Energy transfer in light-adapted photosynthetic membranes: From active to saturated photosynthesis

Biophysical Journal

Volumn 97, Issue 9, 2009, Pages 2464-2473

  Fassioli, Francesca ^a   Olaya Castro, Alexandra ^b   Scheuring, Simon ^c   Sturgis, James N ^d   Johnson, Neil F ^e  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c INSTITUT CURIE   (France)

^d AIX MARSEILLE UNIVERSITY   (France)

^e UNIVERSITY OF MIAMI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ENERGY TRANSFER; IN VIVO STUDY; LIGHT ADAPTATION; NONHUMAN; PERFORMANCE MEASUREMENT SYSTEM; PHOTOSYNTHESIS; RHODOSPIRILLUM; RHODOSPIRILLUM PHOTOMETRICUM;

BACTERIA (MICROORGANISMS); RHODOSPIRILLUM PHOTOMETRICUM;

EID: 70349258427     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.08.033     Document Type: Article

References (49)

1. Vredenberg, W. J., and L. N. M. Duysens. 1963. Transfer of energy from bacteriochlorophyll to a reaction center during bacterial photosynthesis. Nature. 197:355-357.
2. Hu, X., T. Ritz, A. Damjanovic, F. Autenrieth, and K. Schulten. 2002. Photosynthetic apparatus of purple bacteria. Q. Rev. Biophys. 35:1-62.
3. Cogdell, R. J., A. Gall, and J. Köhler. 2006. The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes. Q. Rev. Biophys. 39:227-324.
4. van Amerongen, H., L. Valkunas, and R. van Grondelle. 2000. Photosynthetic Excitons. World Scientific, Singapore.
5. Deisenhofer, J., O. Epp, K. Miki, R. Huber, and H. Michel. 1985. Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 Å resolution. Nature. 318:618-624. (Pubitemid 16172409)
6. Woodbury, N. W., M. 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.
7. Martin, J. L., J. Breton, A. J. Hoff, A. Migus, and A. Antonetti. 1986. Femtosecond spectroscopy of electron transfer in the reaction center of the photosynthetic bacterium Rhodopseudomonas sphaeroides R-26: direct electron transfer from the dimeric bacteriochlorophyll primary donor to the bacteriopheophytin acceptor with a time constant of 2.8 ± 0.2 psec. Proc. Natl. Acad. Sci. USA. 83:957-961.
8. Frenkel, A. 1954. Light-induced phosphorylation by cell-free preparations of photosynthetic bacteria. J. Am. Chem. Soc. 76:5568-5569.
9. Bay, Z., and R. M. Pearlstein. 1963. A theory of energy transfer in the photosynthetic unit. Proc. Natl. Acad. Sci. USA. 50:1071-1078.
10. Knox, R. S. 1968. On the theory of trapping of excitation in the photosynthetic unit. J. Theor. Biol. 21:244-259.
11. Hemenger, R. P., R. M. Pearlstein, and K. Lakatos-Lindenberg. 1972. Incoherent exciton quenching on lattices. J. Math. Phys. 13:1056-1063.
12. Pearlstein, R. M. 1982. Exciton migration and trapping in photosynthesis. Photochem. Photobiol. 35:835-844.
13. Kudzmauskas, S., L. Valkunas, and A. Y. Borisov. 1983. A theory of excitation transfer in photosynthetic units. J. Theor. Biol. 105:13-23.
14. Owens, T. G., S. P. Webb, L. Mets, R. S. Alberte, and G. R. Fleming. 1987. Antenna size dependence of fluorescence decay in the core antenna of photosystem I: estimates of charge separation and energy transfer rates. Proc. Natl. Acad. Sci. USA. 84:1532-1536.
15. Kleinherenbrink, F. A. M., G. Deinum, S. C. M. Otte, A. J. Hoff, and J. Amesz. 1992. Energy-transfer from long-wavelength absorbing antenna bacteriochlorophylls to the reaction center. Biochim. Biophys. Acta. 1099:175-181.
