Photosynthesis Research

, Volume 71, Issue 1–2, pp 99–123 | Cite as

The quantitative relationship between structure and polarized spectroscopy in the FMO complex of Prosthecochloris aestuarii: refining experiments and simulations

  • Markus Wendling
  • Milosz A. Przyjalgowski
  • Demet Gülen
  • Simone I. E. Vulto
  • Thijs J. Aartsma
  • Rienk van Grondelle
  • Herbert van Amerongen
Article

Abstract

New absorption, linear dichroism (LD) and circular dichroism (CD) measurements at low temperatures on the Fenna—Matthews—Olson complex from Prosthecochloris aestuarii are presented. Furthermore, the anisotropy of fluorescence excitation spectra is measured and used to determine absolute LD spectra, i.e. corrected for the degree of orientation of the sample. In contrast to previous studies, this allows comparison of not only the shape but also the amplitude of the measured spectra with that calculated by means of an exciton model. In the exciton model, the point-dipole approximation is used and the calculations are based on the trimeric structure of the complex. An improved description of the absorption and LD spectra by means of the exciton model is obtained by simply using the same site energies and coupling strengths that were given by Louwe et al. (1997, J Phys Chem B 101: 11280–11287) and including three broadening mechanisms, which proved to be essential: Inhomogeneous broadening in a Monte Carlo approach, homogeneous broadening by using the homogeneous line shape determined by fluorescence line-narrowing measurements [Wendling et al. (2000) J Phys Chem B 104: 5825–5831] and lifetime broadening. An even better description is obtained when the parameters are optimized by a global fit of the absorption, LD and CD spectra. New site energies and coupling strengths are estimated. The amplitude of the LD spectrum is described quite well. The shape of the CD spectrum is modelled in a satisfactory way but its size can only be simulated by using a rather large value for the index of refraction of the medium surrounding the chromophores. It is shown that the estimated coupling strengths are compatible with the value of the dipole strength of bacteriochlorophyll a, when using the empty-cavity model for the local-field correction factor.

