Identification of the first steps in charge separation in bacterial photosynthetic reaction centers of Rhodobacter sphaeroides by ultrafast mid-infrared spectroscopy: Electron transfer and protein dynamics

Biophysical Journal

Volumn 95, Issue 3, 2008, Pages 1268-1284

  Pawlowicz, Natalia P ^a   Van Grondelle, Rienk ^a   Van Stokkum, Ivo H M ^a   Breton, Jacques ^b   Jones, Michael R ^c   Groot, Marie Louise ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b CEA SACLAY   (France)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; ELECTRICITY; ELECTRON TRANSPORT; INFRARED SPECTROPHOTOMETRY; KINETICS; LIGHT; METHODOLOGY; PHOTOSYNTHESIS; RADIATION EXPOSURE; RHODOBACTER SPHAEROIDES;

COMPUTER SIMULATION; ELECTRON TRANSPORT; ELECTROSTATICS; KINETICS; LIGHT; MODELS, CHEMICAL; MODELS, MOLECULAR; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; RHODOBACTER SPHAEROIDES; SPECTROPHOTOMETRY, INFRARED;

EID: 51049111660     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.108.130880     Document Type: Article

References (71)

1. Deisenhofer, J., O. Epp, I. Sinning, and H. Michel. 1995. Crystallographic refinement at 2.3-angstrom resolution and refined model of the photosynthetic reaction center from Rhodopseudomonas viridis. J. Mol. Biol. 246:429-457.
2. Chirino, A. J., E. J. Lous, M. Huber, J. P. Allen, C. C. Schenck, M. L. Paddock, G. Feher, and D. C. Rees. 1994. Crystallographic analyses of site-directed mutants of the photosynthetic reaction center from Rhodobacter sphaeroides. Biochemistry. 33:4584-4593.
3. Lancaster, C. R. D., U. Ermler, and H. Michel. 1995. Anoxygenic Photosynthetic Bacteria. Kluwer Academic, Dordrecht, The Netherlands. 503-526.
4. Woodbury, N. W., and J. P. Allen. 1995. The pathway, kinetics and thermodynamics of electron transfer in wild type and mutant bacterial reaction centers of purple nonsulfur bacteria. In Anoxygenic Photosynthetic Bacteria. M. T. M. R. E. Blankenship, and C. E. Bauer, editors. Kluwer Academic, Dordrecht, The Netherlands. 527-557.
5. van Brederode, M. E., and M. R. Jones. 2000. Reaction centres of purple bacteria. In Enzyme-Catalyzed Electron and Radical Transfer. N. S. S. A. Holzenburg, editor. Kluwer Academic/Plenum, New York. 621-676.
6. Zinth, W., and J. Wachtveitl. 2005. The first picoseconds in bacterial photosynthesis - ultrafast electron transfer for the efficient conversion of light energy. Chemphyschem. 6:871-880.
7. Ziolek, M., N. Pawlowicz, R. Naskrecki, and A. Dobek. 2005. Electron transfer in the reaction center of the Rb. sphaeroides R-26 studied by transient absorption. J. Phys. Chem. B. 109:18171-18176.
8. Parson, W. W. 1996. Photosynthetic Bacterial Reaction Centers. In Protein Electron Transfer. D. S. Bendall, editor. BIOS Scientific, Oxford. 125-160.
9. 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.
10. Holzapfel, W., U. Finkele, W. Kaiser, D. Oesterhelt, H. Scheer, H. U. Stilz, and W. Zinth. 1989. Observation of a bacteriochlorophyll anion radical during the primary charge separation in a reaction center. Chem. Phys. Lett. 160:1-7.
11. Holzapfel, W., U. Finkele, W. Kaiser, D. Oesterhelt, H. Scheer, H. U. Stilz, and W. Zinth. 1990. Initial electron-transfer in the reaction center from Rhodobacter sphaeroides. Proc. Natl. Acad. Sci. USA. 87:5168-5172.
12. Schmidt, S., T. Arlt, P. Hamm, H. Huber, T. Nagele, J. Wachtveitl, M. Meyer, H. Scheer, and W. Zinth. 1994. Energetics of the primary electron-transfer reaction revealed by ultrafast spectroscopy on modified bacterial reaction centers. Chem. Phys. Lett. 223:116-120.