16. Pullerits, T., and A. Freiberg. 1992. Kinetic model of primary energy transfer and trapping in photosynthetic membranes. Biophys. J. 63: 879-896.
17. Scheuring, S., J. Seguin, S. Marco, D. Lévy, B. Robert, et al. 2003. Nanodissection and high-resolution imaging of the Rhodopseudomonas viridis photosynthetic core complex in native membranes by AFM. Proc. Natl. Acad. Sci. USA. 100:1690-1693.
18. Scheuring, S., J. N. Sturgis, V. Prima, A. Bernadac, D. Lévy, et al. 2004. Watching the photosynthetic apparatus in native membranes. Proc. Natl. Acad. Sci. USA. 101:11293-11297.
19. Scheuring, S., and J. N. Sturgis. 2005. Chromatic adaptation of photosynthetic membranes. Science. 309:484-487.
20. Bahatyrova, S., R. N. Frese, C. A. Siebert, J. D. Olsen, K. O. van Der Werf, et al. 2004. The native architecture of a photosynthetic membrane. Nature. 430:1058-1062.
21. Scheuring, S., and J. N. Sturgis. 2009. Atomic force microscopy of the bacterial photosynthetic apparatus: plain pictures of an elaborate machinery. Photosynth. Res. In press.
22. Ritz, T., S. Park, and K. Schulten. 2001. Kinetics of excitation migration and trapping in the photosynthetic unit of purple bacteria. J. Phys. Chem. B. 105:8259-8267.
23. Şener, M. K., J. D. Olsen, C. N. Hunter, and K. Schulten. 2007. Atomic-level structural and functional model of a bacterial photosynthetic membrane vesicle. Proc. Natl. Acad. Sci. USA. 104:15723-15728.
24. Godik, V. I., and A. Y. Borisov. 1977. Excitation trapping by different states of photosynthetic reaction centers. FEBS Lett. 82:355-358.
25. McDermott, G., S. M. Prince, A. A. Freer, A. M. Hawthornthwaite-Lawless, M. Z. Papiz, et al. 1995. Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature. 374:517-521.
26. Scheuring, S., J. L. Rigaud, and J. N. Sturgis. 2004. Variable LH2 stoichiometry and core clustering in native membranes of Rhodospirillum photometricum. EMBO J. 23:4127-4133. (Pubitemid 39546151)
27. Sturgis, J. N., C. N. Hunter, and R. A. Niederman. 1988. Spectra and excitation coefficients of near-infrared absorption bands in membranes of Rhodobacter sphaeroides mutants lacking light-harvesting and reaction center complexes. Photochem. Photobiol. 48:243-247.
28. Lakowicz, J. R. 2006. Principles of Fluorescence Spectroscopy, 3rd Ed. Springer, New York.
29. Milano, F., A. Agostiano, F. Mavelli, and M. Trotta. 2003. Kinetics of the quinone binding reaction at the QB site of reaction centers from the purple bacteria Rhodobacter sphaeroides reconstituted in liposomes. Eur. J. Biochem. 270:4595-4605.
30. Gerencsér, L., G. Laczkó, and P. Maróti. 1999. Unbinding of oxidized cytochrome c from photosynthetic reaction center of Rhodobacter sphaeroides is the bottleneck of fast turnover. Biochemistry. 38:16866-16875. (Pubitemid 30013692)
31. - membranes. J. Biol. Chem. 280:11214-11223.
32. Osváth, S., and P. Maróti. 1997. Coupling of cytochrome and quinone turnovers in the photocycle of reaction centers from the photosynthetic bacterium Rhodobacter sphaeroides. Biophys. J. 73:972-982. (Pubitemid 27337632)
33. Allen, J. P., and J. C. Williams. 1995. Relationship between the oxidation potential of the bacteriochlorophyll dimer and electron-transfer in photosynthetic reaction centers. J. Bioenerg. Biomembr. 27:275-283.
34. Mascle-Allemand, C., J. Lavergne, A. Bernadac, and J. N. Sturgis. 2008. Organization and function of the Phaeospirillum molischianum photosynthetic apparatus. Biochim. Biophys. Acta. 1777:1552-1559.
