Energetics and mechanisms of high efficiency of charge separation and electron transfer processes in Rhodobacter sphaeroides reaction centers

Bioelectrochemistry

Volumn 61, Issue 1-2, 2003, Pages 73-84

  Paschenko, Vladimir Z ^a   Gorokhov, Vladimir V ^a   Knox, Peter P ^a   Krasilnikov, Pavel M ^a   Redlin, Harald ^b   Renger, Gernot ^c   Rubin, Andrew B ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b MAX BORN INSTITUT   (Germany)

^c TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Electron transfer; Hydrogen bond; Nonequilibrium cofactor state; Reaction center; Relaxation process

Indexed keywords

FLUORESCENCE; GLYCEROL; HYDROGEN BONDS; KINETIC THEORY; RATE CONSTANTS; SOLVENTS; SPECTROSCOPIC ANALYSIS; SUBSTITUTION REACTIONS;

CRYOSOLVENTS; REACTION CENTERS (RC);

BACTERIA;

ABSORPTION SPECTROSCOPY; ADDITION REACTION; ARTICLE; ELECTRIC ACTIVITY; ELECTRON TRANSPORT; ENERGY TRANSFER; FLUORESCENCE SPECTROSCOPY; HYDROGEN BOND; LINEAR ENERGY TRANSFER; RHODOBACTER SPHAEROIDES; SOLVATION; SUBSTITUTION REACTION;

BACTERIA (MICROORGANISMS); RHODOBACTER; RHODOBACTER SPHAEROIDES;

EID: 0344983900     PISSN: 15675394     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1567-5394(03)00077-X     Document Type: Article

References (50)