13. van Brederode, M. E., M. R. Jones, and R. van Grondelle. 1997. Fluorescence excitation spectra of membrane-bound photosynthetic reaction centers of Rhodobacter sphaeroides in which the tyrosine M210 residue is replaced by tryptophan: evidence for a new pathway of charge separation. Chem. Phys. Lett. 268:143-149.
14. van Brederode, M. E., M. R. Jones, F. van Mourik, I. H. M. van Stokkum, and R. van Grondelle. 1997. A new pathway for transmembrane electron transfer in photosynthetic reaction centers of Rhodobacter sphaeroides not involving the excited special pair. Biochemistry. 36:6855-6861.
15. van Brederode, M. E., F. van Mourik, I. H. M. van Stokkum, M. R. Jones, and R. van Grondelle. 1999. Multiple pathways for ultrafast transduction of light energy in the photosynthetic reaction center of Rhodobacter sphaeroides. Proc. Natl. Acad. Sci. USA. 96:2054-2059.
16. Schlodder, E., and K. Brettel. 1988. Primary charge separation in closed photosystem-II with a lifetime of 11-ns-flash-absorption spectroscopy with O-2-evolving photosystem-II complexes from Synechococcus. Biochim. Biophys. Acta. 933:22-34.
17. Groot, M. L., E. J. G. Peterman, P. J. M. van Kan, I. H. M. van Stokkum, J. P. Dekker, and R. van Grondelle. 1994. Temperaturedependent triplet and fluorescence quantum yields of the photosystem-II reaction-center described in a thermodynamic model. Biophys. J. 67:318-330.
18. van Stokkum, I. H. M., L. M. P. Beekman, M. R. Jones, M. E. van Brederode, and R. van Grondelle. 1997. Primary electron transfer kinetics in membrane-bound Rhodobacter sphaeroides reaction centers: a global and target analysis. Biochemistry. 36:11360-11368.
19. Hamm, P., M. Zurek, W. Mantele, M. Meyer, H. Scheer, and W. Zinth. 1995. Femtosecond infrared-spectroscopy of reaction centers from Rhodobacter sphaeroides between 1000 and 1800 cm(-1). Proc. Natl. Acad. Sci. USA. 92:1826-1830.
20. Hamm, P., and W. Zinth. 1995. Ultrafast initial reaction in bacterial photosynthesis revealed by femtosecond infrared-spectroscopy. J. Phys. Chem. 99:13537-13544.
21. Maiti, S., B. R. Cowen, R. Diller, M. Iannone, C. C. Moser, P. L. Dutton, and R. M. Hochstrasser. 1993. Picosecond infrared studies of the dynamics of the photosynthetic reaction center. Proc. Natl. Acad. Sci. USA. 90:5247-5251.
22. Maiti, S., G. C. Walker, B. R. Cowen, R. Pippenger, C. C. Moser, P. L. Dutton, and R. M. Hochstrasser. 1994. Femtosecond coherent transient infrared-spectroscopy of reaction centers from Rhodobacter sphaeroides. Proc. Natl. Acad. Sci. USA. 91:10360-10364.
23. Walker, G. C., S. Maiti, B. R. Cowen, C. C. Moser, P. L. Dutton, and R. M. Hochstrasser. 1994. Time resolution of electronic-transitions of photosynthetic reaction centers in the infrared. J. Phys. Chem. 98:5778-5783.
24. Wynne, K., G. Haran, G. D. Reid, C. C. Moser, P. L. Dutton, and R. M. Hochstrasser. 1996. Femtosecond infrared spectroscopy of low-lying excited states in reaction centers of Rhodobacter sphaeroides. J. Phys. Chem. 100:5140-5148.
25. Haran, G., K. Wynne, C. C. Moser, P. L. Dutton, and R. M. Hochstrasser. 1996. Level mixing and energy redistribution in bacterial photosynthetic reaction centers. J. Phys. Chem. 100:5562-5569.
26. Wang, H. Y., S. Lin, J. P. Allen, J. C. Williams, S. Blankert, C. Laser, and N. W. Woodbury. 2007. Protein dynamics control the kinetics of initial electron transfer in photosynthesis. Science. 316:747-750.