circular dichroism electron-phonon coupling excitons homogeneous line shape inhomogeneous broadening lifetime broadening light harvesting linear dichroism modeling photosynthesis pigment–protein complex polarized fluorescence polarized spectroscopy 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alden RG, Johnson E, Nagarajan V, Parson WW, Law CJ and Cogdell RJ (1997) Calculations of spectroscopic properties of the LH 2 bacteriochlorophyll-protein antenna complex from Rhodopseudomonas acidophila. J Phys Chem B 101: 4667–4680CrossRefGoogle Scholar
  2. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN and Bourne PE (2000) The Protein Data Bank. Nucleic Acids Res 28: 235–242CrossRefPubMedGoogle Scholar
  3. Blankenship RE, Olson JM and Miller M (1995) Antenna complexes from green photosynthetic bacteria. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 399–435. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  4. Buck DR, Savikhin S and Struve WS (1997) Effect of diagonal energy disorder on circular dichroism spectra of Fenna-Matthews-Olson trimers. J Phys Chem B 101: 8395–8397CrossRefGoogle Scholar
  5. Fenna RE and Matthews BW (1975) Chlorophyll arrangement in a bacteriochlorophyll-protein from Chlorobium limicola. Nature 258: 573–577CrossRefGoogle Scholar
  6. Fidder H, Knoester J and Wiersma DA (1991) Optical properties of disordered molecular aggregates: a numerical study. J Chem Phys 95: 7880–7890CrossRefGoogle Scholar
  7. Francke C and Amesz J (1997) Isolation and pigment composition of the antenna system of four species of green sulfur bacteria. Photosynth Res 52: 137–146CrossRefGoogle Scholar
  8. Gülen D (1996) Interpretation of the excited-state structure of the Fenna-Matthews-Olson pigment protein complex of Prosthecochloris aestuarii based on the simultaneous simulation of the 4 K absorption, linear dichroism, and singlet-triplet absorption difference spectra: a possible excitonic explanation? J Phys Chem 100: 17683–17689CrossRefGoogle Scholar
  9. Iseri EI and Gülen D (1999) Electronic excited states and excitation transfer kinetics in the Fenna-Matthews-Olson protein of the photosynthetic bacterium Prosthecochloris aestuarii at low temperatures. Eur Biophys J 28: 243–253CrossRefGoogle Scholar
  10. Kleima FJ, Hofmann E, Gobets B, van Stokkum IHM, van Grondelle R, Diederichs K and van Amerongen H (2000a) Förster excitation energy transfer in peridinin-chlorophyll-a-protein. Biophys J 78: 344–353PubMedGoogle Scholar
  11. Kleima FJ, Wendling M, Hofmann E, Peterman EJG, van Grondelle R and van Amerongen H (2000b) Peridinin chlorophyll a protein: relating structure and steady-state spectroscopy. Biochemistry 39: 5184–5195CrossRefPubMedGoogle Scholar
  12. Knapp EW (1984) Lineshapes of molecular aggregates. Exchange narrowing and intersite correlation. Chem Phys 85: 73–82Google Scholar
  13. Koepke J, Hu X, Muenke C, Schulten K and Michel H (1996) The crystal structure of the light-harvesting complex II (B800–850) from Rhodospirillum molischianum. Structure 4: 581–597CrossRefPubMedGoogle Scholar
  14. Koolhaas MHC, van Mourik F, van der Zwan G and van Grondelle R (1994) The B820 sub-unit of the bacterial light-harvesting antenna, a dis-ordered dimer? J Lumin 60&61: 515–519CrossRefGoogle Scholar
  15. Koolhaas MHC, van der Zwan G, Frese RN and van Grondelle R (1997a) Red shift of the zero crossing in the CD spectra of the LH2 antenna complex of Rhodopseudomonas acidophila: a structure-based study. J Phys Chem B 101: 7262–7270CrossRefGoogle Scholar
  16. Koolhaas MHC, van der Zwan G, van Mourik F and van Grondelle R (1997b) Spectroscopy and structure of bacteriochlorophyll dimers. I. Structural consequences of nonconservative circular dichroism spectra. Biophys J 72: 1828–1841PubMedGoogle Scholar
  17. Koolhaas MHC, Frese RN, Fowler GJS, Bibby TS, Georgakopoulou S, van der Zwan G, Hunter CN and 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: 4693–4698CrossRefPubMedGoogle Scholar
  18. Koolhaas MHC, van der Zwan G and van Grondelle R (2000) Local and nonlocal contributions to the linear spectroscopy of lightharvesting antenna systems. J Phys Chem B 104: 4489–4502CrossRefGoogle Scholar
  19. Leegwater JA, Durrant JR and Klug DR (1997) Exciton equilibration induced by phonons: theory and application to PS II reaction centers. J Phys Chem B 101: 7205–7210CrossRefGoogle Scholar
  20. Li Y-F, Zhou W, Blankenship RE and Allen JP (1997) Crystal structure of the bacteriochlorophyll a protein from Chlorobium tepidum. J Mol Biol 271: 456–471CrossRefPubMedGoogle Scholar
