The light–arvesting apparatus in purple photosynthetic bacteria introduction to a quantum biological device

Molecular Machines

Volumn , Issue , 2011, Pages 19-48

  Strümpfer, Johan ^a   Hsin, Jen ^a,b   Şener, Melih ^a,b   Chandler, Danielle ^a,b   Schulten, Klaus ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b University of Illinois at Urbana Champaign   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84954242628     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1142/9789814343466_0002     Document Type: Chapter

References (99)

1. M. K. §ener and K. Schulten. 2008. From atomic-level structure to supramolecular organization in the photosynthetic unit of purple bacteria. in The Purple Phototrophic Bacteria, C. N. Hunter, F. Daldal, M. C. Thurnauer and J. T. Beatty, eds., Vol. 28 of Advances in Photosynthesis and Respiration, 275-294, Springer.
2. X. Hu and K. Schulten. 1997. How nature harvests sunlight. Physics Today 50, 28-34.
3. K. Schulten. 1999. From simplicity to complexity and back: Function, architecture and mechanism of light harvesting systems in photosynthetic bacteria. in Simplicity and Complexity in Proteins and Nucleic Acids, H. Frauenfelder, J. Deisenhofer, and P. G. Wolynes, eds. (Berlin), 227-253, Dahlem University Press (pdf available from author upon request).
4. R. J. Cogdell, 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. Quart Rev Biophys 39, 227-324.
5. R. E. Blankenship. 2002. Molecular Mechanisms of Photosynthesis. Malden, MA: Blackwell Science.
6. X. Hu, T. Ritz, A. Damjanovic, F. Autenrieth and K. Schulten. 2002. Photosynthetic apparatus of purple bacteria. Quart Rev Biophys 35, 1-62.
7. T. Förster. 1948. Zwischenmolekulare Energiewanderung und Fluoreszenz. Ann Phys (Leipzig) 2, 55-75.
8. D. Dexter. 1953. A theory of sensitized luminescence in solids. J Chem Phys 21, 836-850.
9. A. Damjanovic, T. Ritz and K. Schulten. 1999. Energy transfer between carotenoids and bacteri-ochlorophylls in a light harvesting protein. Phys Rev E 59, 3293-3311.
10. T. Ritz, A. Damjanovic, K. Schulten, J. Zhang and Y. Koyama. 2000. Efficient light harvesting through carotenoids. Photosyn Res 66, 125-144.
11. A. R. Crofts, B. Barquera, G. Bechmann, M. Guergova, R. Salcedo-Hemandez, B. Hacker, S. Hong and R. B. Gennis. 1995. Structure and function in the bc1-complex of rb. sphaeroides. in Photosynthesis: From light to biosphere, P. Mathis, ed. Kluwer Academic Publ, Dordrecht.
12. S. Bahatyrova, R. N. Frese, C. A. Siebert, J. D. Olsen, K. O. van der Werf, R. van Grondelle, R. A. Niederman, P. A. Bullough, C. Otto and C. N. Hunter. 2004. The native architecture of a photosynthetic membrane, Nature 430, 1058-1062.
13. M. K. Sener, 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 US A 104, 15723-15728.
14. M. Sener, J. Strumpfer, J. A. Timney, A. Freiberg, C. N. Hunter and K. Schulten. 2010. Photosynthetic vesicle architecture and constraints on efficient energy harvesting. Biophys J 99, 67-75.
15. J. Xiong, W. M. Fischer, K. Inoue, M. Nakahara and C. E. Bauer. 2000. Molecular evidence for the early evolution of photosynthesis. Science 289, 1724-1730.
16. R. Emerson and A. Arnold. 1932. The photochemical reaction in photosynthesis. J Gen Physiol 16, 191-205.
17. T. Förster. 1948. Zwischenmolekulare Energiewanderung und Fluoreszenz. Ann Phys (Leipzig), 2, 55-75.
18. J. R. Oppenheimer. 1941. Internal conversion in photosynthesis. in Proceedings of the American Physical Society, vol. 60 of Phys Rev p. 158.
19. W. Arnold and J. R. Oppenheimer. 1950. Internal conversion in the photosynthetic mechanism of blue-green algae. J Gen Physiol 33, 423-435.
20. J. Deisenhofer, O. Epp, K. Mikki, R. Huber and H. Michel. 1985. Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 A resolution. Nature 318, 618-624.