27. Groot, M. L., L. J. G. W. van Wilderen, D. S. Larsen, M. A. van der Horst, I. H. M. van Stokkum, K. J. Hellingwerf, and R. van Grondelle. 2003. Initial steps of signal generation in photoactive yellow protein revealed with femtosecond mid-infrared spectroscopy. Biochemistry. 42:10054-10059.
28. Groot, M. L., J. Breton, L. J. G. W. van Wilderen, J. P. Dekker, and R. van Grondelle. 2004. Femtosecond visible/visible and visible/mid-IR pump-probe study of the photosystem II core antenna complex CP47. J. Phys. Chem. B. 108:8001-8006.
29. 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. 349-386.
30. Ridge, J. P., M. E. van Brederode, M. G. Goodwin, R. van Grondelle, and M. R. Jones. 1999. Mutations that modify or exclude binding of the QA ubiquinone and carotenoid in the reaction center from Rhodobacter sphaeroides. Photosynth. Res. 59:9-26.
31. McAuley, K. E., P. K. Fyfe, J. P. Ridge, R. J. Cogdell, N. W. Isaacs, and M. R. Jones. 2000. Ubiquinone binding, ubiquinone exclusion, and detailed cofactor conformation in a mutant bacterial reaction center. Biochemistry. 39:15032-15043.
32. Breton, J., M. C. Wakeham, P. K. Fyfe, M. R. Jones, and E. Nabedryk. 2004. Characterization of the bonding interactions of Q(B) upon photoreduction via A-branch or B-branch electron transfer in mutant reaction centers from Rhodobacter sphaeroides. Biochim. Biophys. Acta. 1656:127-138.
33. Okamura, M. Y., R. A. Isaacson, and G. Feher. 1975. Primary acceptor in bacterial photosynthesis - obligatory role of ubiquinone in photoactive reaction centers of Rhodopseudomonas spheroides. Proc. Natl. Acad. Sci. USA. 72:3491-3495.
34. Woodbury, N. W., W. W. Parson, M. R. Gunner, R. C. Prince, and P. L. Dutton. 1986. Radical pair energetics and decay mechanisms in reaction centers containing anthraquinones, naphthoquinones or benzoquinones in place of ubiquinone. Biochim. Biophys. Acta. 851:6-22.
35. van Stokkum, I. H. M., D. S. Larsen, and R. van Grondelle. 2004. Global and target analysis of time-resolved spectra. Biochim. Biophys. Acta. 1657:82-104.
36. Lozovoy, V. V., I. Pastirk, M. G. Comstock, and M. Dantus. 2001. Cascaded free-induction decay four-wave mixing. Chem. Phys. 266:205-212.
37. Mitsumori, Y., H. Fukushima, M. Ogura, T. Kuroda, S. Koshihara, F. Minami. 1996. Excitonic free induction decay studied with femtosecond pulse pairs. Luminescence. 66-67:81-83.
38. Holzwarth, A. R., and M. G. Muller. 1996. Energetics and kinetics of radical pairs in reaction centers from Rhodobacter sphaeroides. A femtosecond transient absorption study. Biochemistry. 35:11820-11831.
39. Nabedryk, E. 1996. Light-induced Fourier transform infrared difference spectroscopy of the primary electron donor in photosynthetic reaction centers. In Infrared Spectroscopy of Biomolecules. H. H. Mantsch and D. Chapman, editors. Wiley-Liss, New York. 39-81.
40. - states in reaction centers from Rb. Sphaeroides. In Current Research in Photosynthesis, Vol. I. M. Baltscheffsky, editor. Kluwer Academic Publishers, Dordrecht, The Netherlands. I.1.77-I.1.80.
41. Breton, J., D. L. Thibodeau, C. Berthomieu, W. Mantele, A. Vermeglio, and E. Nabedryk. 1991. Probing the primary quinone environment in photosynthetic bacterial reaction centers by light-induced FTIR difference spectroscopy. FEBS Lett. 278:257-260.
