Role of intramolecular vibrations in long-range electron transfer between pheophytin and ubiquinone in bacterial photosynthetic reaction centers

Biophysical Journal

Volumn 89, Issue 2, 2005, Pages 830-841

  Borrelli, Raffaele ^a,b   Di Donato, Mariangela ^a   Peluso, Andrea ^a  

^a UNIVERSITY OF SALERNO   (Italy)

^b ITALIAN AEROSPACE RESEARCH CENTER   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

PHEOPHYTIN; UBIQUINONE;

ARTICLE; DENSITY FUNCTIONAL THEORY; ELECTRON TRANSPORT; ENERGY; HYDROGEN BOND; KINETICS; MATHEMATICAL ANALYSIS; MATHEMATICAL PARAMETERS; MOLECULAR DYNAMICS; NONHUMAN; PHOTOSYNTHESIS; PHOTOTROPHIC BACTERIUM; PROBABILITY; VIBRATION;

EID: 23244437213     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.060574     Document Type: Article

References (61)

1. Voet, D., and J. Voet. 1995. Biochemistry. John Wiley and Sons, Hoboken, NJ.
2. Bendall, D. S. 1996. Protein Electron Transfer. Bios Scientific Publisher, Oxford, UK.
3. Marcus, R. A. 1956. On the oxidation-reduction reactions involving electron transfer. J. Chem. Phys. 24:966-978.
4. Hopfield, J. J. 1974. Electron transfer between biological molecules by thermal activated tunneling. Proc. Natl. Acad. Sci. USA. 71:3640-3644.
5. Kestner, N. R., J. Logan, and J. Jortner. 1974. Thermal electron transfer reactions in polar solvents. J. Phys. Chem. 78:2148-2166.
6. Sumi, H., and R. A. Marcus. 1986. Dynamical effects in electron transfer reactions. J. Chem. Phys. 84:4894-4914.
7. Di Valentin, M., A. Bisol, G. Agostini, M. Fuhs, P. A. Liddell, A. L. Moore, T. A. Moore, D. Gust, and D. Carbonera. 2004. Photochemistry of artificial photosynthetic reaction center in liquid crystals probed by multifrequency EPR (9.5 and 95 GHz). J. Am. Chem. Soc. 126:17074-17086.
8. Liddell, P. A., G. Kodis, L. de la Garza, A. L. Moore, and T. A. Moore. 2004. Benzene templated model systems for photosynthetic antenna-reaction centers function. J. Phys. Chem. B. 108:10256-10265.
9. Peluso, A., M. Di Donato, and G. A. A. Saracino. 2000. An alternative way of thinking about electron transfer in proteins: proton assisted electron transfer between the primary and secondary quinones in photosynthetic reaction centers. J. Chem. Phys. 113:3212-3218.
10. Hung, S., A. N. McPherson, S. Lin, P. A. Liddell, G. R. Seely, T. A. Moore, and D. Gust. 1995. Coordinated photoinduced electron and proton transfer in a molecular triad. J. Am. Chem. Soc. 117:1657-1658.
11. - in photosynthetic bacterial reaction centers and related model systems. J. Phys. Chem. B. 102:4648-4657.
12. Okamura, M. Y., M. Paddock, M. S. Graige, and G. Feher. 2000. Proton and electron transfer in bacterial reaction centers. Biochim. Biophys. Acta. 1458:148-163.
13. Markel, F., N. Ferris, I. Gould, and A. Myers. 1992. Mode-specific vibrational reorganization energies accompanying photoinduced electron transfer in the hexamethylbenzene/tetracyanoethylene charge-transfer complex. J. Am. Chem. Soc. 114:6208-6219.
14. Fischer, S. F., and R. P. Van Duyne. 1977. On the theory of electron transfer reactions. The naphtalene/TCNQ system. Chem. Phys. 26:9-16.
15. A site and the oxidized bacteriochlorophyll dimer. J. Phys. Chem. 90:3783-3795.
16. A. J. Am. Chem. Soc. 111:3400-3412.
17. Wegenwijs, B., and J. W. Verhoeven. 1999. Long-range charge separation in solvent free donor-bridge-acceptor systems. Adv. Chem. Phys. 106:221-264.
18. Paddow-Row, M. N. 1994. Investigating long-range electron transfer with rigid, covalently linked donor-(norbornylogous bridge)-acceptor systems. Acc. Chem. Res. 27:18-25.
19. Xie, A., F. G. v. d. M. Alexandre, and R. H. Austin. 2002. Excited-state lifetimes of far-infrared collective modes in proteins. Phys. Rev. Lett. 88:018102(1-4).
20. Moritsugu, K., O. Miyoshita, and A. Kidera. 2000. Vibrational energy transfer in a protein molecule. Phys. Rev. Lett. 85:3970-3973.