21. R. A. Marcus. 1956. On the energy of oxidation-reduction reactions involving electron transfer. I. J Chem Phys 24, 966-978.
22. R. A. Marcus. 1956. Electrostatic free energy and other properties of states having nonequilibrium polarization. II, J Chem Phys 24, 979-989.
23. W. L. Liang. 1970. Excitons. Phys Educ 5, 226.
24. J. Frenkel. 1931. On the transformation of light into heat in solids. Phys Rev 37, 17-44.
25. G. McDermott, S. M. Prince, A. A. Freer, A. M. Hawthornthwaite-Lawless, M. Z. Papiz, R. J. Cogdell and N. W. Isaacs. 1995. Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374, 517-521.
26. S. Karrasch, P. Bullough and R. Ghosh. 1995. The 8.5 Â projection map of the light-harvesting complex I from Rho do spirillum rubrum reveals a ring composed of 16 sub-units. EMBO J 14, 631.
27. X. Hu, D. Xu, K. Hamer, K. Schulten, J. Koepke and H. Michel. 1995. Predicting the structure of the light-harvesting complex II of Rhodospirillum molischianum. Prot Sci 4, 1670-1682.
28. J. Koepke, X. Hu, C. Muenke, K. Schulten and H. Michel. 1996. The crystal structure of the light harvesting complex II (B800-850) from Rhodospirillum molischianum. Structure 4, 581-597.
29. M. Z. Papiz, S. M. Prince, T. Howard, R. J. Cogdell and N. W. Isaacs. 2003. The structure and thermal motion of the B800-850 LH2 complex from Rps. acidophila at 2.0 Â resolution and 100 K: New structural features and functionally relevant motions. J Mol Biol 326, 1523-1538.
30. J. Allen, T. Yeates, H. Komiya and D. Rees. 1987. Structure of the reaction center from Rhodobacter sphaeroides R-26: The protein subunits. Proc Natl Acad Sci U S A 84, 6162-6166.
31. K. J. Visscher, H. Bergstrom, V. Sundström, C. Hunter and R. van Grondelle. 1989. Temperature dependence of energy transfer from the long wavelength antenna Bchl-896 to the reaction center in Rhodospirillum rubrum, Rhodobacter sphaeroides (w.t. and M21 mutant) from 77 to 177 K, studied by picosecond absorption spectroscopy. Photosynthesis Research 22, 211-217.
32. U. Ermler, G. Fritzsch, S. K. Buchanan and H. Michel. 1994. Structure of the photosynthetic reaction center from Rhodobacter sphaeroides at 2.65 Â resolution: Cofactors and protein-cofactor interactions. Structure 2, 925-936.
33. M. J. Conroy, W. Westerhuis, P. S. Parkes-Loach, P. A. Loach, C. N. Hunter and M. P. Williamson. 2000. The solution structure of the Rhodobacter sphaeroides LH1 ß reveals two helical domains separated by a more flexible region: Structural consequences for the LH1 complex. J Mol Biol 298, 83-94.
34. A. Camara-Artigas, D. Brune and J. P. Allen. 2002. Interactions between lipids and bacterial reaction centers determined by protein crystallography. Proc Natl Acad Sci U S A 99, 11055-11060.
35. A. W. Roszak, T. Howard, J. Southall, A. T. Gardiner, C. J. Law, N. W. Isaacs and R. J. Cogdell. 2003. Crystal structure of the RC-LH1 core complex from Rhodopseudomonas palustris. Science 302, 1969-1972.
36. D. Fotiadis, P. Qian, A. Philippsen, P. A. Bullough, A. Engel and C. N. Hunter. 2004. Structural analysis of the reaction center light-harvesting complex I photosynthetic core complex of Rhodospirillum rubrum using atomic force microscopy. J Biol Chem 279, 2063-2068.
37. G. Uyeda, A. Camara-Artigas, J. C. Williams and J. P. Allen. 2005. Design of a redox-linked active metal site: Manganese bound to bacterial reaction centers at a site resembling that of photosystem II. Biochemistry 44, 7389-7394.
38. 1 complex mutant from Rhodobacter sphaeroides. Biochim Biophys Acta 1757, 835-840.
