Charge separation, stabilization, and protein relaxation in photosystem II core particles with closed reaction Center

Biophysical Journal

Volumn 96, Issue 2, 2009, Pages 621-631

  Szczepaniak, M ^a   Sander, J ^b   Nowaczyk, M ^b   Muller M G ^a   Rogner, M ^b   Holzwarth, A R ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ENERGY CONVERSION   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYANOBACTERIA;

EID: 58849120026     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2008.09.036     Document Type: Article

References (69)

1. Barber, J. 2003. Photosystem II: the engine of life. Q. Rev. Biophys. 36:71-89.
2. Barber, J. 2006. Photosystem II: an enzyme of global significance. Biochem. Soc. Trans. 34:619-631.
3. Ferreira, K. N., T. M. Iverson, K. Maghlaoui, J. Barber, and S. Iwata. 2004. Architecture of the photosynthetic oxygen-evolving center. Science. 303:1831-1838.
4. Loll, B., J. Kern, W. Saenger, A. Zouni, and J. Biesiadka. 2005. Towards complete cofactor arrangement in the 3.0 angstrom resolution structure of photosystem II. Nature. 438:1040-1044.
5. Diner, B. A., and F. Rappaport. 2002. Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu. Rev. Plant Biol. 53:551-580.
6. Dekker, J. P., and R. van Grondelle. 2000. Primary charge separation in photosystem II. Photosynth. Res. 63:195-208.
7. Renger, G., and A. R. Holzwarth. 2005. Primary electron transfer. In Photosystem II: The Light-Driven Water: Plastoquinone Oxidoreductase. T. J. Wydrzynski and K. Satoh, editors. Springer Netherlands, Berlin. 139-175.
8. Holzwarth, A. R., M. G. Müller, M. Reus, M. Nowaczyk, J. Sander, et al. 2006. Kinetics and mechanism of electron transfer in intact photo-system II and in the isolated reaction center: pheophytin is the primary electron acceptor. Proc. Natl. Acad. Sci. USA. 103:6895-6900.
9. Groot, M. -L., N. P. Pawlowicz, L. J. G. W. van der Wilderen, J. Breton, I. H. M. van Stokkum, et al. 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.
10. Prokhorenko, V. I., and A. R. Holzwarth. 1998. Primary charge separation at low temperatures in D1-D2 reaction centers, studied by photon echo and pump-probe spectroscopy. In Photosynthesis: Mechanism and Effects. G. Garab, editor. Kluwer Academic Publishers, Dordrecht. 1033-1036.
11. Schlodder, E., T. Renger, G. Raszewski, W. J. Coleman, P. J. Nixon, et al. 2008. Site-directed mutations at D1-Thr179 of photosystem II in Synechocystis sp PCC 6803 modify the spectroscopic properties of the accessory chlorophyll in the D1-branch of the reaction center. Biochemistry. 47:3143-3154.
12. Holzwarth, A. R., and T. A. Roelofs. 1992. Recent advances in the understanding of chlorophyll excited state dynamics in thylakoid membranes and isolated reaction centre complexes. J. Photochem. Pho-tobiol. B. 15:45-62.
13. Roelofs, T. A., C. -H. Lee, and A. R. Holzwarth. 1992. Global target analysis of picosecond chlorophyll fluorescence kinetics from pea chloroplasts. A new approach to the characterization of the primary processes in photosystem II α- and β-units. Biophys. J. 61:1147-1163.
14. 2-evolving photosystem II complexes from Synechococcus. Bio-chim. Biophys. Acta. 933:22-34.
15. Roelofs, T. A., and A. R. Holzwarth. 1990. In search of a putative long-lived relaxed radical pair state in closed photosystem II. Kinetic modeling of picosecond fluorescence data. Biophys. J. 57:1141-1153.
16. Schatz, G. H., H. Brock, and A. R. Holzwarth. 1987. Picosecond kinetics of fluorescence and absorbance changes in photosystem II particles excited at low photon density. Proc. Natl. Acad. Sci. USA. 84:8414-8418.
17. Schatz, G. H., H. Brock, and A. R. Holzwarth. 1988. A kinetic and energetic model for the primary processes in photosystem II. Biophys. J. 54:397-405.
18. Gibasiewicz, K., A. Dobek, J. Breton, and W. Leibl. 2001. Modulation of primary radical pair kinetics and energetics in photosystem II by the redox state of the quinone electron acceptor Q(A). Biophys. J. 80:1617-1630.
19. Vassiliev, S., C. -I. Lee, G. W. Brudvig, and D. Bruce. 2002. Structure-based kinetic modeling of excited-state transfer and trapping in histidine-tagged photosystem II core complexes from Synechocystis. Biochemistry. 41:12236-12243.
