Residual water modulates QA--to-QB electron transfer in bacterial reaction centers embedded in trehalose amorphous matrices

Biophysical Journal

Volumn 85, Issue 4, 2003, Pages 2760-2775

  Francia, Francesco ^a   Palazzo, Gerardo ^b,c   Mallardi, Antonia ^d   Cordone, Lorenzo ^e   Venturoli, Giovanni ^a,e  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF BARI   (Italy)

^c UNIVERSITY OF MOLISE   (Italy)

^d CNR   (Italy)

^e INFM   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

TREHALOSE;

ANALYTIC METHOD; ARTICLE; BACTERIAL MEMBRANE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ELECTRON TRANSPORT; EXTRACELLULAR MATRIX; INFRARED RADIATION; MOLECULAR DYNAMICS; NONHUMAN; PHOTOSYNTHESIS; RHODOBACTER SPHAEROIDES; ROOM TEMPERATURE; WATER TRANSPORT;

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

EID: 0141530934     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74698-0     Document Type: Article

References (77)

1. Ambrosone, L., A. Mallardi, G. Palazzo, and G. Venturoli. 2002. Effect of heterogeneity in the distribution of ligands and proteins among disconnected particles: the binding of ubiquinone to the bacterial reaction center. Phys. Chem. Chem. Phys. 4:3071-3077.
2. Arata, H., and W. W. Parson. 1981. Enthalpy and volume changes accompanying electron transfer from P-870 to quinones in Rhodopseudomonas sphaeroides reaction centers. Biochim. Biophys. Acta. 636:70-81.
3. Austin, R. H., K. W. Beeson, L. Eisenstein, H. Frauenfelder, and I. C. Gunsalus. 1975. Dynamics of ligand binding to myoglobin. Biochemistry. 14:5355-5373.
4. B. Biochemistry. 34:7967-7972.
5. Balabin, I. A., and J. N. Onuchic. 2000. Dynamically controlled protein tunneling paths in photosynthetic reaction centers. Science. 290:114-117.
6. Barron, L. D., L. Hecht, and G. Wilson. 1997. The lubricant of life: a proposal that solvent water promotes extremely fast conformational fluctuations in mobile heteropolypeptide structure. Biochemistry. 36:13143-13147.
7. Beechem, J. M. 1992. Global analysis of biochemical and biophysical data. Methods Enzymol. 20:37-54.
8. Bevington, P. R. 1969. Data Reduction and Error Analysis for the Physical Sciences. McGraw-Hill, New York.
9. 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.
10. Brzezinski, P., and L.-E. Andreasson. 1995. Trypsin treatment of reaction centers from Rhodobacter sphaeroides in the dark and under illumination: protein structural changes follow charge separation. Biochemistry. 34:7498-7506.
11. Careri, G. 1992. Proton percolation and emergence of function in nearly dry biosystems. Nanobiology. 1:117-126.
12. Cherepanov, D. A., L. I. Krishtalik, and A. Y. Mulkidjanian. 2001. Photosynthetic electron transfer controlled by protein relaxation: analysis by Langevin stochastic approach. Biophys. J. 80:1033-1049.
13. Cordone, L., P. Galajada, E. Vitrano, A. Gassmann, A. Ostermann, and F. Parak. 1998. A reduction of protein-specific motions in co-ligated myoglobin embedded in a trehalose glass. Eur. Biophys. J. 27:173-176.
14. Cordone, L., M. Ferrand, E. Vitrano, and G. Zaccai. 1999. Harmonic behavior of trehalose-coated carbon-monoxy-myoglobin at high temperature. Biophys. J. 76:1043-1047.
15. Cottone, G., L. Cordone, and G. Ciccotti. 2001. Molecular dynamics simulation of carboxy-myoglobin embedded in a trehalose-water matrix. Biophys. J. 80:931-938.
16. Cottone, G., G. Ciccotti, and L. Cordone. 2002. Protein-trehalose-water structures in trehalose coated carboxy-myoglobin. J. Chem. Phys. 117:9862-9866.