39. H. L. Axelrod, E. C. Abresch, M. Y. Okamura, A. P. Yeh, D. C. Ress and G. Feher. 2002. X-ray structure determination of the cytochrome c2: Reaction center electron transfer complex from Rhodobacter sphaeroides. J Mol Biol 319, 501-515.
40. S. Scheuring, J. N. Sturgis, V. Prima, A. Bernadac, D. Levy and J.-L. Rigaud. 2004. Watching the photosynthetic apparatus in native membranes. Proc Natl Acad Sci U S A 91, 11293-11297.
41. R. N. Frese, C. A. Siebert, R. A. Niederman, C. N. Hunter, C. Otto and R. van Grondelle. 2004. The long-range organization of a native photosynthetic membrane. Proc Natl Acad Sci USA 101, 17994-17999.
42. S. Scheuring, D. Lévy and J.-L. Rigaud. 2005. Watching the components of photosynthetic bacterial membranes and their in situ organisation by atomic force microscopy. Biochim Biophys Acta 1712, 109-127.
43. C. Jungas, J. Ranck, J. Rigaud, P. Joliot and A. Verméglio. 1999. Supramolecular organization of the photosynthetic apparatus of Rhodobacter sphaeroides. EMBO J 18(3), 534-542.
44. S. J. Jamieson, P. Wang, P. Qian, J. Y. Kirkland, M. J. Conroy, C. N. Hunter and P. A. Bullough. 2002. Projection structure of the photosynthetic reaction centre-antenna complex of Rhodospirillum rubrum at 8.5 Â resolution. EMBO J 21, 3927-3935.
45. C. A. Siebert, P. Qian, D. Fotiadis, A. Engel, C. N. Hunter and P. A. Bullough. 2004. Molecular architecture of photosynthetic membranes in Rhodobacter sphaeroides: The role of PufX. EMBO J 23, 690-700.
46. P. Qian, C. N. Hunter and P. A. Bullough. 2005. The 8.5 Â projection structure of the core RC-LH1-PufX dimer of Rhodobacter sphaeroides. J Mol Biol 349, 948-960.
47. M. K. Sener, D. Lu, T. Ritz, S. Park, P. Fromme and K. Schulten. 2002. Robustness and optimality of light harvesting in cyanobacterial photosystem I. J Phys Chem B 106, 7948-7960.
48. A. G. Redfield. 1965. The theorie of relaxation process. Adv Magn Reson 1, 1.
49. A. O. Cardeira and A. J. Leggett. 1983. Quantum tunnelling in a dissipative system. J Ann Phys (N.Y.) 149, 374-456.
50. H. Sumi and R. A. Marcus. 1986. Dynamical effects in electron transfer reactions. J Chem Phys 84, 4894-4914.
51. A. Warshel, Z. T. Chu and W. W. Parson. 1989. Dispersed polaron simulations of electron transfer in photosynthetic reaction center. Science 246, 112-116.
52. Y. Tanimura and R. Kubo. 1989. Two-time correlation functions of a system coupled to a heat bath with a Gaussian-Markoffian interaction. J Phys Soc Jpn 58(4), 1199-1206.
53. S. Mukamel. 1995. Principles of Nonlinear Optical Spectroscopy. Oxford University Press, New York.
54. X. Hu, T. Ritz, A. Damjanovic and K. Schulten. 1997. Pigment organization and transfer of electronic excitation in the purple bacteria. J Phys Chem B 101, 3854-3871.
55. A. Damjanovic, I. Kosztin, U. Kleinekathoefer and K. Schulten. 2002. Excitons in a photosynthetic light-harvesting system: A combined molecular dynamics, quantum chemistry and polaron model study. Phys Rev E 65, 031919, (24 pages).
56. M. Sener and K. Schulten. 2002. A general random matrix approach to account for the effect of static disorder on the spectral properties of light harvesting systems. Phys Rev E 65, 031916, (12 pages).
57. A. Ishizaki and G. R. Fleming. 2009. Theoretical examination of quantum coherence in a photosynthetic system at physiological temperature. Proc Natl Acad Sci U S A 106(41), 17255.
58. J. Strümpfer and K. Schulten. 2009. Light harvesting complex II B850 excitation dynamics. J Chem Phys 131, 225101, (9 pages).
59. J. Hsin, J. Strumpfer, M. Sener, P. Qian, C. N. Hunter and K. Schulten. 2010. Energy transfer dynamics in an RC-LH1-PufX tubular photosynthetic membrane. New J Phys 12, 085005, (19 pages).