42. Groot, M. L., N. P. Pawlowicz, L. J. G. W. van Wilderen, J. Breton, I. H.M. van Stokkum, and R. van Grondelle. 2005. Initial electron donor and acceptor in isolated Photosystem II reaction centers identified with femtosecond mid-IR spectroscopy. Proc. Natl. Acad. Sci. USA. 102:13087-13092.
43. Nabedryk, E., S. Andrianambinintsoa, D. Dejonghe, and J. Breton. 1995. FTIR spectroscopy of the photoreduction of the bacteriopheophytin electron-acceptor in reaction centers of Rhodobacter sphaeroides and Rhodopseudomonas viridis. Chem. Phys. 194:371-378.
44. Mantele, W. G., A. M. Wollenweber, E. Nabedryk, and J. Breton. 1988. Infrared spectroelectrochemistry of bacteriochlorophylls and bacteriopheophytins-implications for the binding of the pigments in the reaction center from photosynthetic bacteria. Proc. Natl. Acad. Sci. USA. 85:8468-8472.
45. Nabedryk, E., K. A. Bagley, D. L. Thibodeau, M. Bauscher, W. Mantele, and J. Breton. 1990.Aprotein conformational change associated with the photoreduction of the primary and secondary quinones in the bacterial reaction center. FEBS Lett. 266:59-62.
46. Thibodeau, D. L., J. Breton, C. Barthomieu, W. Mantele, and E. Nabedryk. 1990. Reaction Centres of Photosynthetic Bacteria. Springer, Berlin. 87-98.
47. Nabedryk, E., B.A. Tavitian, W.Mantele, W. Kreutz, and J. Breton. 1987. Progress in Photosynthesis Research. Kluwer. Dordrecht. 177-180.
48. Nabedryk, E., B. A. Tavitian, W. Mantele, and J. Breton. 1985. Spectroscopy of Biological Molecules. Wiley-Liss, New York. 367-369.
49. Mantele, W., E. Nabedryk, B. A. Tavitian, W. Kreutz, and J. Breton. 1985. Light-induced Fourier-transform infrared (FTIR) spectroscopic investigations of the primary donor oxidation in bacterial photosynthesis. FEBS Lett. 187:227-232.
50. Wakeham, M. C., M. G. Goodwin, C. McKibbin, and M. R. Jones. 2003. Photo-accumulation of the P(+)Q(B)(-) radical pair state in purple bacterial reaction centres that lack the Q(A) ubiquinone. FEBS Lett. 540:234-240.
51. Breton, J., E. Nabedryk, and W. W. Parson. 1992. A new infrared electronic-transition of the oxidized primary electron-donor in bacterial reaction centers - a way to assess resonance interactions between the bacteriochlorophylls. Biochemistry. 31:7503-7510.
52. Breton, J., E. Nabedryk, and A. Clerici. 1999. Light-induced FTIR difference spectroscopy of photosynthetic charge separation between 9000 and 250 cm(-1). Vib. Spectrosc. 19:71-75.
53. Reimers, J. R., and N. S. Hush. 1995. Nature of the ground and first excited-states of the radical cations of photosynthetic bacterial reaction centers. Chem. Phys. 197:323-332.
54. 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.
55. Lockhart, D. J., and S. G. Boxer. 1987. Magnitude and direction of the change in dipole-moment associated with excitation of the primary electron-donor in Rhodopseudomonas sphaeroides reaction centers. Biochemistry. 26:664-668.
56. Lockhart, D. J., and S. G. Boxer. 1988. Stark-effect spectroscopy of Rhodobacter sphaeroides and Rhodopseudomonas viridis reaction centers. Proc. Natl. Acad. Sci. USA. 85:107-111.
57. Breton, J., M. Bauscher, C. Berthomieu, D. L. Thibodeau, S. Andiranambinintsoa, D. Dejonghe, W. Mantele, and E. Nabedryk. 1991. Spectroscopy of Biological Molecules. The Royal Society of Chemistry, Cambridge. 43-46.
58. Breton, J., J. R. Burie, C. Berthomieu, G. Berger, and E. Nabedryk. 1994. The binding-sites of quinones in photosynthetic bacterial reaction centers investigated by light-induced FTIR difference spectroscopy - assignment of the Q(a) vibrations in Rhodobacter sphaeroides using O-18-labeled or C-13-labeled ubiquinone and vitamin-K-1. Biochemistry. 33:4953-4965.
