Photosynthesis Research

, Volume 125, Issue 1–2, pp 31–42 | Cite as

Orientation of B798 BChl a Q y transition dipoles in Chloroflexus aurantiacus chlorosomes: polarized transient absorption spectroscopy studies

  • Andrei Yakovlev
  • Vladimir Novoderezhkin
  • Alexandra Taisova
  • Vladimir Shuvalov
  • Zoya Fetisova
Regular Paper


Isotropic and anisotropic pump-probe spectra of Cfx. aurantiacus chlorosomes were measured on the fs-through ps-time scales for the B798 BChl a Q y band upon direct excitation of the B798 band at T = 293 K and T = 90 K. Upon direct excitation of the B798 band, the anisotropy parameter value r(λ) was constant within the whole BChl a Q y band at any delay time at both temperatures. The value of the anisotropy parameter r decayed from r = 0.4 at both temperatures (at 200 fs delay time after excitation) to the steady-state values r = 0.1 at T = 293 K and to r = 0.09 at T = 90 K (at 30 ÷ 100 ps delay time after excitation). The results were considered within the framework of the model of uniaxial orientation distribution of BChl-a transition dipoles within a single Cfx. aurantiacus chlorosome. This implies that the B798 BChl a Q y transition dipoles, randomly distributed around the normal to the baseplate plane, form the angle θ with the plane. For this model, the theoretical dependence of the steady-state anisotropy parameter r on the angle θ was derived. According to the theoretical dependence r(θ), the angle θ corresponding to the experimental steady-state value r = 0.1 at T = 293 K was found to equal 55°. As the temperature drops to 90 K, the angle θ decreases to 54°.


Bacterial photosynthesis Green bacteria Chlorosome Bacteriochlorophyll a antenna Polarized pump-probe spectroscopy Room and low-temperature spectroscopy 



The work was supported by the Russian Foundation for Basic Research (Grant 08-04-01587a, 10-04-01758-a).


  1. Arellano JB, Melo TB, Borrego CM, Garcia-Gil J, Naqvi KR (2000) Nanosecond laser photolysis studies of chlorosomes and artificial aggregates containing bacteriochlorophyll e: Evidence for the proximity of carotenoids and bacteriochlorophyll a in chlorosomes from Chlorobium phaeobacteroides strain CL1401. Photochem Photobiol 72:669–675PubMedCrossRefGoogle Scholar
  2. Carbonera D, Bordignon E, Giacometti G, Agostini G, Vianelli A, Vannini C (2001) Fluorescence and absorption detected magnetic resonance of chlorosomes from green bacteria Chlorobium tepidum and Chloroflexus aurantiacus. A comparative study. J Phys Chem B 105:246–255CrossRefGoogle Scholar
  3. Didraga C, Knoester J (2003) Absorption and dichroism spectra of cylindrical J aggregates and chlorosomes of green bacteria. J Lumin 102:60–66CrossRefGoogle Scholar
  4. Dracheva T, Taisova A, Fetisova Z (1998) Circular dichroism spectroscopy as a test for the chlorosome antenna structure. In: Garab G (ed) Photosynthesis: Mechanisms and Effects, vol 1. Kluwer Academic Publishers, Dordrecht, pp 129–132CrossRefGoogle Scholar
  5. Egawa A, Fujiwara T, Mizoguchi T, Kakitani Y, Koyama Y, Akutsu H (2007) Structure of the light-harvesting bacteriochlorophyll c assembly in chlorosomes from Chlorobium limicola determined by solid-state NMR. Proc Natl Acad Sci USA 104(3):790–795PubMedCentralPubMedCrossRefGoogle Scholar
  6. Feick RG, Fitzpatrick M, Fuller RC (1982) Isolation and characterization of cytoplasmic membranes and chlorosomes from the green bacterium Chloroflexus aurantiacus. J Bacteriol 150(2):905–915PubMedCentralPubMedGoogle Scholar