60. J. Strumpfer and K. Schulten. 2011. The effect of correlated bath fluctuations on exciton transfer. J Chem Phys 134, 095102-095111.
61. M. Sener and K. Schulten. 2005. Physical principles of efficient excitation transfer in light harvesting. in Energy Harvesting Materials (D. L. Andrews, ed.), pp. 1-26, World Scientific, Singapore.
62. T. Walz, S. J. Jamieson, C. M. Bowers, P. A. Bullough and C. N. Hunter. 1998. Projection structures of three photosynthetic complexes from Rhodobacter sphaeroides: LH2 at 6 Â, LH1 and RC-LH1 at 25 Â. JMol Biol 282, 833-845.
63. D. Chandler, J. Hsin, C. B. Harrison, J. Gumbart and K. Schulten. 2008. Intrinsic curvature properties of photosynthetic proteins in chromatophores. Biophys J 95, 2822-2836.
64. D. E. Chandler, J. Gumbart, J. D. Stack, C. Chipot and K. Schulten. 2009. Membrane curvature induced by aggregates of LH2s and monomeric LH1s. Biophys J 97, 2978-2984.
65. J. Hsin, D. E. Chandler, J. Gumbart, C. B. Harrison, M. Sener, J. Strumpfer and K. Schulten. 2010. Self-assembly of photosynthetic membranes. ChemPhysChem 11, 1154-1159.
66. N. Pfennig. 1967. Photosynthetic bacteria. Annu Rev Med 21, 285-324.
67. N. Pfennig. 1969. Rhodopseudomonas acidophila, sp. n., a new species of the budding purple nonsulfur bacteria. J Bacteriol 99(2), 597-602.
68. P. Qian, P. A. Bullough and C. N. Hunter. 2008. Three-dimensional reconstruction of a membranebending complex: The RC-LHl-PufX core dimer of Rhodobacter sphaeroides. J Biol Chem 283, 14002-14011.
69. J. Hsin, J. Gumbart, L. G. Trabuco, E. Villa, P. Qian, C. N. Hunter and K. Schulten. 2009. Protein-induced membrane curvature investigated through molecular dynamics flexible fitting. Biophys J 97, 321-329.
70. M. K. Sener, J. Hsin, L. G. Trabuco, E. Villa, P. Qian, C. N. Hunter and K. Schulten. 2009. Structural model and excitonic properties of the dimeric RC-LHl-PufX complex from Rhodobacter sphaeroides. Chem Phys 357, 188-197.
71. S. Scheuring, F. Francia, J. Busselez, B. A. Melandris, J.-L. Rigaud and D. Levy. 2004. Structural role of PufX in the dimerization of the photosynthetic core complex of Rhodobacter sphaeroides. J Biol Chem 279(5), 3620-3626.
72. S. Scheuring, J. Busselez and D. Levy. 2005. Structure of the dimeric PufX-containing core complex of Rhodobacter blasticus by in situ atomic force microscopy. J Biol Chem 280, 1426-1431.
73. J. Busselez, M. Cottevielle, P. Cuniasse, F. Gubellini, N. Boisset and D. Lévy. 2007. Structural basis for the PufX-mediated dimerization of bacterial photosynthetic core complexes. Structure 15, 1674-1683.
74. R. Frese, J. Olsen, R. Branvall, W. Westerhuis, C. Hunter and R. van Grondelle. 2000. The long-range supraorganization of the bacterial photosynthetic unit: A key role for PufX. Proc Natl Acad Sci U S A 97, 5197-5202.
75. S. Scheuring. 2006. AFM studies of the supramolecular assembly of bacterial photosynthetic corecomplexes. Curr Opin Chem Biol 10, 387-393.
76. J. Hsin, C. Chipot and K. Schulten. 2009. A glycophorin A-like framework for the dimerization of photosynthetic core complexes. J Am Chem Soc 131, 17096-17098.
77. X. Hu and K. Schulten. 1998. A model for the light-harvesting complex I (B875) of Rhodobacter sphaeroides. Biophys J 75, 683-694.
78. J. Deisenhofer and H. Michel. 1987. in The crystal structure of the photosynthetic reaction center from Rhodopseudomonas viridis (J. Breton and A. Vermeglio, eds.), The photosynthetic bacterial reaction center: Structure and dynamics, pp. 1-3, Plenum Press, London.