35. Borisov, A. Y., A. M. Freiberg, V. I. Godik, K. K. Rebane, and K. E. Timpmann. 1985. Kinetics of picosecond bacteriochlorophyll luminescence in vivo as a function of the reaction center state. Biochim. Biophys. Acta. 807:221-229.
36. Campillo, A. J., R. C. Hyer, T. G. Monger, W. W. Parson, and S. L. Shapiro. 1977. Light collection and harvesting processes in bacterial photosynthesis investigated on a picosecond time scale. Proc. Natl. Acad. Sci. USA. 74:1997-2001.
37. Şener, M. K., and K. Schulten. 2005. Physical principles of efficient excitation transfer in light harvesting. In Energy Harvesting Materials. World Scientific, Singapore.
38. Hess, S., M. Chachisvilis, K. Timpmann, M. R. Jones, G. J. S. Fowler, et al. 1995. Temporally and spectrally resolved subpicosecond energy transfer within the peripheral antenna complex (LH2) and from LH2 to the core antenna complex in photosynthetic purple bacteria. Proc. Natl. Acad. Sci. USA. 92:12333-12337.
39. Timpmann, K., F. G. Zhang, A. Freiberg, and V. Sundström. 1993. Detrapping of excitation energy from the reaction center in the photosynthetic purple bacterium Rhodospirillum rubrum. Biochim. Biophys. Acta. 1183:185-193.
40. Scheuring, S., and J. N. Sturgis. 2006. Dynamics and diffusion in photosynthetic membranes from Rhodospirillum photometricum. Biophys. J. 91:3707-3717. (Pubitemid 44788313)
41. Geyer, T., and V. Helms. 2006. Reconstruction of a kinetic model of the chromatophore vesicles from Rhodobacter sphaeroides. Biophys. J. 91:927-937. (Pubitemid 44161925)
42. Trissl, H. W., C. J. Law, and R. J. Cogdell. 1999. Uphill energy transfer in LH2-containing purple bacteria at room temperature. Biochim. Biophys. Acta. 1412:149-172.
43. Paillotin, G. 1976. Capture frequency of excitations and energy transfer between photosynthetic units in the photosystem II. J. Theor. Biol. 58:219-235.
44. Paillotin, G. 1976. Movement of excitations in the photosynthetic domains of photosystem II. J. Theor. Biol. 58:237-252.
45. Lavergne, J., and H. W. Trissl. 1995. Theory of fluorescence induction in photosystem-II-derivation of analytical expressions in a model including exciton-radical-pair equilibrium and restricted energy-transfer between photosynthetic units. Biophys. J. 68:2474-2492.
46. Comayras, F., C. Jungas, and J. Lavergne. 2005. Functional consequences of the organization of the photosynthetic apparatus in Rhodobacter sphaeroides. I. Quinone domains and excitation transfer in chromatophores and reaction center antenna complexes. J. Biol. Chem. 280:11203-11213.
47. Şener, M. K., J. Hsin, L. G. Trabuco, E. Villa, P. Qian, et al. 2009. Structural model and excitonic properties of the dimeric RC-LH1-PufX complex from Rhodobacter sphaeroides. Chem. Phys. 357:188-197.
48. Fujii, R., S. Shimonaka, N. Uchida, A. T. Gardiner, R. J. Cogdell, et al. 2008. Construction of hybrid photosynthetic units using peripheral and core antennae from two different species of photosynthetic bacteria: detection of the energy transfer from bacteriochlorophyll-a in LH2 to bacteriochlorophyll-b in LH1. Photosynth. Res. 95:327-337.
49. Escalante, M., Y. Zhao, M. J. W. Ludden, R. Vermeij, J. D. Olsen, et al. 2008. Nanometer arrays of functional light harvesting antenna complexes by nanoimprint lithography and host-guest interactions. J. Am. Chem. Soc. 130:8892-8893.