Q-band hyperchromism and B-band hypochromism of bacteriochlorophyll c as a tool for investigation of the oligomeric structure of chlorosomes of the green photosynthetic bacterium Chloroflexus aurantiacus

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Chlorosomes of green photosynthetic bacteria are the most amazing example of long-range ordered natural light-harvesting antennae. Chlorosomes are the largest among all known photosynthetic light-harvesting structures (~ 104–105 pigments in the aggregated state). The chlorosomal bacteriochlorophyll (BChl) c/d/e molecules are organized via self-assembly and do not require proteins to provide a scaffold for efficient light harvesting. Despite numerous investigations, a consensus regarding the spatial structure of chlorosomal antennae has not yet been reached. In the present work, we studied hyperchromism/hypochromism in the chlorosomal BChl c Q/B absorption bands of the green photosynthetic bacterium Chloroflexus (Cfx.) aurantiacus. The chlorosomes were isolated from cells grown under different light intensities and therefore, as we discovered earlier, they had different sizes of both BChl c antennae and their unit building blocks. We have shown experimentally that the Q-/B-band hyperchromism/hypochromism is proportional to the size of the chlorosomal antenna. We explained theoretically these findings in terms of excitonic intensity borrowing between the Q and B bands for the J-/H-aggregates of the BChls. The theory developed by Gülen (Photosynth Res 87:205–214, 2006) showed the dependence of the Q-/B-band hyperchromism/hypochromism on the structure of the aggregates. For the model of exciton-coupled BChl c linear chains within a unit building block, the theory predicted an increase in the hyperchromism/hypochromism with the increase in the number of molecules per chain and a decrease in it with the increase in the number of chains. It was previously shown that this model ensured a good fit with spectroscopy experiments and approximated the BChl c low packing density in vivo. The presented experimental and theoretical studies of the Q-/B-band hyperchromism/hypochromism permitted us to conclude that the unit building block of Cfx. aurantiacus chlorosomes comprises of several short BChl c chains.

This conclusion is in accordance with previous linear and nonlinear spectroscopy studies on Cfx. aurantiacus chlorosomes.

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Cfx :



Chlorosome-membrane complexes

Cba :



Optical density


  1. Arellano J, Melo T, Borrego C, Garcia-Gil J, Naqvi K (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 72:669–675

  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 105:246–255

  3. Castenholz RW (1969) Thermophilic blue-green algae and the thermal environment. Bacteriol Rev 33:476–504

  4. Clayton RK (1980) Photosynthesis: physical mechanisms and chemical patterns. Cambridge University Press, Cambridge

  5. DeVoe H, Tinoco I Jr (1962) The hypochromism of helical polynucleotides. J Mol Biol 4:518–527

  6. Didraga C, Knoester J (2003) Absorption and dichroism spectra of cylindrical J aggregates and chlorosomes of green bacteria. J Lumin 102:60–66

  7. 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 129–132

  8. 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):790–795

  9. Fetisova Z (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 model calculations. Mol Biol (Mosk) 38:434–440

  10. Fetisova Z, Fok M (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. Mol Biol (Mosk) 18:1354–1359

  11. Fetisova Z, Kharchenko S, Abdourakhmanov I (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 199:234–236

  12. Fetisova Z, Freiberg A, Timpmann K (1988) Long-range molecular order as an efficient strategy for light harvesting in photosynthesis. Nature (London) 334:633–634

  13. Fetisova Z, Shibaeva L, Fok M (1989) Biological expedience of oligomerization of chlorophyllous pigments in natural photosynthetic systems. J Theor Biol 140:167–184

  14. Fetisova Z, Mauring K (1992) Experimental evidence of oligomeric organization of antenna bacteriochlorophyll c in green bacterium Chloroflexus aurantiacus by spectral hole burning. FEBS Lett 307:371–374

  15. Fetisova Z, Mauring K (1993) Spectral hole burning study of intact cells of green bacterium Chlorobium limicola. FEBS Lett 323:159–162