  7. Fetisova ZG (2004) Survival strategy of photosynthetic organisms. 1. variability of the extent of light-harvesting pigment aggregation as a structural factor optimizing the function of oligomeric photosynthetic antenna (Mosk). Model Calculations Mol Biol 38:434–440CrossRefGoogle Scholar
  8. Fetisova ZG, Fok MV (1984) Optimization routes for the transformation of light energy in primary acts of photosynthesis. I. The necessity of structure optimization for photosynthetic unit and method for the calculation of its efficiency (Mosk). Mol Biol 18:1354–1359Google Scholar
  9. Fetisova ZG, Kharchenko SG, Abdourakhmanov IA (1986) Strong orientational ordering of the near-infrared transition moment vectors of light-harvesting antenna bacterioviridin in chromatophores of the green photosynthetic bacterium Chlorobium limicola. FEBS Lett 199:234–236CrossRefGoogle Scholar
  10. Fetisova ZG, Freiberg AM, Timpmann KE (1988) Long-range molecular order as an efficient strategy for light harvesting in photosynthesis (London). Nature 334:633–634CrossRefGoogle Scholar
  11. Fetisova Z, Freiberg A, Mauring K, Novoderezhkin V, Taisova A, Timpmann K (1996) Excitation energy transfer in chlorosomes of green bacteria: theoretical and experimental studies. Biophys J 71:995PubMedCentralPubMedCrossRefGoogle Scholar
  12. Frigaard N-U, Bryan D, Fetisova Z (2006) Chlorosomes: antenna organelles in green photosynthetic bacteria. In: Shively JM (ed) Complex intracellular structures in prokaryotes. Microbiology monographs, vol 2. Springer, Berlin, pp 79–114CrossRefGoogle Scholar
  13. Garab G, Van Amerongen H (2009) Linear dichroism and circular dichroism in photosynthesis research. Photosynth Res 101:135–146PubMedCentralPubMedCrossRefGoogle Scholar
  14. Gerola PD, Olson JM (1986) A new bacteriochlorophyll a-protein complex associated with chlorosomes of green sulfur bacteria. Biochim Biophys Acta 848:69–76PubMedCrossRefGoogle Scholar
  15. Golecki JR, Oelze J (1987) Quantitative relationship between bacteriochlorophyll content, cytoplasmic membrane structure and chlorosome size in Chloroflexus aurantiacus. Arch Microbiol 148:236–241Google Scholar
  16. Jendrny M, Aartsma TJ, Kohler J (2014) Insights into the Excitonic States of Individual Chlorosomes from Chlorobaculum tepidum. Biophys J 106:1921–1927PubMedCentralPubMedCrossRefGoogle Scholar
  17. Lin S, Van Amerongen H, Struve WS (1991) Ultrafast pump-probe spectroscopy of bacteriochlorophyll c antennae in bacteriochlorophyll a-containing chlorosomes from the green photosynthetic bacterium Chloroflexus aurantiacus. Biochim Biophys Acta 1060:13–22CrossRefGoogle Scholar
  18. Linnanto JM, Korppi-Tommola JEI (2008) Investigation on chlorosomal antenna geometries: tube, lamella and spiral-type self-aggregates. Photosynth Res 96:227–245PubMedCrossRefGoogle Scholar
  19. Linnanto JM, Korppi-Tommola JEI (2013) Exciton description of chlorosome to baseplate excitation energy transfer in filamentous anoxygenic phototrophs and green sulfur bacteria. J Phys Chem B 117:11144–11161PubMedCrossRefGoogle Scholar
  20. Ma Y-Z, Cox RP, Gillbro T, Miller M (1996) Bacteriochlorophyll organization and energy transfer kinetics in chlorosomes from Chloroflexus aurantiacus depend on the light regime during growth. Photosynth Res 47:157–165PubMedCrossRefGoogle Scholar