1. Lancaster C.R.D., Ermler U., Michel H. The structure of photosynthetic reaction centers from purple bacteria as revealed by X-ray crystallography. Blankenship R.E., Madigan M.T., Bauer C.E. Anoxygenic Photosynthetic Bacteria. 1995;503-526 Kluwer Academic Publishers, Netherlands.
2. Fleming G.R., Van Grondelle R. The primary steps of photosynthesis. Phys. Today. 47:1994;48-55.
3. El-Kabbani O., Chang C.H., Tiede D.M., Norris J.R., Shiffer M. Comparison of reaction centers from Rhodobacter sphaeroides and Rhodopseudomonas viridis: overall architecture and protein-pigment interactions. Biochemistry. 30:1991;5361-5369.
4. Ermler U., Fritsch G., Buchanan S.K., Michel H. Structure of the photosynthetic reaction centre from Rhodobacter sphaeroides at 2.65 Å resolution: cofactors and protein-cofactors interactions. Structure. 2:1994;925-936.
5. Deisenhofer J., Michel H. Crystallographic refinement at 2.3 Å resolution and refined model of the photosynthetic reaction center of Rhodopseudomonas viridis. J. Mol. Biol. 246:1995;429-457.
6. Katilius E., Kataliene Z., Lin S., Taguchi A.K.W., Woodbury N.W. B side electron transfer in a Rhodobacter sphaeroides reaction center mutant in which the B side monomer bacteriochlorophyll is replaced with bacteriopheophytin: low-temperature study and energetics of charge-separated states. J. Phys. Chem. B. 106:2002;1471-1475.
7. de Boer A.L., Neerken S., de Wijn R., Permentier H.P., Gast P., Vijgenboom E., Hoff A.J. High yield of B-branch electron transfer in a quadruple reaction center mutant of the photosynthetic bacterium Rhodobacter sphaeroides. Biochemistry. 41:2002;3081-3088.
8. B. Biochemistry. 42:2003;2016-2024.
9. A ubiquinone. FEBS Lett. 540:2003;234-240.
10. Kirmaier C., Holten D., Parson W.W. Temperature and detection-wavelength dependence of the picosecond electron-transfer kinetics measured in Rhodobacter sphaeroides reaction centers. Resolution of new spectral kinetic components in the primary charge-separation process. Biochim. Biophys. Acta. 810:1985;33-48.
11. Shuvalov V.A., Dyusens L.N.M. Primary electron transfer reactions in modified reaction centers from Rhodopseudomonas sphaeroides. Proc. Natl. Acad. Sci. U. S. A. 83:1986;1690-1694.
12. Holzapfel W., Finkele U., Kaiser W., Osterhelt D., Scheer H., Stilz H.U., Zinth W. Observation of a bacteriochlorophyll anion radical during the primary charge separation in a reaction center. Chem. Phys. Lett. 160:1989;1-7.
13. Holzwarth A.R., Muller M.G. Energetics and kinetics of radical pairs in reaction centers from Rhodobacter sphaeroides. A femtosecond transient absorption study. Biochemistry. 35:1996;11820-11831.
14. Ivashin N., Larsson S. Vibrational mechanism for primary charge separation in the reaction center of Rhodobacter sphaeroides. J. Phys. Chem. B. 106:2002;3996-4009.
15. Xu H., Zhang R.-B., Ma S.-H., Qu Z.-W., Zhang X.-K., Zhang Q.-Y. Theoretical studies on the mechanism of primary electron transfer in the photosynthetic reaction center of Rhodobacter sphaeroides. Photosynth. Res. 74:2002;11-36.
16. Trissl H.-W., Bernhardt K., Lapin M. Evidence for protein dielectric relaxations in reaction centers associated with the primary charge separation detected from Rhodospirillum rubrum chromatophores by combined photovoltage and absorption measurements in the 1-15 ns time range. Biochemistry. 40:2001;5290-5298.
17. van Mourik F., Rens M., Holzwarth A.R. Long-lived charge-separated states in bacterial reaction centers isolated from Rhodobacter sphaeroides. Biochim. Biophys. Acta. 1504:2001;311-318.
18. Williams J.C., Alden R.G., Murchison M.A., Peloquin J.M., Woodbury N.W., Allen J.P. Effect of mutation near the bacteriophyll in the reaction centers from Rhodobacter sphaeroides. Biochemistry. 31:1992;11029-11037.
19. Murchison M.A., Alden R.G., Allen J.P., Peloquin J.M., Taguchi A.K.W., Woodbury N.W., Williams J.C. Mutations designed to modify the environment of the primary electron donor of the reaction center from Rhodobacter sphaeroides: phenylalanine to leucine at L167 and histidine to phenylalanine at L168. Biochemistry. 32:1993;3498-3505.
20. Mattioli T.A., Williams J.C., Allen J.P., Robert B. 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. 33:1994;1636-1943.
21. Lin X., Murchison H.A., Nagarajan V., Parson W.W., Williams C.J., Allen J.P. Specific alteration of the oxidation potential of the electron donor in the reaction centers from Rhodobacter sphaeroides. Proc. Natl. Acad. Sci. U. S. A. 91:1994;10265-10269.
22. Mattioli T.A., Lin X., Allen J.P., Williams J.C. Correlation between multiple hydrogen oxidation potential of the bacteriochlorophyll dimer of reaction center from Rhodobacter sphaeroides. Biochemistry. 34:1995;6142-6152.
23. Ivancich A., Arltz K., Williams J.C., Allen J.P., Mattioli T.A. Effects of hydrogen bonds on the redox potential and electronic structure of the bacterial primary electron donor. Biochemistry. 37:1998;11812-11820.
