Photosynthesis Research

, Volume 97, Issue 3, pp 215–222

Energy migration as related to the mutual position and orientation of donor and acceptor molecules in LH1 and LH2 antenna complexes of purple bacteria

Regular Paper

Abstract

Many approaches to discovering the interaction energy of molecular transition dipoles use the well-known coefficient ξ(φ, ψ1ψ2) = (cos φ − 3 cos ψ1 cos ψ2)2, where φ, Ψ1, and Ψ2 are inter-dipole angles. Unfortunately, this formula often yields rather approximate results, in particular, when it is applied to closely positioned molecules. This problem is of great importance when dealing with energy migration in photosynthetic organisms, because the major part of excitation transfers in their chlorophyllous antenna proceed between closely positioned molecules. In this paper, the authors introduce corrected values of the orientation factor for several types of mutual orientation of molecules exchanging with electronic excitations for realistic ratios of dipole lengths and spacing. The corrected magnitudes of interaction energies of neighboring bacteriochlorophyll molecules in LH2 and LH1 light-absorbing complexes are calculated for the class of photosynthetic purple bacteria. Some advantageous factors are revealed in their mutual positions and orientations in vivo.

Keywords

Bacterial photosynthesis Energy migration Precision of theory 

Abbreviations

SEE

Singlet electronic excitation

/B/Chl

/Bacterio/chlorophyll

RC

Reaction center

B800, B850, B875

Light-harvesting BChl fractions, having absorption maxima at about 800, 850, and 875 nm, respectively