  21. Martiskainen J, Linnanto J, Kananavičius R, Lehtovuori V, Korppi-Tommola J (2009) Excitation energy transfer in isolated chlorosomes from Chloroflexus aurantiacus. Chem Phys Lett 477:216–220CrossRefGoogle Scholar
  22. Martiskainen J, Kananavičius R, Linnanto J, Lehtivuori H, Keränen M, Aumanen V, Tkachenko N, Korppi-Tommola J (2011) Excitation energy transfer in the LHC-II trimer: from carotenoids to chlorophylls in space and time. Photosynth Res 107:195–207PubMedCrossRefGoogle Scholar
  23. Mimuro M, Hirota M, Nishimura Y, Moriyama T, Yamazaki I, Shimada K, Matsuura K (1994) Molecular organization of bacteriochlorophyll in chlorosomes of the green photosynthetic bacterium Chloroflexus aurantiacus: studies of fluorescence depolarization accompanied by energy transfer process. Photosynth Res 41:181–191PubMedCrossRefGoogle Scholar
  24. Montaňo GA, Wu HM, Lin S, Brune DC, Blankenship RE (2003) Isolation and characterization of the B798 light-harvesting baseplate from the chlorosomes of Chloroflexus aurantiacus. Biochemistry 42:10246–10251PubMedCrossRefGoogle Scholar
  25. Murata N, Fork DC (1975) Temperature dependence of chlorophyll a fluorescence in relation to the physical phase of membrane lipids in algae and higher plants. Plant Physiol 56:791–796PubMedCentralPubMedCrossRefGoogle Scholar
  26. Niedermeier G, Shiozawa JA, Lottespeich F, Feick RG (1994) The primary structure of two chlorosome proteins from Chloroflexus aurantiacus. FEBS Lett 342:61–65PubMedCrossRefGoogle Scholar
  27. Novoderezhkin VI, Taisova AS, Fetisova ZG (1998a) Pigment organization and exciton dynamics in the B808-866 antenna of the green bacterium Chloroflexus aurantiacus. Biochem Mol Biol Intern 45:355–362Google Scholar
  28. Novoderezhkin VI, Taisova AS, Fetisova ZG, Blankenship RE, Savikhin S, Buck DR, Struve WS (1998b) Energy transfers in the B808-866 antenna from the green bacterium Chloroflexus aurantiacus. Biophys J 74:2069–2075PubMedCentralPubMedCrossRefGoogle Scholar
  29. Novoderezhkin VI, Taisova AS, Fetisova ZG (2001) Unit building block of the oligomeric chlorosomal antenna of the green photosynthetic bacterium Chloroflexus aurantiacus: modeling of nonlinear optical spectra. Chem Phys Lett 335:234–240CrossRefGoogle Scholar
  30. Novoderezhkin V, van Grondelle R (2002) Exciton-vibrational relaxation and transient absorption dynamics in LH1 of Rhodopseudomonas viridis: a redfield theory approach. J Phys Chem B 106:6025–6037Google Scholar
  31. Oelze J (1992) Light and oxygen regulation of the synthesis of bacteriochlorophyll a and bacteriochlorophyll c in Chloroflexus aurantiacus. J Bacteriol 174:5021–5026PubMedCentralPubMedGoogle Scholar
  32. Oelze J, Fuller RC (1983) Temperature dependence of growth and membrane-bound activities of Chloroflexus aurantiacus energy metabolism. J Bacteriol 155:90–96PubMedCentralPubMedGoogle Scholar
  33. Oelze J, Fuller RC (1987) Growth rate and control of development of the photosynthetic apparatus in Chloroflexus aurantiacus. Arch Microbiol 148:132–136CrossRefGoogle Scholar
  34. Oelze J, Golecki JR (1995) Membranes and chlorosomes of green bacteria: structure, composition and development. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic Photosynthetic Bacteria. Kluwer Academic Publishers, The Netherlands, pp 259–278Google Scholar
  35. Olson JM (1980) Chlorophyll organization in green photosynthetic bacteria. Biochim Biophys Acta 594:33–51PubMedCrossRefGoogle Scholar