24. Bylina E.J., Kirmaier C., McDowell L., Holten D., Youvan D.C. Influence of an amino-acid residue on the optical properties and electron transfer dynamics of a photosynthetic reaction centre complex. Nature. 336:1988;182-184.
25. Paschenko V.Z., Korvatovsky B.N., Logunov S.L., Knox P.P., Zakharova N.I., Grishanova N.P., Rubin A.B. Modification of protein hydrogen bonds influences the efficiency of picosecond electron transfer in bacterial reaction centers. FEBS Lett. 214:1987;28-34.
26. Paschenko V.Z., Gorokhov V.V., Grishanova N.P., Goryacheva E.A., Korvatovsky B.N., Knox P.P., Zakharova N.I., Rubin A.B. The influence of structural-dynamic organization of RC from purple bacterium Rhodobacter sphaeroides on picosecond stages of photoinduced reactions. Biochim. Biophys. Acta. 1364:1998;361-372.
27. 2O and cryosolvents on the redox properties of bacteriochlorophyll dimer and electron transfer processes in Rhodobacter sphaeroides reaction centers. Bioelectrochemistry. 53:2001;233-241.
28. Paschenko V.Z. Correlation between structural-dynamic organization of the reaction centers of the purple bacterium Rhodobacter sphaeroides and the picosecond stages of photosynthesis. Biophysics. 45:2000;449-456.
29. Zakharova N.I., Churbanova I.Yu. Methods of reaction center preparations from photosynthetic purple bacteria. Biochemistry. 65:2000;181-193.
30. Wright C.A., Clayton R.K. The absolute quantum efficiency of bacteriochlorophyll photooxidation in reaction centres of Rhodopseudomonas sphaeroides. Biochim. Biophys. Acta. 333:1973;246-260.
31. 2; on a possible charge transfer process between guanine and porphyrin in its excited singlet state. J. Photochem. Photobiol. 40:1997;154-162.
32. Luck W.A.P. Role of hydrogen bonding in the structure of liquids. Acta Chim. Hung. 121:1986;119-145.
33. Kleeberg H. Influence of alkali cations on the infrared spectra of water molecules in aprotic solvents. J. Phys. Chem. 90:1986;4427-4430.
34. Chamorovsky S.K., Mamedov M.D., Semenov A.Yu. , Zakharova N.I., Knox P.P., Rubin A.B. The influence of glycerol and dimethylsulfoxide on the midpoint potential of bacteriochlorophyll dimer in Rhodobacter sphaeroides reaction center. Doklady Biochem. Biophys. (Moscow). 361:1998;120-122.
35. Hartwich G., Lossau H., Michel-Beyerle M.E., Ogrodnik A. Nonexponential fluorescence decay in reaction centers of Rhodobacter sphaeroides reflecting dispersive charge separation up to 1 ns. J. Phys. Chem. B. 102:1998;3815-3820.
36. - in reaction centers of Rb. sphaeroides R26: a spontaneous emission study. Chem. Phys. 244:1999;461-478.
37. Marcus R.A., Sutin N. Electron transport in chemistry and biology. Biochim. Biophys. Acta. 811:1985;265-322.
38. Moser C.C., Page C.C., Chen X., Dutton P.L. Intraprotein electron transfer: illustrations from the photosynthetic reaction center. Peschek G., Loffelhandt W., Schemetter G. The Phototropic Procaryotes. 1999;105-111 Plenum, New York.
39. 2O and cryoprotectants. Biomembranes (Moscow). 17:2000;271-281.
40. Brown W. Dielectrics. Flugge S. Handbuch der Physik. vol. XVII:1961;Springer, Berlin.
41. Aksenov S.I., Gavrilova I.I., Gangard M.G., Revokatov O.P. Investigation of dimethylsulfoxide interaction with protein macromolecules using method of spin echo NMR. Kryobiology (Moscow). 4:1985;31-33.
42. Rishel C., Spiedel D., Ridge J.P., Breton J., Lambry J.C., Martin J.L., Vos M.H. Low frequency vibrational modes in proteins: changes induced by point-mutations in the protein-cofactor matrix of bacterial reaction centers. Proc. Natl. Acad. Sci. U. S. A. 95:1998;12306-12311.
43. Fritzsch G., Kampmann L., Kapaun G., Michel H. Water clusters in the reaction centre of Rhodobacter sphaeroides. Photosynth. Res. 55:1998;127-132.
44. Karplus M., McCammon J.M. Dynamics of protein: elements and function. Ann. Rev. Biochem. 53:1983;263-300.
45. Nitzan A. Ultrafast relaxation in water. Nature. 402:1999;472-475.
46. Volk M., Aumeier G., Langenbacher T., Feick R., Ogrodnik A. Energetics and mechanism of primary charge separation in bacterial photosynthesis. A comparative study on reaction centers of Rhodobacter sphaeroides and Chloroflexus aurantiacus. J. Phys. Chem. B. 102:1998;735-751.
47. Priev A., Almagor A., Yedgar S., Savish G. Glycerol decreases the volume and compressibility of protein interior. Biochemistry. 35:1996;2061-2066.
48. Goldanskii V.I., Krupyanskii Y.F. Protein dynamics: hydration, temperature and solvent viscosity effects as revealed by Rayleigh scattering radiation. Gregory R.B. Protein-Solvent Interactions. 1995;289-326 Marcel Dekker, New York.
49. Yu.N. Kukushkin, Dimethylsulfoxide - an important aprotic solvent. Soros Ed. Journal 7 (1997) 54-59.
50. Santucci R., Laurenti E., Sinibaldi F., Ferrari R.P. Effect of dimethylsulfoxide on the structure and the functional properties of horseradish peroxidase as observed by spectroscopy and cyclic voltammetry. Biochim. Biophys. Acta. 1596:2002;225-233.