20. Nuijs, A. M., H. J. van Gorkom, J. J. Plijter, and L. N. M. Duysens. 1986. Primary-charge separation and excitation of chlorophyll a in photosystem II particles from spinach as studied by picosecond absor-bance-difference spectroscopy. Biochim. Biophys. Acta. 848:167-175.
21. A on the fluorescence decay kinetics of photosystem II. Biochim. Biophys. Acta. 1100:198-206.
22. A in photosystem II. Biochim. Biophys. Acta. 1183:388-396.
23. Miloslavina, Y., M. Szczepaniak, M. G. Müller, J. Sander, M. Nowaczyk, et al. 2006. Charge separation kinetics in intact photosystem II core particles is trap-limited. A picosecond fluorescence study. Biochemistry. 45:2436-2442.
24. Andrizhiyevskaya, E. G., D. Frolov, R. van Grondelle, and J. P. Dekker. 2004. On the role of the CP47 core antenna in the energy transfer and trapping dynamics of photosystem II. Phys. Chem. Chem. Phys. 6:4810-4819.
25. Schelvis, J. P. M., M. Germano, T. J. Aartsma, and H. J. van Gorkom. 1995. Energy transfer and trapping in photosystem II core particles with closed reaction centers. Biochim. Biophys. Acta. 1230:165-169.
26. Vasil'ev, S., P. Orth, A. Zouni, T. G. Owens, and D. Bruce. 2001. Excited-state dynamics in photosystem II: Insights from the x-ray crystal structure. Proc. Natl. Acad. Sci. USA. 98:8602-8607.
27. Holzwarth, A. R., and M. G. Müller. 1996. Energetics and kinetics of radical pairs in reaction centers from Rhodobacter sphaeroides. A femtosecond transient absorption study. Biochemistry. 35:11820-11831.
28. Müller, M. G., G. Drews, and A. R. Holzwarth. 1996. Primary charge separation processes in reaction centers of an antenna-free mutant of Rhodobacter capsulatus. Chem. Phys. Lett. 258:194-202.
29. Woodbury, N. W., J. M. Peloquin, R. G. Alden, X. Lin, S. Lin, et al. 1994. Relationship between thermodynamics and mechanism during photoinduced charge separation in reaction centers from Rhodobacter sphaeroides. Biochemistry. 33:8101-8112.
30. Peloquin, J. M., J. C. Williams, X. Lin, R. G. Alden, A. K. W. Taguchi, et al. 1994. Time-dependent thermodynamics during early transfer in reaction centers from Rhodobacter sphaeroides. Biochemistry. 33:8089-8100.
31. Goushcha, A. O., M. T. Kapoustina, V. N. Kharkyanen, and A. R. Holz-warth. 1997. Nonlinear dynamic processes in an ensemble of photosynthetic reaction centers. Theory and experiment. J. Phys. Chem. B. 101:7612-7619.
32. Goushcha, A. O., A. R. Holzwarth, and V. N. Kharkyanen. 1999. Self-regulation phenomenon of electron-conformational transitions in biological electron transfer under nonequilibrium conditions. Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics. 59:3444-3452.
33. Kleinfeld, D., M. Y. Okamura, and G. Feher. 1984. 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.
34. 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.
35. Goushcha, A. O., A. J. Manzo, V. N. Kharkyanen, R. van Grondelle, and G. W. Scott. 2004. Light-induced equilibration kinetics in membrane-bound photosynthetic reaction centers: nonlinear dynamic effects in multiple scattering media. J. Phys. Chem. B. 108:2717-2725.
36. Kriegl, J. M., and G. U. Nienhaus. 2004. Structural, dynamic, and energetic aspects of long-range electron transfer in photosynthetic reaction centers. Proc. Natl. Acad. Sci. USA. 101:123-128.
37. Booth, P. J., B. Crystall, L. B. Giorgi, J. Barber, D. R. Klug, and G. Porter. 1990. Thermodynamic properties of D1/D2/cytochrome B-559 reaction centers investigated by time-resolved fluorescence measurements. Biochim. Biophys. Acta. 1016:141-152.
38. Roelofs, T. A., S. L. S. Kwa, R. van Grondelle, J. P. Dekker, and A. R. Holzwarth. 1993. Primary processes and structure of the photosystem II reaction center: II. Low-temperature picosecond fluorescence kinetics of a D1-D2-cyt-b-559 reaction center complex isolated by short Triton exposure. Biochim. Biophys. Acta. 1143:147-157.
39. 559 complex at 77K. J. Phys. Chem. B. 101:2933-2944.
40. Hsu, B. D., J. Y. Lee, and R. L. Pan. 1986. The two binding sites for DCMU in photosystem II. Biochem. Biophys. Res. Commun. 141:682-688.
41. Wraight, C. A. 1981. Oxidation-reduction physical chemistry of the acceptor quinone complex in bacterial photosynthetic reaction centers: evidence for anew model of herbicide activity. Isr. J. Chem. 21:348-354.
42. Müller, M. G., K. Griebenow, and A. R. Holzwarth. 1992. Primary processes in isolated bacterial reaction centers from Rhodobacter sphaeroides studied by picosecond fluorescence kinetics. Chem. Phys. Lett. 199:465-469.