21. Borrelli, R., and A. Peluso. 2003. Dynamics of radiationless transitions in large molecular systems: a Franck-Condon based method accounting for displacements and rotations of all the normal coordinates. J. Chem. Phys. 119:8437-8448.
22. Robinson, G. W., and R. P. Frosch. 1962. Theory of electronic energy relaxation in solid phase. J. Chem. Phys. 37:1962-1973.
23. Bixon, M., and J. Jortner. 1999. Electron transfer: from isolated molecules to biomolecules. Adv. Chem. Phys. 106:35-203.
24. Alfano, D., A. Peluso, and R. Borrelli. 2002. A simple method for estimating activation energies of proton-transfer reactions. J. Phys. Chem. A. 106:7018-7025.
25. Mead, C. A., and D. G. Truhlar. 1979. On the determination of Born-Oppehneimer nuclear motion wave functions including complications due to conical intersections and identical nuclei. J. Chem. Phys. 70:2284-2296.
26. Ivashin, N., B. Kallebring, S. Larsson, and O. Hansson. 1998. Charge separation in photosynthetic reaction centers. J. Phys. Chem. B. 102 :5017-5022.
27. Duschinsky, F. 1937. On the interpretation of electronic spectra of polyatomic molecules. I. Concerning the Franck-Condon principle. Acta Phisicochim. URSS. 7:551-566.
28. Sharp, T. E., and K. M. Rosenstock. 1964. Franck-Condon factors for polyatomic molecules. J. Chem. Phys. 41:3453-3463.
29. Reimers, J. R. 2001. A practical method for the use of curvilinear coordinates in calculations of normal-mode-projected displacements and Duschinsky rotation matrices for large molecules. J. Chem. Phys. 115:9103-9109.
30. Peluso, A., F. Santoro, and G. Del Re. 1997. Vibronic coupling in electronic transitions with significant Duschinsky effect. Int. J. Quantum Chem. 63:233-244.
31. Doktorov, E. V., I. A. Malkin, and M.V.I. 1975. Dynamical symmetry of vibronic transitions in polyatomic molecules and the Franck-Condon principle. J. Mol. Spec. 56:1-20.
32. Borrelli, R., and A. Peluso. 2004. MolFC: a program for Franck-Condon integrals calculation. Available at http://pcdual.chem.unisa.it. [Online].
33. Kleinfeld, D., M. Y. Okamura, and G. Feher. 1984. Electron transfer kinetics in photosynthetic reaction center cooled to cryogenic temperature in the charge separated state: evidence for light-induced structural changes. Biochemistry. 23:5780-5786.
34. Franzen, S., and S. G. Boxer. 1993. Temperature dependence of the electric field modulation of electron transfer rates: charge recombination in photosynthetic reaction centers. J. Phys. Chem. 97:6304-6318.
35. - determined from delayed fluorescence in reaction centers from Rhodobacter sphaeroides R-26. Biochim. Biophys. Acta. 1019:91-94.
36. Breton, J., and E, Nabedryk. 1998. Proton uptake upon quinone reduction in bacterial reaction centers: IR signature and possible participation of a highly polarizable hydrogen bond network. Photosynth. Res. 55:301-307.
37. Stowell, M. H. B., T. McPhillips, D. C. Rees, S. M. Soltis, E. Abresch, and G. Feher. 1997. Light induced structural changes in photosynthetic reaction center: implications for mechanism of electron-proton transfer. Science 276:812-816. PDB ID: 1AIG.
38. Di Donato, M., A. Peluso, and G. Villani. 2004. Electron transfer between quinones in photosynthetic reaction centers. J. Phys. Chem. B. 108:3068-3077.
39. Almeida, R., and R. A. Marcus. 1990. Dynamics of electron transfer for a nonsuperexchange coherent mechanism. 2. Numerical calculations. J. Phys. Chem. 94:2978-2985.
40. Kuhn, H. 1986. Electron transfer mechanism in the reaction center of photosynthetic bacteria. Phys. Rev. A. 34:3409-3425.
41. Schenck, C. C. W. W. Parson, D. Holten, M. W. Windsor, and A. Sarai. 1981. Temperature dependence of electron transfer between bacteriopheophytine and ubiquinone in protonated and deuterated reaction centers of Rhodopseudomonas sphaeroides. Biophys. J. 36:479-489.