17. Crowe, L. M., D. S. Reid, and J. H. Crowe. 1996. Is trehalose special for preserving biomaterials? Biophys. J. 71:2087-2093.
18. Davidson, V. L. 1996. Unravelling the kinetic complexity of interprotein electron transfer reactions. Biochemistry. 45:14035-14039.
19. - from excited reaction centers of Rhodobacter sphaeroides. J. Am. Chem. Soc. 122:1479-1485.
20. Feher, G., and M. Y. Okamura. 1978. Chemical composition and properties of reaction centers. In The Photosynthetic Bacteria. R. K. Clayton, and W. R. Sistrom, editors. Plenum Press, New York. pp.349-386.
21. Feher, G., M. Okamura, and D. Kleinfeld. 1987. Electron transfer reactions in bacterial photosynthesis: charge recombination kinetics as a structure probe. In Protein Structure. Molecular and Electronic Reactivity. R. Austin, E. Buhks, B. Chance, D. De Vault, P. L. Dutton, H. Frauenfelder, and V. I. Goldanskii, editors. Springer-Verlag, New York. pp.399-421.
22. Feher, G., J. P. Allen, M. Y. Okamura, and D. C. Rees. 1989. Structure and function of bacterial photosynthetic reaction centres. Nature. 33:111-116.
23. Frauenfelder, H., F. Parak, and R. D. Young. 1988. Conformational substates in proteins. Annu. Rev. Biophys. Biophys. Chem. 17:451-479.
24. Frauenfelder, H., S. G. Sligar, and P. G. Wolynes. 1991. The energy landscapes and motions of proteins. Science. 254:1598-1603.
25. Frauenfelder, H., and P. G. Wolynes. 1994. Biomolecules: where the physics of complexity and simplicity meet. Phys. Today. 47:58-64.
26. Frauenfelder, H., and B. McMahon. 1998. Dynamics and function of proteins: the search for general concepts. Proc. Natl. Acad. Sci. USA. 95:4795-4797.
27. Gottfried, D. S., E. S. Peterson, A. G. Sheikh, J. Wang, M. Yang, and J. M. Friedman. 1996. Evidence for damped hemoglobin dynamics in a room temperature trehalose glass. J. Phys. Chem. 100:12034-12042.
28. - in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay. Proc. Natl. Acad. Sci. USA. 95:11679-11684.
29. Gray, K. A., J. W. Farchaus, J. Wachtveitl, J. Breton, and D. Oesterhelt. 1990. Initial characterization of site-directed mutants of tyrosine M210 in the reaction centre of Rhodobacter sphaeroides. EMBO J. 9:2061-2070.
30. Gunner, M. R. 1991. The reaction center protein from purple bacteria: structure and function. Curr. Topics Bioenerg. 16:319-367.
31. Hagen, S. J., J. Hofrichter, and W. A. Eaton. 1995. Protein reaction kinetics in a room-temperature glass. Science. 269:959-962.
32. Hagen, S. J., J. Hofrichter, and W. A. Eaton. 1996. Geminate rebinding and conformational dynamics of myoglobin embedded in a glass at room temperature. J. Phys. Chem. 100:12008-12021.
33. Hoffman, B. M., and M. A. Ratner. 1987. Gated electron transfer: when are observed rates controlled by conformational interconversion? J. Am. Chem. Soc. 109:6237-6242.
34. Holzwarth, A. R. 1996. Data analysis of time-resolved measurements. In Biophysical Techniques in Photosynthesis. J. Amesz, and A. J. Hoff, editors. Kluwer Academic Publishers, Dordrecht, The Netherlands. pp.75-92.
35. 1 complex. Biophys. J. 77:1753-1768.
36. Kalman, L., and P. Maroti. 1997. Conformation-activated protonation in reaction centers of the photosynthetic bacterium Rhodobacter sphaeroides. Biochemistry. 36:15269-15276.
37. Kirmaier, C., D. Holten, and W. W. Parson. 1985. Temperature and detection-wavelength dependence of the picosecond electron transfer kinetics measured in Rhodopseudomonas sphaeroides reaction centers. Resolution of new spectral and kinetic components in the primary charge separation process. Biochim. Biophys. Acta. 810:37-48.