  21. Louwe RJW and Aartsma TJ (1997) On the nature of energy transfer at low temperatures in the BChl a pigment-protein complex of green sulfur bacteria. J Phys Chem B 101: 7221–7226CrossRefGoogle Scholar
  22. Louwe RJW, Vrieze J, Aartsma TJ and Hoff AJ (1997a) Toward an integral interpretation of the optical steady-state spectra of the FMO-complex of Prosthecochloris aestuarii. 1. An investigation with linear-dichroic absorbance-detected magnetic resonance. J Phys Chem B 101: 11273–11279CrossRefGoogle Scholar
  23. Louwe RJW, Vrieze J, Hoff AJ and Aartsma TJ (1997b) Toward an integral interpretation of the optical steady-state spectra of the FMO-complex of Prosthecochloris aestuarii. 2. Exciton simulations. J Phys Chem B 101: 11280–11287CrossRefGoogle Scholar
  24. Lu X and Pearlstein RM (1993) Simulations of Prosthecochloris bacteriochlorophyll a-protein optical spectra improved by parametric computer search. Photochem Photobiol 57: 86–91Google Scholar
  25. Matsuzaki S, Zazubovich V, Rätsep M, Hayes JM and Small GJ (2000) Energy transfer kinetics and low energy vibrational structure of the three lowest energy Qy-states of the Fenna-Matthews-Olson antenna complex. J Phys Chem B 104: 9564–9572CrossRefGoogle Scholar
  26. McDermott G, Prince SM, Freer AA, Hawthornthwaite-Lawless AM, Papiz MZ, Cogdell RJ and Isaacs NW (1995) Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374: 517–521Google Scholar
  27. Monshouwer R, Abrahamsson M, van Mourik F and van Grondelle R (1997) Superradiance and exciton delocalisation in bacterial photosynthetic light-harvesting systems. J Phys Chem B 101: 7241–7248CrossRefGoogle Scholar
  28. Olson JM (1980) Chlorophyll organization in green photosynthetic bacteria. Biochim Biophys Acta 594: 33–51PubMedGoogle Scholar
  29. Olson JM (1998) Chlorophyll organization and function in green photosynthetic bacteria. Photochem Photobiol 67: 61–75CrossRefGoogle Scholar
  30. Olson JM, Ke B and Thompson KH (1976) Exciton interaction among chlorophyll molecules in bacteriochlorophyll a proteins and bacteriochlorophyll a reaction center complexes from green bacteria. Biochim Biophys Acta 430: 524–537PubMedGoogle Scholar
  31. Owen GM and Hoff AJ (2001) Absorbance detected magnetic resonance spectra of the FMO complex of Prosthecochloris aestuarii reconsidered: Exciton simulations. J Phys Chem B105: 1458–1463Google Scholar
  32. Pearlstein RM (1991) Theoretical interpretation of antenna spectra. In: Scheer H (ed) Chlorophylls, pp 1047–1078. CRC Press, Boca Raton, FloridaGoogle Scholar
  33. Pearlstein RM (1992) Theory of the optical spectra of the bacteriochlorophyll a antenna protein trimer from Prosthecochloris aestuarii. Photosynth Res 31: 213–226CrossRefGoogle Scholar
  34. Pearlstein RM and Hemenger RP (1978) Bacteriochlorophyll electronic transition moment directions in bacteriochlorophyll a-protein. Proc Natl Acad Sci USA 75: 4920–4924Google Scholar
  35. Philipson KD and Sauer K (1972) Exciton interaction in a bacteriochlorophyll-protein from Chloropseudomonas ethylica. Absorption and circular dichroism at 77 °K. Biochemistry 11: 1880–1885CrossRefPubMedGoogle Scholar
  36. Press WH, Teukolsky SA, Vetterling WT and Flannery BP (1992) Numerical Recipes in C: The Art of Scientific Computing. Cambridge University Press, CambridgeGoogle Scholar
  37. Pullerits T, Monshouwer R, van Mourik F and van Grondelle R (1995) Temperature dependence of electron-vibronic spectra of photosynthetic systems. Computer simulations and comparison with experiment. Chem Phys 194: 395–407CrossRefGoogle Scholar
  38. Rätsep M, Blankenship RE and Small GJ (1999) Energy transfer and spectral dynamics of the three lowest energy Qy-states of the Fenna-Matthews-Olson antenna complex. J Phys Chem B 103: 5736–5741CrossRefGoogle Scholar
  39. Renger T and May V (1998) Ultrafast exciton motion in photosynthetic antenna systems: the FMO-complex. J Phys Chem A 102: 4381–4391CrossRefGoogle Scholar
  40. Savikhin S, Buck DR and Struve WS (1998) Toward level-to-level energy transfers in photosynthesis: the Fenna-Matthews-Olson protein. J Phys Chem B 102: 5556–5565CrossRefGoogle Scholar
  41. Savikhin S, Buck DR and Struve WS (1999) The Fenna-Matthews-Olson protein: a strongly coupled photosynthetic antenna. In: Andrews DL and Demidov AA (eds) Resonance Energy Transfer, pp 399–434. John Wiley & Sons, Chichester, UKGoogle Scholar
  42. Somsen OJG, van Grondelle R and van Amerongen H (1996) Spectral broadening of interacting pigments: polarized absorption by photosynthetic proteins. Biophys J 71: 1934–1951PubMedGoogle Scholar