  16. Fetisova Z, Mauring K, Taisova A (1994) Strongly exciton coupled BChl e chromophore system in chlorosomal antenna of intact cells of green bacterium Chlorobium phaeovibrioides: A spectral hole burning study. Photosynth Res 41:205–210

  17. 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 71:101–995

  18. Frigaard N-U, Bryant DA (2004) Seeing green bacteria in a new light: genomics-enabled studies of the photosynthetic apparatus in green sulfur bacteria and filamentous anoxygenic phototrophic bacteria. Arch Microbiol 182:265–276

  19. Frigaard N-U, Bryant D (2006) Chlorosomes: antenna organelles in green photosynthetic bacteria. In: Shively JM (ed) Complex intracellular structures in prokaryotes Microbiology monographs, vol 2. Springer, Berlin, pp 79–114

  20. Furumaki S, Vacha F, Habuchi S, Tsukatani Y, Bryant D, Vacha M (2011) Absorption linear dichroism measured directly on a single light-harvesting system: the role of disorder in chlorosomes of green photosynthetic bacteria. J Am Chem Soc 133(17):6703–6710

  21. Furumaki S, Yabiku Y, Habuchi S, Tsukatani Y, Bryant D, Vacha M (2012) Circular dichroism measured on single chlorosomal light-harvesting complexes of green photosynthetic bacteria. J Phys Chem Lett 3:3545–3549

  22. Ganapathy S, Oostergetel G, Wawrzyniak P, Reus M, Gomez Maqueo Chew A, Buda F, Boekema E, Bryant D, Holzwarth A, de Groot H (2009) Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes. Proc Natl Acad Sci USA 106:8525–8530

  23. Gerola P, Olson J (1986) A new bacteriochlorophyll a-protein complex associated with chlorosomes of green sulfur bacteria. Biochim Biophys Acta 848:69–76

  24. Golecki J, Oelze J (1987) Quantitative relationship between bactenochlorophyll content, cytoplasmic membrane structure and chlorosome size in Chloroflexus aurantiacus. Arch Microbiol 148:236–241

  25. Gomez Maqueo Chew A, Frigaard N-U, Bryant D (2007) Bacteriochlorophyllide c C-82 and C-121 methyltransferases are essential for adaptation to low light in Chlorobaculum tepidum. J Bacteriol 189(17):6176–6184

  26. Graczyk A, Żurek JM, Paterson MJ (2014) On the linear and non-linear electronic spectroscopy of chlorophylls: a computational study. Photochem Photobiol Sci 13:103–111

  27. Gülen D (2006) Significance of the excitonic intensity borrowing in the J-/H-aggregates of bacteriochlorophylls/chlorophylls. Photosynth Res 87:205–214

  28. Gunther L, Jendrny M, Bloemsma E, Tank M, Oostergetel G, Bryant D, Knoester J, Köhler J (2016) Structure of light-harvesting aggregates in individual chlorosomes. J Phys Chem B 120:5367–5376

  29. Hartigan N, Tharia H, Sweeney F, Lawless A, Papiz M (2002) The 7.5-A electron density and spectroscopic properties of a novel low-light B800 LH2 from Rhodopseudomonas palustris. Biophys J 82:963–977

  30. Holzwarth AR, Schaffner K (1994) On the structure of bacteriochlorophyll molecular aggregates in the chlorosomes of green bacteria. A molecular modelling study. Photosynth Res 41:225–233

  31. Jendrny M, Aartsma T, Kӧhler J (2014) Insights into the excitonic states of individual chlorosomes from Chlorobaculum tepidum. Biophys J 106:1921–1927

  32. Krasnovsky A, Bystrova M (1980) Self-assembly of chlorophyll aggregated structures. BioSystems 12:181–194

  33. Lin S, Van Amerongen H, Struve W (1991) Ultrafast pump-probe spectroscopy of bacteriochlorophyll c antennae in bacteriochlorophyll a-containing chlorosomes from the green photosynthetic bacterium Chloroflexus aurantiacus. Biochim Biophys Acta 1060:13–22