  36. Olson JM (1998) Chlorophyll organization and function in green photosynthetic bacteria. Photochem Photobiol 67:61–75CrossRefGoogle Scholar
  37. Oostergetel GT, van Amerongen H, Boekema EJ (2010) The chlorosome: a prototype for efficient light harvesting in photosynthesis. Photosynth Res 104(2–3):245–255PubMedCentralPubMedCrossRefGoogle Scholar
  38. Overath P, Thilo L, Triuble H (1976) Lipid phase transitions and membrane function. Trends Biochem Sci 1:186–189CrossRefGoogle Scholar
  39. Pedersen MØ, Linnanto J, Frigaard NU, Nielsen NC, Miller M (2010) A model of the protein-pigment baseplate complex in chlorosomes of photosynthetic green bacteria. Photosynth Res 104:233–243PubMedCrossRefGoogle Scholar
  40. Pierson BK, Castenholz RW (1992) The family Chloroflexaceae. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH (eds) The Prokaryotes, vol 4, 2nd edn., Springer-Verlag, NY, Heidelberg, pp 3754–3774Google Scholar
  41. Pierson BK, Castenholz RW (1995) Taxonomy and physiology of filamentous anoxygenic phototrophs. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic Photosynthetic Bacteria. Kluwer Academic Publishers, Dordrecht, pp 31–47Google Scholar
  42. Pšenčik J, Ikonen TP, Laurinmäki P, Merckel MC, Butcher SJ, Serimaa RE, Tuma R (2004) Lamellar organization of pigments in chlorosomes, the light harvesting system of green bacteria. Biophys J 87:1165–1172Google Scholar
  43. Pšenčik J, Arellano JB, Ikonen TP, Borrego CM, Laurinmäki P, Butcher SJ, Serimaa RE, Tuma R (2006) Internal structure of chlorosomes from brown-colored Chlorobium species and the role of carotenoids in their assembly. Biophys J 91:1433–1440Google Scholar
  44. Pšenčik J, Collins AM, Liljeroos L, Torkkeli M, Laurinmäki P, Ansink HM, Ikonen TP, Serimaa RE, Blankenship RE, Tuma R, Butcher SJ (2009) Structure of chlorosomes from the green filamentous bacterium Chloroflexus aurantiacus. J Bacteriol 191:6701–6708PubMedCentralPubMedCrossRefGoogle Scholar
  45. Pšenčik J, Torkkeli M, Zupčanová A, Vácha F, Serimaa RE, Tuma R (2010) The lamellar spacing in self-assembling bacteriochlorophyll aggregates is proportional to the length of the esterifying alcohol. Photosynth Res 104:211–219PubMedCrossRefGoogle Scholar
  46. Saga Y, Tamiaki H (2006) Transmission electron microscopic study on supramolecular nanostructures of bacteriochlorophyll self-aggregates in chlorosomes of green photosynthetic bacteria. J Biosc Bioeng 102:18–23CrossRefGoogle Scholar
  47. Saga Y, Wazawa T, Mizoguchi T, Ishii Y, Yanagida T, Tamiaki H (2002) Spectral heterogeneity in single light-harvesting chlorosomes from green sulfur photosynthetic bacterium Chlorobium tepidum. Photochem Photobiol 75:433–436PubMedCrossRefGoogle Scholar
  48. Sakuragi Y, Frigaard N-U, Shimada K, Matsuura K (1999) Association of bacteriochlorophyll a with the CsmA protein in chlorosomes of the photosynthetic green filamentous bacterium Chloroflexus aurantiacus. Biochim Biophys Acta 1413:172–180PubMedCrossRefGoogle Scholar
  49. Savikhin S, Buck DR, Struve WS, Blankenship RE, Taisova AS, Novoderezhkin VI, Fetisova ZG (1998) Exciton delocalization in the bacteriochlorophyll c antenna of the green bacterium Chloroflexus aurantiacus as revealed by ultrafast pump-probe spectroscopy. FEBS Lett 430:323–326PubMedCrossRefGoogle Scholar