42. Woodbury, W. T., and W. W. Parson. 1984. Nanosecond fluorescence from isolated photosynthetic reaction centers of Rhodopseudomonas sphaeroides. Biochim. Biophys. Acta. 767:345-361.
43. Woodbury, N. W. T., N. Becker, D. Middendorf, and W. W. Parson. 1985. Picosecond kinetics of the initial photochemical electron-transfer reaction in bacterial photosynthetic reaction centers. Biochemistry. 24:7516-7521.
44. 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. 810:33-48.
45. McElroy, J. D., D. C. Mauzerall, and G. Feher. 1974. Characterization of primary reactants in bacterial photosynthesis. II. Kinetics studies of the light induced signal (g = 2.0026) and the optical absorbance changes at cryogenic temperatures. Biochim. Biophys. Acta. 333:261-278.
46. Kriegl, J. M., and G. U. Niehaus. 2004. Structural, dynamic, and energetic aspects of long-range electron transfer in photosynthetic reaction centers. Proc. Natl. Acad. Sci. USA. 101:123-128.
47. Kriegl, J. M., F. K. Forster, and G. U. Nienhaus. 2003. Charge recombination and protein dynamics in bacterial photosynthetic reaction centers entrapped in a sol-gel matrix. Biophys. J. 85:1851-1870.
48. Xu, D., and K. Schulten. 1994. Coupling of protein motion to electron transfer in a photosynthetic reaction center: investigating the low temperature behavior in the framework of the spin-boson model. Chem. Phys. 182:91-117.
49. Czarnecki, K., J. R. Diers, V. Chynwat, J. P. Erickson, H. A. Frank, and D. F. Bocian. 1997. Characterization of the strongly coupled, low-frequency vibrational modes of the special pair of photosynthetic reaction centers via isotopic labeling of the cofactors. J. Am. Chem. Soc. 119:415-426.
50. -1 regime, intermolecular solvent modes, and relevance to photosynthesis. J. Am. Chem. Soc. 125:11810-11811.
51. Rischel, C., D. Spiedel, J. P. Ridge, M. R. Jones, J. Breton, J.-C. Lambry, J.-L. Martin, and M. H. Vos. 1998. Low frequency vibrational modes in proteins: changes induced by point-mutations in the protein-cofactor matrix of bacterial reaction centers. Proc. Natl. Acad. Sci. USA. 95:12306-12311.
52. Reimers, J. R., and N. S. Hush. 2004. A unified description of the electrochemical, charge distribution, and spectroscopic properties of the special-pair radical cation in bacterial photosynthesis. J. Am. Chem. Soc. 126:4132-4144.
53. Beratan, D. N., J. N. Betts, and J. N. Onuchic. 1991. Protein electron transfer rates set by the bridging secondary and tertiary structure. Science 252:1285-1288.
54. Beratan, D. N., J. N. Onuchic, J. R. Winkler, and H. B. Gray. 1992. Electron tunneling pathways in proteins. Science. 258:1740-1741.
55. Page, C. C., C. C. Moser, X. Chen, and P. L. Dutton. 1999. Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature. 402:47-52.
56. Lee, C., W. Yang, and R. G. Parr. 1988. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys. Rev. B. 37:785-789.
57. Frisch, M. J., G. W. Trucks, H. B. Schlegel, P. W. Gill, B. G. Johnson, M. A. Robb, J. R. Cheeseman, T. Keith, G. A. Petersson, J. A. Montgomery, K. Raghavachari, M. A. Al-Laham, et al. 1995. Gaussian 94, Revision C.2. Gaussian Inc., Pittsburgh, PA.
58. Berman, H. M., J. Westbrook, Z. Feng, G. Gilliand, T. N. Bhat, H. Weissig, I. N. Shindyalov, and P. E. Bourne. 2000. The protein data bank. Nucleic Acids Res. 28:235-242.
59. Park, J. T., and J. C. Light. 1986. Unitary quantum time evolution by iterative Lanczos reduction. J. Chem. Phys. 85:5870-5876.
60. Beyer, T., and D. F. Swinehart. 1973. Number of multiply restricted partitions. Commun. Assoc. Comput. Machin. 16:379.
61. Stein, S. E., and B. S. Rabinovitch. 1973. Accurate evaluation of internal energy level sums and densities including anharmonic oscillators and hindered rotors. J. Chem. Phys. 58:2438-2445.