  34. Linnanto J, Korppi-Tommola J (2008) Investigation on chlorosomal antenna geometries: tube, lamella and spiral-type self-aggregates. Photosynth Res 96:227–245

  35. Linnanto J, Korppi-Tommola J (2013) Exciton description of chlorosome to baseplate excitation energy transfer in filamentous anoxygenic phototrophs and green sulfur bacteria. J Phys Chem B 117:11144–11161

  36. Ma Y-Z, Cox R, 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 47:157–165

  37. Martiskainen J, Linnanto J, Kananavičius R, Lehtovuori V, Korppi-Tommola J (2009) Excitation energy transfer in isolated chlorosomes from Chloroflexus aurantiacus. Chem Phys Lett 477:216–220

  38. Martiskainen J, Linnanto J, Aumanen V, Myllyperkio P, Korppi-Tommola J, (2012) Excitation energy transfer in isolated chlorosomes from Chlorobaculum tepidum and Prosthecochloris aestuarii. Photochem Photobiol 88(3):675–683

  39. Mauring K, Novoderezhkin V, Taisova A, Fetisova Z (1999) Exciton levels structure of antenna bacteriochlorophyll c aggregates in the green bacterium Chloroflexus aurantiacus as probed by 1.8–293 K fluorescence spectroscopy. FEBS Lett 456:239–242

  40. 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 41:181–191

  41. Mirkovic T, Ostroumov E, Anna J, van Grondelle R, Govindjee SG (2017) Light absorption and energy transfer in the antenna complexes of photosynthetic organisms. Chem Rev 117(2):249–293

  42. Montaňo G, Wu H, Lin S, Brune D, Blankenship R (2003) Isolation and characterization of the B798 light-harvesting baseplate from the chlorosomes of Chloroflexus aurantiacus. Biochemistry 42:10246–10251

  43. Novoderezhkin V, Taisova A, Fetisova Z, Blankenship R, Savikhin S, Buck D, Struve W (1998) Energy transfers in the B808–866 antenna from the green bacterium Chloroflexus aurantiacus. Biophys J 74:2069–2075

  44. Novoderezhkin V, Taisova A, Fetisova Z (2001) Unit building block of the oligomeric chlorosomal antenna of the green photosynthetic bacterium Chloroflexus aurantiacus: modeling of nonlinear optical spectra. Chem Phys Lett 335:234–240

  45. Oelze J (1992) Light and oxygen regulation of the synthesis of bacteriochlorophyll a and bacteriochlorophyll c in Chloroflexus aurantiacus. J Bacteriol 174:5021–5026

  46. Oelze J, Golecki J (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, Dordrecht, pp 259–278

  47. Olson JM (1980) Chlorophyll organization in green photosynthetic bacteria. Biochim Biophys Acta 594:33–51

  48. Olson J (1998) Chlorophyll organization and function in green photosynthetic bacteria. Photochem Photobiol 67:61–75

  49. Oostergetel G, van Amerongen H, Boekema E (2010) The chlorosome: a prototype for efficient light harvesting in photosynthesis. Photosynth Res 104(2–3):245–255

  50. Orf G, Blankenship R (2013) Chlorosome antenna complexes from green photosynthetic bacteria. Photosynth Res 116:315–331

  51. Pandit A, de Groot H (2012) Solid-state NMR applied to photosynthetic light-harvesting complexes. Photosynth Res 111:219–226

  52. Pierson B, Castenholz R (1974) Pigments and growth in Chloroflexus aurantiacus, a phototrophic filamentous bacterium. Arch Microbiol 100:283–305

  53. Pierson B, Castenholz R (1992) The family Chloroflexaceae. In: Balows A, Trüper H, Dworkin M, Harder W, Schleifer K (eds) The prokaryotes, vol 4, 2nd edn. Springer, Heidelberg, pp 3754–3774