59. Breton, J., and E. Nabedryk. 1996. Protein-quinone interactions in the bacterial photosynthetic reaction center: light-induced FTIR difference spectroscopy of the quinone vibrations. Biochim. Biophys. Acta. 1275:84-90.
60. Breton, J., E. Nabedryk, J. P. Allen, and J. C. Williams. 1997. Electrostatic influence of Q(A) reduction on the IR vibrational mode of the 10a-ester C=O of H-A demonstrated by mutations at residues Glu L104 and Trp L100 in reaction centers from Rhodobacter sphaeroides. Biochemistry. 36:4515-4525.
61. Hamm, P., K. A. Gray, D. Oesterhelt, R. Feick, H. Scheer, and W. Zinth. 1993. Subpicosecond emission studies of bacterial reaction centers. Biochim. Biophys. Acta. 1142:99-105.
62. Arlt, T., S. Schmidt, W. Kaiser, C. Lauterwasser, M. Meyer, H. Scheer, and W. Zinth. 1993. The accessory bacteriochlorophyll-a real electron carrier in primary photosynthesis. Proc. Natl. Acad. Sci. USA. 90:11757-11761.
63. Jia, Y. W., D. M. Jonas, T. H. Joo, Y. Nagasawa, M. J. Lang, and G. R. Fleming. 1995. Observation of ultrafast energy transfer from the accessory bacteriochlorophylls to the special pair in photosynthetic reaction centers. J. Phys. Chem. 99:6263-6266.
64. Beekman, L. M. P., R. W. Visschers, R. Monshouwer, M. Heerdawson, T. A. Mattioli, P. McGlynn, C. N. Hunter, B. Robert, I. H. M. van Stokkum, R. van Grondelle, and M. R. Jones. 1995. Timeresolved and steady-state spectroscopic analysis of membranebound reaction centers from Rhodobacter sphaeroides - comparisons with detergent-solubilized complexes. Biochemistry. 34:14712-14721.
65. Robert, B., and M. Lutz. 1988. Proteic events following charge separation in the bacterial reaction center: resonance Raman spectroscopy. Biochemistry. 27:5108-5114.
66. Breton, J., and E. Nabedryk. 1993. S0-T1 infrared difference spectrum of the triplet-state of the primary electron-donor in Rhodobacter sphaeroides photosynthetic bacterial reaction centers. Chem. Phys. Lett. 213:571-575.
67. Hartwich, G., C. Geskes, H. Scheer, J. Heinze, and W. Mantele. 1995. Fourier transform infrared spectroscopy of electrogenerated anions and cations of metal-substituted bacteriochlorophyll a. J. Am. Chem. Soc. 117:7784-7790.
68. Breton, J., J. Burie, C. Berthomieu, D. L. Thibodeau, S. Andiranambinintsoa, D. Dejonghe, G. Berger, and E. Nabedryk. 1992. Exploring the primary electron acceptor QA. In The Photosynthetic Bacterial Reaction Center II. Structure, Spectroscopy and Dynamics. J. Breton, editor. Plenum Press, New York. 155-162.
69. Adolphs, J., T. Renger, F. Muh, and M. Madjet. 2007. Theory of optical spectra - how proteins control excitation energy transfer. Photosynth. Res. 91:161-162.
70. Brudler, R., H. J. M. de Groot, W. B. S. van Liemt, W. F. Steggerda, R. Esmeijer, P. Gast, A. J. Hoff, J. Lugtenburg, and K. Gerwert. 1994. Asymmetric binding of the 1-C=0 and 4-C=0 groups of Q(a) in Rhodobacter sphaeroides-R26 reaction centers monitored by Fouriertransform infrared-spectroscopy using site-specific isotopically labeled ubiquinone-10. EMBO J. 13:5523-5530.
71. Vos, M. H., M. R. Jones, C. N. Hunter, J. Breton, J. C. Lambry, and J. L. Martin. 1994. Coherent dynamics during the primary electrontransfer reaction in membrane-bound reaction centers of Rhodobacter sphaeroides. Biochemistry. 33:6750-6757.