79. P. Jordan, P. Fromme, H. T. Witt, O. Klukas, W. Saenger and N. Krauß. 2001. Three-dimensional structure of cyanobacterial photosystem I at 2.5 Â resolution. Nature 411, 909-917.
80. A. Ben-Shem, F. Frolow and N. Nelson. 2003. Crystal structure of plant photosystem I. Nature 426, 630-635.
81. A. Guskov, J. Kern, A. Gabdulkhakov, M. Broser, A. Zouni and W. Saenger. 2009. Cyanobacterial photosystem II at 2.9-resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16(3), 334-342.
82. J. Tucker, C. Siebert, M. Escalante, P. Adams, J. Olsen, C. Otto, D. Stokes and C. Hunter. 2010. Membrane invagination in Rhodobacter sphaeroides is initiated at curved regions of the cytoplasmic membrane, then forms both budded and fully detached spherical vesicles. Mol Microbiol 76(4), 833-847.
83. C. N. Hunter, R. van Grondelle, N. G. Holmes, O. T. G. Jones and R. A. Niederman. 1985. Linear dichroism and fluorescence emission of antenna complexes during photosynthetic unit assembly in Rhodopseudomonas sphaeroides. Biochim Biophys Acta 807, 44-51.
84. M. Sener, J. Strumpfer, J. Hsin, D. Chandler, S. Scheuring, C. N. Hunter and K. Schulten. 2011. Förster energy transfer theory as reflected in the structures of photosynthetic light harvesting systems. Chem Phys Chem 12, 518-531.
85. T. Geyer and V. Helms. 2006. A spatial model of the chromatophore vesicles of Rhodobacter sphaeroides and the position of the cytochrome bcj complex. Biophys J 91, 921-926.
86. J. J. Sakurai. 1985. Modern quantum mechanics. Addison Wesley Publishing Company, Boston.
87. E. Fermi. 1950. Nuclear Physics. University of Chicago Press, Chicago.
88. V. May, O. Kühn, J. Wiley and S. Inc. 2004. Charge and Energy Transfer Dynamics in Molecular Systems. Wiley-VCH, Weinheim.
89. A. Freiberg, M. Ratsep, K. Timpmann and G. Trinkunas. 2009. Excitonic polarons in quasi-one-dimensional LH1 and LH2 bacteriochlorophyll a antenna aggregates from photosynthetic bacteria: A wavelength-dependent selective spectroscopy study. Chem Phys 357, 102-112.
90. R. S. Knox and B. Q. Spring. 2003. Dipole strengths in the chlorophylls. J Photochem Photobiol 77, 497-501.
91. M. G. Cory, M. C. Zerner, X. Hu and K. Schulten. 1998. Electronic excitations in aggregates of bacte-riochlorophylls. J Phys Chem B 102, 7640-7650.
92. J. Eccles, B. Honig and K. Schulten. 1988. Spectroscopic determinants in the reaction center of Rhodopseudomonas viridis. Biophys J 53, 137-144.
93. M. Groot, J. Yu, R. Agarwal, J. R. Norris and G. R. Fleming. 1998. Three-pulse photon echo measur-ments on the accessory pigments in the reaction center of Rhodobacter sphaeroides. J Phys Chem B 102, 5923-5931.
94. T. Ritz, S. Adem and K. Schulten. 2000. A model for photoreceptor-based magnetoreception in birds. Biophys J 78, 707-718.
95. F. Fassioli, A. Olaya-Castro, S. Scheuring, J. Sturgis and N. Johnson. 2009. Energy transfer in light-adapted photosynthetic membranes: From active to saturated photosynthesis. Biophys J 97, 2464-2473.
96. T. Ritz, X. Hu, A. Damjanovic and K. Schulten. 1998. Excitons and excitation transfer in the photosynthetic unit of purple bacteria. J Luminesc 76-77, 310-321.
97. M. K. Sener, S. Park, D. Lu, A. Damjanovic, T. Ritz, P. Fromme and K. Schulten. 2004. Excitation migration in trimeric cyanobacterial photosystem I. J Chem Phys 120, 11183-11195.
98. R. Loudon. 2001. The Quantum Theory of Light, Oxford University Press, Oxford, Third edition.
99. J. D. Jackson. 1999. Classical Electrodynamics. John Willey & Sons, New York, Third edition.