  54. Pierson B, Castenholz R (1995) Taxonomy and physiology of filamentous anoxygenic phototrophs. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer Academic Publishers, Dordrecht, pp 31–47

  55. Prokhorenko VI, Steensgaard DB, Holzwarth AR (2000) Exciton dynamics in the chlorosomal antennae of the green bacteria Chloroflexus aurantiacus and Chlorobium tepidum. Biophys J 79:2105–2120

  56. Prokhorenko VI, Steensgaard DB, Holzwarth AR (2003) Exciton theory for supramolecular chlorosomal aggregates: 1. Aggregate size dependence of the linear spectra. Biophys J 85:3173–3186

  57. Pšenčik J, Ikonen T, Laurinmäki P, Merckel M, Butcher S, Serimaa R, Tuma R (2004) Lamellar organization of pigments in chlorosomes, the light harvesting system of green bacteria. Biophys J 87:1165–1172

  58. Pšenčik J, Torkkeli M, Zupčanová A, Vácha F, Serimaa R, Tuma R (2010) The lamellar spacing in self-assembling bacteriochlorophyll aggregates is proportional to the length of the esterifying alcohol. Photosynth Res 104:211–219

  59. Pšenčik J, Arellano J, Collins A, Laurinmäki P, Torkkeli M, Lӧflund B, Serimaa R, Blankenship R, Tuma R, Butcher S (2013) Structural and functional roles of carotenoids in chlorosomes. J Bacteriol 195:1727–1734

  60. Rich A, Tinoco I Jr (1960) The effect of chain length upon hypochromism in nucleic acids and polynucleotides. J Am Chem Soc 82:6409–6410

  61. 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 102:18–23

  62. Savikhin S, Zhu Y, Lin S, Blankenship RE, Struve WS (1994) Femtosecond spectroscopy of chlorosome antennas from the green photosynthetic bacterium Chloroflexus aurantiacus. J Phys Chem 98:10322–10334

  63. Savikhin S, Buck D, Struve W, Blankenship R, Taisova A, Novoderezhkin V, Fetisova Z (1998) Exciton delocalization in the bacteriochlorophyll c antenna of the green bacterium Chloroflexus aurantiacus as revealed by ultrafast pump-probe spectroscopy. FEBS Lett 430:323–326

  64. Sawaya N, Huh J, Fujita T, Saikin S, Aspuru-Guzik A (2015) Fast delocalization leads to robust long-range excitonic transfer in a large quantum chlorosome model. Nano Lett 15:1722–1729

  65. Scherz A, Parson WW (1984a) Oligomers of bacteriochlophyll and bacteriophyophytin with spectroscopic properties resembling those found in photosynthetic bacteria. Biochim Biophys Acta 766:653–665

  66. Scherz A, Parson WW (1984b) Exciton interactions in dimers of bacteriochlorophyll and related molecules. Biochim Biophys Acta 766:666–678

  67. Schmidt K, Maarzahl M, Mayer F (1980) Development and pigmentation of chlorosomes in Chloroflexus aurantiacus Ok-70-fl. Arch Microbiol 127:87–97

  68. Scholes GD, Fleming GR, Alexandra Olaya-Castro A, van Grondelle R (2011) Lessons from nature about solar light harvesting. Nat Chem 3:763–774

  69. 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 91:3787–3796

  70. 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 46:7062–7068

  71. 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 49:7504–7515

  72. Smith K, Kehres L, Fajer J (1983) Aggregation of bacteriochlorophylls c, d or e. Models for the antenna chlorophylls of green and brown photosynthetic bacteria. J Am Chem Soc 105:1387–1389

  73. Sprague S, Staehelin L, DiBartolomeis M, Fuller R (1981) Isolation and development of chlorosomes in the green bacterium Chloroflexus aurantiacus. J Bacteriol 147:1021–1031

  74. Staehelin L, Golecki J, Fuller R, Drews G (1978) Visualization of the supramolecular architecture of chlorosomes (Chlorobium type vesicles) in freeze-fractured cells of Chloroflexus aurantiacus. Arch Microbiol 119:269–277