  50. Schmidt K, Maarzahl M, Mayer F (1980) Development and pigmentation of chlorosomes in Chloroflexus aurantiacus Ok-70-fl. Arch Microbiol 127:87–97CrossRefGoogle Scholar
  51. Shibata Y, Saga Y, Tamiaki H, Itoh S (2006) Low temperature fluorescence from single chlorosomes, photosynthetic antenna complexes of green filamentous and sulfur bacteria. Biophys J 91:3787–3796PubMedCentralPubMedCrossRefGoogle Scholar
  52. Shibata Y, Saga Y, Tamiaki H, Itoh S (2007) Polarized fluorescence of aggregated bacteriochlorophyll c and baseplate bacteriochlorophyll a in single chlorosomes isolated from Chloroflexus aurantiacus. Biochemistry 46:7062–7068PubMedCrossRefGoogle Scholar
  53. Shibata Y, Saga Y, Tamiaki H, Itoh S (2009) Anisotropic distribution of emitting transition dipoles in chlorosome from Chlorobium tepidum: fluorescence polarization anisotropy study of single chlorosomes. Photosynth Res 100:67–78PubMedCrossRefGoogle Scholar
  54. Shibata Y, Tateishi S, Nakabayashi S, Itoh S, Tamiaki H (2010) Intensity borrowing via excitonic couplings among Soret and Qy-transitions of bacteriochlorophylls in the pigment aggregates of chlorosomes, the light-harvesting antennae of green sulfur bacteria. Biochemistry 49:7504–7515PubMedCrossRefGoogle Scholar
  55. Somsen OJ, van Grondelle R, van Amerongen H (1996) Spectral broadening of interacting pigments: polarized absorption by photosynthetic proteins. Biophys J 71(4):1934–1951PubMedCentralPubMedCrossRefGoogle Scholar
  56. Sprague SD, Varga AR (1986) Membrane architecture of anoxygenic photosynthetic bacteria. In: Staehelin LA, Arntzen CJ (eds) Encyclopedia of Plant Physiology, vol 19. Springer - Verlag, Berlin-Heidelberg, pp 603–619Google Scholar
  57. Sprague SG, Staehelin LA, DiBartolomeis MJ, Fuller RC (1981) Isolation and development of chlorosomes in the green bacterium Chloroflexus aurantiacus. J Bacteriol 147:1021–1031PubMedCentralPubMedGoogle Scholar
  58. Staehelin LA, Golecki JR, Drews G (1978) Visualization of the supramolecular architecture of chlorosomes (Chlorobium type vesicles) in freeze-fractured cells of Chloroflexus aurantiacus. Arch Microbiol 119:269–277CrossRefGoogle Scholar
  59. Staehelin LA, Golecki JR, Drews G (1980) Supramolecular organization of chlorosomes (Chlorobium Vesicles) and of their membrane attachment sites in Chlorobium limicola. Biochim Biophys Acta 589:30–45PubMedCrossRefGoogle Scholar
  60. Taisova AS, Keppen OI, Lukashev EP, Arutyunyan AM, Fetisova ZG (2002) Study of the chlorosomal antenna of the green mesophilic filamentous bacterium Oscillochloris trichoides. Photosynth Res 74:73–85PubMedCrossRefGoogle Scholar
  61. Taisova AS, Lukashev EP, Fedorova NV, Zobova AV, Dolgova TA, Fetisova ZG (2012) Experimental proof of optimality of interfacing of chlorosome BChl c and membrane BChl a subantennae in superantenna of photosynthetic green bacteria from the Oscillochloridaceae family. Dokl Biochem Biophys 444:154–157PubMedCrossRefGoogle Scholar
  62. Taisova AS, Yakovlev AG, Fetisova ZG (2014) Size variability of the unit building block of peripheral light-harvesting antennas as a strategy for effective functioning of antennas of variable size that is controlled in vivo by light intensity. Biochemistry (Mosc) 79:251–259CrossRefGoogle Scholar
  63. Van Amerongen H, Vasmel H, van Grondelle R (1988) Linear dichroism of chlorosomes from Chloroflexus aurantiacus in compressed gels and electric fields. Biophys J 54:65–76PubMedCentralPubMedCrossRefGoogle Scholar