38. Kleinfeld, D., M. Y. Okamura, and G. Feher. 1984a. 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.
39. -. Biochim. Biophys. Acta. 766:126-140.
40. Kotelnikov, A. I., V. R. Vogel, A. V. Pastuchov, V. L. Voskoboinikov, and E. S. Medvedev. 1998. Coupling of electron transfer and protein dynamics. In Biological Electron Transfer Chains: Genetic, Composition and mode of Operation. G. V. Canters, and E. Vijgenbom, editors. Kluwer Academic Publishers, Dordrecht, The Netherlands. pp.29-51.
41. Kuglstatter, A., U. Emler, H. Michel, L. Baciou, and G. Fritzsch. 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.
42. A site. Chem. Phys. 197:355-366.
43. Leslie, S. B., E. Israeli, B. Lighthaert, J. H. Crowe, and L. M. Crowe. 1995. Trehalose and sucrose protect both membranes and proteins in intact bacteria during drying. Appl. Environ. Microbiol. 91:3592-3597.
44. - and the associated processes in Rhodobacter sphaeroides R-26 reaction centers. Biochemistry. 37:2818-2829.
45. - in Rhodobacter sphaeroides reaction centers. Biochemistry. 39:7445-7454.
46. Librizzi, F., E. Vitrano, and L. Cordone. 1999. Inhibition of A substates interconversion in trehalose-coated carbonmonoxy-myoglobin. In Biological Physics. H. Frauenfelder, G. Hummer, and R. Garcia, editors. American Institute of Physics, Melville, New York. pp.132-138.
47. Librizzi, F., C. Viappiani, S. Abbruzzetti, and L. Cordone. 2002. Residual water modulates the dynamics of the protein and of the external matrix in "trehalose-coated" MbCO: an infrared and flash-photolysis study. J. Chem. Phys. 116:1193-1200.
48. Lieutaud, C., W. Nitschke, A. Verméglio, P. Parot, and B. Schoepp-Cothenet. 2003. HiPIP in Rubrivivax gelatinosus is firmly associated to the membrane in a conformation efficient for electron transfer towards the photosynthetic reaction centre. Biochim. Biophys. Acta. 1557:83-90.
49. Mallardi, A., G. Palazzo, and G. Venturoli. 1997. Binding of ubiquinone to photosynthetic reaction centers: determination of enthalpy and entropy changes in reverse micelles. J. Phys. Chem. B. 101:7850-7857.
50. - reaction in isolated reaction centers from the photosynthetic bacterium Rhodopseudomonas sphaeroides. Biochim. Biophys. Acta. 764:46-54.
51. Mattos, C. 2002. Protein-water interactions in a dynamic world. Trends Biochem. Sci. 27:203-208.
52. McMahon, B. H., J. D. Müller, C. A. Wraight, and G. U. Nienhaus. 1998. Electron transfer and protein dynamics in the photosynthetic reaction center. Biophys. J. 74:2567-2587.
53. Nabedryk, E., K. A. Bagley, D. L. Thibodeau, M. Bausher, W. Mäntele, and J. Breton. 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.
54. Okamura, M. Y., M. L. Paddock, M. S. Graige, and G. Feher. 2000. Proton and electron transfer in bacterial reaction centers. Biochim. Biophys. Acta. 1458:148-163.
55. Ortega, J. M., P. Mathis, J. C. Williams, and J. P. Allen. 1996. Temperature dependence of the reorganization energy for charge recombination in the reaction center from Rhodobacter sphaeroides. Biochemistry. 35:3354-3361.
56. Paddock, M. L., S. H. Rongey, G. Feher, and M. Y. Okamura. 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. USA. 86:6602-6606.
57. Palazzo, G., A. Mallardi, M. Giustini, D. Berti, and G. Venturoli. 2000. Cumulant analysis of charge recombination kinetics in bacterial reaction centers reconstituted into lipid vesicles. Biophys. J. 79:1171-1179.