  43. Sundström V, Pullerits T and van Grondelle R (1999) Photosynthetic light-harvesting: reconciling dynamics and structure of purple bacterial LH2 reveals function of photosynthetic unit. J Phys Chem B 103: 2327–2346CrossRefGoogle Scholar
  44. Tronrud DE and Matthews BW (1993) Refinement of the structure of a water-soluble antenna complex from green photosynthetic bacteria by incorporation of the chemically determined amino acid sequence. In: Deisenhofer J and Norris JR (eds) The Photosynthetic Reaction Center, Vol. 1, pp 13–21. Academic Press, San Diego, CaliforniaGoogle Scholar
  45. Tronrud DE, Schmid MF and Matthews BW (1986) Structure and X-ray amino acid sequence of a bacteriochlorophyll a protein from Prosthecochloris aestuarii refined at 1.9 Å resolution. J Mol Biol 188: 443–454CrossRefPubMedGoogle Scholar
  46. van Amerongen H and Struve WS (1995) Polarized optical spectroscopy of chromoproteins. Meth Enzymol 246: 259–283PubMedGoogle Scholar
  47. van Amerongen H, van Haeringen B, van Gurp M and van Grondelle R (1991) Polarized fluorescence measurements on ordered photosynthetic antenna complexes: chlorosomes of Chloroflexus aurantiacus and B800–850 antenna complexes of Rhodobacter sphaeroides. Biophys J 59: 992–1001Google Scholar
  48. van Amerongen H, Kwa SLS, van Bolhuis BM and van Grondelle R (1994) Polarized fluorescence and absorption of macroscopically aligned light-harvesting complex II. Biophys J 67: 837–847PubMedGoogle Scholar
  49. van Amerongen H, Valkunas L and van Grondelle R (2000) Photosynthetic Excitons. World Scientific, SingaporeGoogle Scholar
  50. van Grondelle R, Dekker JP, Gillbro T and Sundström V (1994) Energy transfer and trapping in photosynthesis. Biochim Biophys Acta 1187: 1–65Google Scholar
  51. van Mourik F, Visschers RW and van Grondelle R (1992) Energy transfer and aggregate size effects in the inhomogeneously broadened core light-harvesting complex of Rhodobacter sphaeroides. Chem Phys Lett 193: 1–7CrossRefGoogle Scholar
  52. van Mourik F, Verwijst RR, Mulder JM and van Grondelle R (1994) Singlet-triplet spectroscopy of the light-harvesting BChl a complex of Prosthecochloris aestuarii. The nature of the low-energy 825 nm transition. J Phys Chem 98: 10307–10312CrossRefGoogle Scholar
  53. Vasmel H, Swarthoff T, Kramer HJM and Amesz J (1983) Isolation and properties of a pigment-protein complex associated with the reaction center of the green photosynthetic sulfur bacterium Prosthecochloris aestuarii. Biochim Biophys Acta 725: 361–367Google Scholar
  54. Vulto SIE, Streltsov AM and Aartsma TJ (1997) Excited state energy relaxation in the FMO complexes of the green bacterium Prosthecochloris aestuarii at low temperatures. J Phys Chem B 101: 4845–4850CrossRefGoogle Scholar
  55. Vulto SIE, De Baat MA, Louwe RJW, Permentier HP, Neef T, Miller M, van Amerongen H and Aartsma TJ (1998) Exciton simulations of optical spectra of the FMO complex from the green sulfur bacterium Chlorobium tepidum at 6 K. J Phys Chem B 102: 9577–9582CrossRefGoogle Scholar
  56. Vulto SIE, De Baat MA, Neerken S, Nowak FR, van Amerongen H, Amesz J and Aartsma TJ (1999) Excited state dynamics in FMO antenna complexes from photosynthetic green sulfur bacteria: A kinetic model. J Phys Chem B 103: 8153–8161CrossRefGoogle Scholar
  57. Wendling M, Pullerits T, Przyjalgowski MA, Vulto SIE, Aartsma TJ, van Grondelle R and van Amerongen H (2000) Electron-vibrational coupling in the Fenna-Matthews-Olson complex of Prosthecochloris aestuarii determined by temperature-dependent absorption and fluorescence line-narrowing measurements. J Phys Chem B 104: 5825–5831CrossRefGoogle Scholar
  58. Whitten WB, Olson JM and Pearlstein RM (1980) Seven-fold exciton splitting of the 810-nm band in bacteriochlorophyll a-proteins from green photosynthetic bacteria. Biochim Biophys Acta 591: 203–207PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Markus Wendling
    • 1
  • Milosz A. Przyjalgowski
    • 1
  • Demet Gülen
    • 2
  • Simone I. E. Vulto
    • 3
  • Thijs J. Aartsma
    • 3
  • Rienk van Grondelle
    • 1
  • Herbert van Amerongen
    • 1
  1. 1.Division of Physics and Astronomy, Department of Biophysics and Physics of Complex SystemsVrije Universiteit, Faculty of SciencesAmsterdamThe Netherlands
  2. 2.Department of PhysicsMiddle East Technical UniversityAnkaraTurkey
  3. 3.Department of Biophysics, Huygens LaboratoryRijksuniversiteit LeidenLeidenThe Netherlands

Personalised recommendations