References

  1. Abdourakhmanov IA, Ganago AO, Erokhin YE, Solov’ev AA, Chugunov VA (1979) Orientation and linear dichroism of the reaction centers from Rhodopseudomonas sphaeroides R-26. Biochim Biophys Acta 546:183–186. doi:10.1016/0005-2728(79)90180-4 PubMedCrossRefGoogle Scholar
  2. Agranovich VM, Galanin MD (1982) Excitation transfer in condensed matter. In: V.3 of Modern problems in condensed matter science. North-Holland, AmsterdamGoogle Scholar
  3. Bahatyreva S, Frese RN, Seibert CA, Olsen JD, van der Werf KO, van Grondelle R, Niederman RA, Bullough PA, Otto C, Hunter CN (2004) The native architecture of a photosynthetic membrane. Nature 430:1058–1062. doi:10.1038/nature02823 CrossRefGoogle Scholar
  4. Beenken WJD, Pullerits T (2004) Excitonic coupling in polythiophenes: comparison of different calculation methods. J Chem Phys 120:2490–2495. doi:10.1063/1.1636460 PubMedCrossRefGoogle Scholar
  5. Ben-Shem A, Frolow F, Nelson N (2003) Crystal structure of plant photosystem I. Nature 426:630–635. doi:10.1038/nature02200 PubMedCrossRefGoogle Scholar
  6. Brunisholz RA, Zuber H (1992) Structure, function and organization of antenna polypeptides and antenna complexes from the three families of Rhodospirillaneae. J Photochem Photobiol 15:113–140. doi:10.1016/1011-1344(92)87010-7 CrossRefGoogle Scholar
  7. Chachisvilis M, Kühn O, Pullerits T, Sundström V (1997) Excitons in photosynthetic purple bacteria: wavelike motion or incoherent hopping? J Phys Chem B 101:7275–7283CrossRefGoogle Scholar
  8. Chang JCP (1977) Monopole effects on electronic excitation interactions between large molecules. I. Application to energy transfer in chlorophylls. J Chem Phys 67:3901–3909CrossRefGoogle Scholar
  9. Clayton RK (1966) Relations between photochemistry and fluorescence in cells and extracts of photosynthetic bacteria. Photochem Photobiol 5:807–821CrossRefGoogle Scholar
  10. Duysens LMN (1951) Transfer of light energy within the pigment systems present in photosynthesizing cells. Nature 168:548–550. doi:10.1038/168548a0 PubMedCrossRefGoogle Scholar
  11. Fenna RE, Matthews BW, Olson JM, Shaw EK (1974) Structure of a bacteriochlorophyll-protein from the green photosynthetic bacterium Chlorobium limicola: Crystallographic evidence for a trimer. J Mol Biol 84:231–234. doi:10.1016/0022-2836(74)90581-6 PubMedCrossRefGoogle Scholar
  12. Förster Th (1948) Intermolecular energy transfer and fluorescence. Ann Phys 2:55–75Google Scholar
  13. Hu X, Damjanović A, Ritz T, Schulten K (1998) Architecture and mechanism of the light-harvesting apparatus of purple bacteria. Proc Natl Acad Sci USA 95:5935–5941. doi:10.1073/pnas.95.11.5935 PubMedCrossRefGoogle Scholar
  14. Jimenez R, van Mourik R, Yu JY, Fleming GR (1997) Three-pulse photon echo measurements on LH1 and LH2 complexes of Rhodobacter sphaeroides: a nonlinear spectroscopic probe of energy transfer. J Phys Chem B 101:7350–7359CrossRefGoogle Scholar
  15. Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauss N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411:909–917. doi:10.1038/35082000 PubMedCrossRefGoogle Scholar
  16. Jordanides XJ, Scholes GD, Fleming GR (2001) The mechanism of energy transfer in the bacterial photosynthetic reaction center. J Phys Chem B 105:1652–1669. doi:10.1021/jp003572e CrossRefGoogle Scholar
  17. Karrasch S, Bullough PA, Ghosh R (1995) The 8.5 A projection map of the light-harvesting complex I from Rhodospirillum rubrum reveals a ring composed of 16 subunits. EMBO J 14:631–638PubMedGoogle Scholar
  18. Kenkre VM, Knox RS (1974) Theory of fast and slow excitation transfer rates. Phys Rev Lett 33:803–806. doi:10.1103/PhysRevLett.33.803 CrossRefGoogle Scholar
  19. Koepke J, Hu X, Muenke C, Schulten K, Michel H (1996) The crystal structure of the light-harvesting complex II (B800–850) from Rhodospirillum molischianum. Structure 4:581–597. doi:10.1016/S0969-2126(96)00063-9 PubMedCrossRefGoogle Scholar
  20. Koolhaus MH, Frese RN, Fowler GJ, Bibby TS, Georgakopoulou S, van der Zwan G, Hunter CN, van Grondelle R (1998) Identification of the upper exciton component of the B850 bacteriochlorophylls of the LH2 antenna complex, using a B800-free mutant of Rhodobacter sphaeroides. Biochemistry 37:4693–4698PubMedCrossRefGoogle Scholar
  21. Krueger BP, Scholes GD, Fleming GR (1998) Calculation of couplings and energy-transfer pathways between the pigments of LH2 by the ab initio transition density cube method. J Phys Chem B 102:5378–5386. doi:10.1021/jp9811171 CrossRefGoogle Scholar
  22. Kühlbrandt W, Wang DN, Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367:614–621. doi:10.1038/367614a0 PubMedCrossRefGoogle Scholar
  23. Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X, Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428:287–292. doi:10.1038/nature02373 PubMedCrossRefGoogle Scholar
  24. Madjet ME, Abdurahman A, Renger T (2006) Intermolecular Coulomb couplings from ab initio electrostatic potentials: application to optical transitions of strongly coupled pigments in photosynthetic antennae and reaction centers. J Phys Chem B 110:17268–17281. doi:10.1021/jp0615398 PubMedCrossRefGoogle Scholar
  25. McDermott G, Prince SM, Freer AA, Hawthornthwaite-Lawless AM, Papiz MS, Cogdell RJ, Isaacs NW (2002) Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374:517–521. doi:10.1038/374517a0 CrossRefGoogle Scholar
  26. Monshouwer R, Baltuska A, van Mourik F, van Grondelle R (1998) Time-resolved absorption difference spectroscopy of the LH-1 antenna of Rhodopseudomonas viridis. J Chem Phys 102A:4360–4371Google Scholar
  27. Papiz MZ, Prince SM, Howard T, Cogdell RJ, Isaacs NW (2003) The structure and thermal motion of the B800–850 LH2 complex from Rps.acidophila at 2.0A resolution and 100K: new structural features and functionally relevant motions. J Mol Biol 326:1523–1538. doi:10.1016/S0022-2836(03)00024-X PubMedCrossRefGoogle Scholar
  28. Pullerits T, Sundström V (1996) Photosynthetic light-harvesting pigment–protein complexes: toward understanding how and why. Acc Chem Res 29:381–389. doi:10.1021/ar950110o CrossRefGoogle Scholar
  29. Rahman TS, Knox RS, Kenkre VT (1979) Theory of depolarization of fluorescence in molecular pairs. Chem Phys 44:197–211. doi:10.1016/0301-0104(79)80119-6 CrossRefGoogle Scholar
  30. Robert B, Cogdell RJ, van Grondelle R (2003) Light-harvesting antennas in photosynthesis. In: Green BR, Parson WW (eds) The light-harvesting system of purple bacteria. Kluwer, The Netherlands, pp 170–194Google Scholar
  31. Roszak AW, Howard TD, Southall J, Gardiner AT, Law CJ, Isaacs NW, Cogdell RJ (2003) Crystal structure of the RC-LH1 core complex from Rhodopseudomonas palustris. Science 302:1969–1972. doi:10.1126/science.1088892 PubMedCrossRefGoogle Scholar
  32. Scholes GD (1996) Energy transfer and spectroscopic characterization of multichromophoric assemblies. J Phys Chem 100:18731–18739. doi:10.1021/jp961784z CrossRefGoogle Scholar
  33. Scholes GD, Jordanides XJ, Fleming GR (2001) Adapting the Förster theory of energy transfer for modeling dynamics in aggregated molecular assemblies. J Phys Chem B 105:1640–1651. doi:10.1021/jp003571m CrossRefGoogle Scholar
  34. Schubert WD, Klukas O, Krauß N, Saenger W, Fromme P, Witt HT (1997) Photosystem I of Synechococcus elongatus at 4 Å resolution: comprehensive structure analysis. J Mol Biol 272:741–769. doi:10.1006/jmbi.1997.1269 PubMedCrossRefGoogle Scholar
  35. van Grondelle R, Dekker JP, Gilbro T, Sundström V (1994) Energy transfer and trapping in photosynthesis. Biochim Biophys Acta 1187:1–65. doi:10.1016/0005-2728(94)90166-X CrossRefGoogle Scholar
  36. Verméglio A, Joliot P (2002) Supramolecular organisation of the photosynthetic chain in anoxygenic bacteria. Biochim Biophys Acta 1555:60–64PubMedCrossRefGoogle Scholar
  37. Yang M, Agarval R, Fleming GR (2001) The mechanism of energy transfer in the antenna of photosynthetic purple bacteria. J Photochem Photobiol A 142:107–119. doi:10.1016/S1010-6030(01)00504-4 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.A.N. Belozersky Institute of Physico-Chemical BiologyM.V. Lomonosov Moscow State UniversityMoscowRussia
  2. 2.Faculty of Bioengineering and BioinformaticsM.V. Lomonosov Moscow State UniversityMoscowRussia

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