58. Palazzo, G., A. Mallardi, A. Hochkoeppler, L. Cordone, and G. Venturoli. 2002. Electron transfer kinetics in photosynthetic reaction centers embedded in trehalose glasses: trapping of conformational substates at room temperature. Biophys. J. 82:558-568.
59. Parot, P., J. Thiery, and A. Vermeglio. 1987. Charge recombination at low temperature in photosynthetic bacteria reaction centers: evidence for two conformational states. Biochim. Biophys. Acta. 893:534-543.
60. Peloquin, J. M., J. C. Williams, X. Lin, R. G. Alden, A. K. W. Taguchi, J. P. Allen, and N. W. Woodbury. 1994. Time-dependent thermodynamics during early electron transfer in reaction centers from Rhodobacter sphaeroides. Biochemistry. 33:8089-8100.
61. Sharp, R. E., and S. K. Chapman. 1999. Mechanisms for regulating electron transfer in multi-centre redox proteins. Biochim. Biophys. Acta. 1432:143-158.
62. Shopes, R. J., and C. A. Wraight. 1985. The acceptor quinone complex of Rhodopseudomonas viridis reaction centers. Biochim. Biophys. Acta. 806:348-356.
63. Stowell, M. H. B., T. M. McPhillips, D. C. Rees, S. M. Soltis, E. Abresch, and G. Feher. 1997. Light-induced structural changes in photosynthetic reaction center: implication for mechanism of electron-proton transfer. Science. 276:812-816.
64. B binding site. Biochemistry. 31:855-866.
65. Tiede, D. M., J. Vázquez, J. Córdova, and P. A. Marone. 1996. Time-resolved electrochromism associated with the formation of quinone anions in the Rhodobacter sphaeroides R26 reaction center. Biochemistry. 35:10763-10775.
66. Tiede, D. M., L. Utschig, D. K. Hanson, and D. M. Gallo, 1998. Resolution of electron and proton transfer events in the electrochromism associated with quinone reduction in bacterial reaction centers. Photosynth. Res. 55:267-273.
67. Uritani, M., M. Takai, and K. Yoshinaga. 1995. Protective effect of disaccharides on restriction endonucleases during drying under vacuum. J. Biochem. 117:774-779.
68. Van Mourik, F., M. Reus, and A. R. Holzwarth. 2001. Long-lived charge-separated states in bacterial reaction centers isolated from Rhodobacter sphaeroides. Biochim. Biophys. Acta. 1504:311-318.
69. Vermeglio, A., and R. K. Clayton. 1977. Kinetics of electron transfer between the primary and the secondary electron acceptor in reaction centers from Rhodopseudomonas sphaeroides. Biochim. Biophys. Acta. 461:159-165.
70. Vitkup, D., D. Ringe, G. A. Petsko, and M. Karplus. 2000. Solvent mobility and the protein "glass" transition. Nat. Struct. Biol. 7:34-38.
71. Walden, S. E., and R. A. Wheeler. 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.
72. Woodbury, N. W. T., and W. W. Parson. 1984. Nanosecond fluorescence from isolated photosynthetic reaction centers of Rhodopseudomonas sphaeroides. Biochim. Biophys. Acta. 767:345-361.
73. Woodbury, N. W. T., and W. W. Parson. 1986. Nanosecond fluorescence from chromatophores of Rhodopseudomonas sphaeroides and Rhodospirillum rubrum. Biochim. Biophys. Acta. 850:197-210.
74. Xu, Q., and M. R. Gunner. 2001. Trapping conformational intermediate states in the reaction center protein from photosynthetic bacteria. Biochemistry. 40:3232-3241.
75. B electron transfer reaction in bacterial photosynthetic reaction centers: pH dependence of the conformational gating step. Biochemistry. 41:2694-2701.
76. B electron transfer in bacterial photosynthetic reaction centers: effect of substrate position and tail length on the conformational gating step. Biochemistry. 41:10021-10025.
77. 1. Nature. 392:677-684.