43. Holzwarth, A. R. 1996. Data analysis of time-resolved measurements. In Biophysical Techniques in Photosynthesis. Advances in Photosynthesis Research. J. Amesz and A. J. Hoff, editors. Kluwer Academic Publishers, Dordrecht, The Netherlands. 75-92.
44. 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.
45. Arsköld, S. P., B. J. Prince, E. Krausz, P. J. Smith, R. J. Pace, et al. 2004. Low-temperature spectroscopy of fully active PSII cores. Comparisons with CP43, CP47, D1/D2/cyt b(559) fragments. J. Lumin. 108:97-100.
46. Müller, M. G., J. Niklas, W. Lubitz, and A. R. Holzwarth. 2003. Ultra-fast transient absorption studies on photosystem I reaction centers from Chlamydomonas reinhardtii. 1. A new interpretation of the energy trapping and early electron transfer steps in photosystem I. Biophys. J. 85:3899-3922.
47. Ishikita, H., J. Biesiadka, B. Loll, W. Saenger, and E. -W. Knapp. 2006. Cationic state of accessory chlorophyll and electron transfer through pheophytin to plastoquinone in photosystern II. Angew. Chem. Int. Ed. 45:1964-1965.
48. Martinez-Junza, V., M. Szczepaniak, S. E. Braslavsky, J. Sander, M. Rogner, et al. 2008. A new photoprotection mechanism in photosystem II cores with closed reaction center. Photochem. Photobiol. Sci. 7: 1337-1343.
49. Wang, H. Y., S. Lin, J. P. Allen, J. C. Williams, S. Blankert, et al. 2007. Protein dynamics control the kinetics of initial electron transfer in photosynthesis. Science. 316:747-750.
50. Ehrenberg, A. 2004. Protein dynamics and reactions of photosystem II. Biochim. Biophys. Acta. 1655:231-234.
51. 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.
52. Katiliene, Z., E. Katilius, and N. W. Woodbury. 2003. Energy trapping and detrapping in reaction center mutants from Rhodobacter sphaeroides. Biophys. J. 84:3240-3251.
53. 559 complex measured by time-resolved fluorescence. J. Phys. Chem. 100:7269-7278.
54. Barter, L. M. C., and D. R. Klug. 2005. A unified picture of energy and electron transfer in primary photosynthesis. Chem. Phys. 319:308-315.
55. A redox potential? J. Photochem. Photobiol. A Chem. 142:127-132.
56. Parak, F., and H. Frauenfelder. 1993. Protein dynamics. Physica A. 201:332-345.
57. Nienhaus, G. U., J. R. Mourant, and H. Frauenfelder. 1992. Spectro-scopic evidence for conformational relaxation in myoglobin. Proc. Natl. Acad. Sci. USA. 89:2902-2906.
58. Frauenfelder, H., S. G. Sligar, and P. G. Wolynes. 1991. The energy landscapes and motions of proteins. Science. 254:1598-1603.
59. Papageorgiou, G., M. Tsimilli-Michael, and K. Stamatakis. 2007. The fast and slow kinetics of chlorophyll a fluorescence induction in plants, algae and cyanobacteria: a viewpoint. Photosynth. Res. 94:275-290.
60. Govindjee 2004. Chlorophyll a fluorescence: a bit of basics and history. In Chlorophyll a Fluorescence: A Signature of Photosynthesis. G. C. Papageorgiou and Govindjee., editors. Springer, Dordrecht. 1-42.
61. Maxwell, K., and G. N. Johnson. 2000. Chlorophyll fluorescence - a practical guide. J. Exp. Bot. 51:659-668.
62. Govindjee, and G. C. Papageorgiou. 1971. Chlorophyll fluorescence and photosynthesis: fluorescence transients. In Photophysiology. 6th ed. A. C. Giese, editor. Academic Press, New York. 1-46.
63. Lazar, D. 1999. Chlorophyll a fluorescence induction. Biochim. Biophys. Acta. 1412:1-28.
64. Krause, G. H., and E. Weis. 1991. Chlorophyll fluorescence and photosynthesis: the basics. Annu. Rev. Plant Physiol. 42:313-349.
65. Telfer, A. 2005. Too much light? How β-carotene protects the photo-system II reaction centre. Photochem. Photobiol. Sci. 4:950-956.
66. Hanley, J., Y. Deligiannakis, A. Pascal, P. Faller, and A. W. Rutherford. 1999. Carotenoid oxidation in photosystem II. Biochemistry. 38:8189-8195.
67. Rutherford, A. W., A. Boussac, and P. Faller. 2004. The stable tyrosyl radical in photosystem II: why D? Biochim. Biophys. Acta. 1655:222-230.
68. Johnson, G. N., A. Boussac, and A. W. Rutherford. 1994. The origin of 40-50°C thermoluminescence bands in photosystem II. Biochim. Biophys. Acta. 1184:85-92.
69. Raszewski, G., and T. Renger. 2008. Light harvesting in photosystem II core complexes is limited by the transfer to the trap: can the core complex turn into a photoprotective mode? J. Am. Chem. Soc. 130:4431-4446.