  64. Van Amerongen H, van Haeringen B, van Gurp M, van Grondellle R (1991) Polarized fluorescence measurements on ordered photosynthetic antenna complexes. Biophys J 59:992–1001PubMedCentralPubMedCrossRefGoogle Scholar
  65. Van Dorssen RJ, Amesz J (1988) Pigment organization and energy transfer in the green photosynthetic bacterium Chloroflexus aurantiacus. III. Energy transfer in whole cells. Photosynth Res 15:177–189PubMedCrossRefGoogle Scholar
  66. Van Dorssen RJ, Vasmel H, Amesz J (1986) Pigment organization and energy transfer in the green photosynthetic bacterium Chloroflexus aurantiacus. II. The chlorosome. Photosynth Res 9:33–45CrossRefGoogle Scholar
  67. Vasmel H, van Dorssen RJ, De Vos GJ, Amesz J (1986) Pigment organization and energy transfer in the green photosynthetic bacterium Chloroflexus aurantiacus: I. The cytoplasmic membrane. Photosynth Res 7:281–294CrossRefGoogle Scholar
  68. Pierson BK, Castenholz RW (I974) Pigments and growth in Chloroflexus aurantiacus, a phototrophic filamentous bacterium. Arch Microbiol 100: 283–305Google Scholar
  69. Yakovlev AG, Shkuropatov AY, Shuvalov VA (2000) Nuclear wavepacket motion producing a reversible charge separation in bacterial reaction centers. FEBS Lett 466:209–212PubMedCrossRefGoogle Scholar
  70. Yakovlev AG, Novoderezhkin VI, Taisova AS, Fetisova ZG (2002a) Exciton dynamics in the chlorosomal antenna of the green bacterium Chloroflexus aurantiacus: experimental and theoretical studies of femtosecond pump-probe spectra. Photosynth Res 71:19–32PubMedCrossRefGoogle Scholar
  71. Yakovlev AG, Taisova AS, Fetisova ZG (2002b) Light control over the size of an antenna unit building block as an effecient strategy for light harvesting in photosynthesis. FEBS Lett 512:129–132PubMedCrossRefGoogle Scholar
  72. Yakovlev A, Novoderezhkin V, Taisova A Zobova A, Fetisova Z (2013) Optimal mutual orientational ordering of QY transition dipoles of adjacent subantennae pigments in the superantenna of the photosynthetic green bacterium Chloroflexus aurantiacus. Theoretical and experimental studies. In: Kuang T, Lu C, Zhang L (eds) Photosynthesis Research for Food, Fuel and Future, Advanced Topics in Science and Technology in China-15th International Conference on Photosynthesis, Symposium 03: Light Harvesting Anaerobic Systems. Zhejiang University Press, Heidelberg, pp 113–116Google Scholar
  73. Zobova AV, Yakovlev AG, Taisova AS, Fetisova ZG (2009) The search for an optimal orientational ordering of Qy transition dipoles of subantennae molecules in the superantenna of photosynthetic green bacteria: model calculations. Molecular Biology (Mosk) 43:426–443CrossRefGoogle Scholar
  74. Zobova A, Taisova A, Lukashev E, Fedorova N, Baratova L, Fetisova Z (2011) CsmA protein is associated with BChl a in the baseplate subantenna of chlorosomes of the photosynthetic green filamentous bacterium Oscillochloris trichoides belonging to the family Oscillochloridaceae. J of Biophysics. doi: 10.1155/2011/860382 Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Andrei Yakovlev
    • 2
  • Vladimir Novoderezhkin
    • 2
  • Alexandra Taisova
    • 2
  • Vladimir Shuvalov
    • 1
    • 2
  • Zoya Fetisova
    • 2
  1. 1.Institute of Basic Biological ProblemsRussian Academy of SciencesMoscowRussian Federation
  2. 2.Belozersky Institute of Physico-Chemical BiologyLomonosov Moscow State UniversityMoscowRussian Federation

Personalised recommendations