., and Nienhaus, G. U. (1998) Electron transfer and protein dynamics in the photosynthetic reaction center, Biophys. J. 74, 2567-2587.
73. - state, Biochim. Biophys. Acta 1319, 242-250.
74. Shopes, R. J., and Wraight, C. A. (1985) The acceptor quinone complex of Rhodopseudomonas viridis reaction centers, Biochim. Biophys. Acta 806, 348-356.
75. Sebban, P., Maróti, P., Schiffer, M., and Hanson, D. (1995) Electrostatic dominoes: Long distance propagation of mutational effects in photosynthetic reaction centers of Rhodobacter capsulatus, Biochemistry 34, 8390-8397.
76. - and the associated processes in Rhodobacter sphaeroides reaction centers, Biochemistry 37, 2818-2829.
77. Remy, A., and Klaus, G. (2003) Coupling of light-induced electron transfer to proton uptake in photosynthesis, Nat. Struct. Biol. 10, 637-644.
78. Yeates, T. O., Komiya, H., Rees, D. C., Allen, J. P., and Feher, G. (1987) Structure of the reaction center from Rhodobacter sphaeroides R-26: Membrane-protein interaction, Proc. Natl. Acad. Sci. U.S.A. 84, 6438-6442.
79. Graige, M. S., Paddock, M. L., Feher, G., and Okamura, M. Y. (1999) Observation of the protonated semiquinone intermediate in isolated reaction centers from Rhodobacter sphaeroides: Implications for the mechanism of electron and proton transfer in proteins, Biochemistry 38, 11465-11473.
80. Katona, G., Andreasson, U., Landau, E. M., Andreasson, L. E., and Neutze, R. (2003) Lipidic cubic phase crystal structure of the photosynthetic reaction centre from Rhodobacter sphaeroides at 2.35 angstrom resolution, J. Mol. Biol. 331, 681-692.
81. Yosikawa, S., Shinzawa-Itoh, K., and Tsukihara, T. (1998) Crystal structure of bovine heart cytochrome c oxidase at 2.8 Å resolution, J. Bioenerg. Biomembr. 30, 7-14.
82. Domonkos, I., Malec, P., Sallai, A., Kovács, L., Itoh, K., Shen, G., Ughy, B., Bogos, B., Sakurai, B., Strzalka, K., Wada, H., Itoh, S., Farkas, T., and Gombos, Z., (2004) Phosphatidylglycerol is essential for oligomerization of photosystem I reaction center, Plant Physiol. 134, 1471-1478.
83. Kruse, O., Hankamer, B., Konczak, C., Gerle, C., Morris, E., Radunz, A., Schmid, G. H., and Barber, J. (2000) Phosphatidyl-glycerol is involved in the dimerization of photosystem II, J. Biol. Chem. 275, 6509-6514.
84. Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J., and Iwata, S. (2004) Architecture of the photosynthetic oxygen-evolving center, Science 303, 1831-1838.