  75. Taisova A, Gulen D, Iseri E, Drachev V, Cherenkova T, Fetisova Z (2001) Antenna-size dependent hyperchromism of the Q y absorption band of chlorosomal oligomeric bacteriochlorophyll (BChl) c antennae of green bacteria. Photosynth Res 69:9

  76. Taisova A, Keppen O, Lukashev E, Arutyunyan A, Fetisova Z (2002) Study of the chlorosomal antenna of the green mesophilic filamentous bacterium Oscillochloris trichoides. Photosynth Res 74:73–85

  77. Taisova A, Keppen O, Novikov A, Naumova M, Fetisova Z (2006) Some factors controlling the biosynthesis of chlorosome antenna bacteriochlorophylls in green filamentous anoxygenic phototrophic bacteria of the family Oscillochloridaceae. Microbiology 75(2):129–135

  78. Tamiaki H (1996) Supramolecular structure in extramembraneous antennae of green photosynthetic bacteria. Coord Chem Rev 148:183–197

  79. Tamiaki H, Amakawa M, Holzwarth AR, Schaffner K (2002) Aggregation of synthetic metallochlorins in hexane. A model of chlorosomal bacteriochlorophyll self-assemblies in green bacteria. Photosynth Res 71:59–67

  80. Tamiaki H, Shibata R, Mizoguchi T (2007) The 17-propionate function of (bacterio)chlorophylls: biological implication of their long esterifying chains in photosynthetic systems. Photochem Photobiol 83:152–162

  81. Tinoco I (1960) Hypochromism in polynucleotides. J Am Chem Soc 82:4785–4790

  82. Tinoco I Jr (1962) Theoretical Aspects of Optical Activity. Part Two: Polymers Advances in Chemical Physics, vol 4, pp 113–160. Interscience Publishers, New York.

  83. Umetsu M, Wang ZY, Kobayashi M, Nozawa T (1999) Interaction of photosynthetic pigments with various organic solvents: magnetic circular dichroism approach and application to chlorosomes. Biochim Biophys Acta 1410:19–31

  84. Van Dorssen R, Amesz J (1988) Pigment organization and energy transfer in the green photosynthetic bacterium Chloroflexus aurantiacus. III. Energy transfer in whole cells. Photosynth Res 15:177–189

  85. Van Amerongen H, Vasmel H, van Grondelle R (1988) Linear dichroism of chlorosomes from Chloroflexus aurantiacus in compressed gels and electric fields. Biophys J 54:65–76

  86. 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 9:33–45

  87. Yakovlev A, Novoderezhkin V, Taisova A, Fetisova Z (2002a) Exciton dynamics in the chlorosomal antenna of the green bacterium Chloroflexus aurantiacus: experimental and theoretical studies of femtosecond pump-probe spectra. Photosynth Res 71:19–32

  88. Yakovlev A, Taisova A, Fetisova Z (2002b) Light control over the size of an antenna unit building block as an effecient strategy for light harvesting in photosynthesis. FEBS Lett 512:129–132

  89. Yakovlev A, Taisova A, Arutyunyan A, Shuvalov V, Fetisova Z (2017) Variability of aggregation extent of light-harvesting pigments in peripheral antenna of Chloroflexus aurantiacus. Photosynth Res 133:343–356

  90. Yakovlev AG, Taisova AS, Shuvalov VA, Fetisova ZG (2018) Estimation of the bacteriochlorophyll c oligomerisation extent in Chloroflexus aurantiacus chlorosomes by very low-frequency vibrations of the pigment molecules: a new approach. Biophys Chem 240:1–8

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The authors are very grateful to Prof. Dr. Demet Gülen for fruitful cooperation and assistance in theoretical modeling. This work was supported in part by the Russian Foundation for Basic Research (Grants 18-04-00105a, 14-04-00295a).

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Yakovlev, A.G., Taisova, A.S. & Fetisova, Z.G. Q-band hyperchromism and B-band hypochromism of bacteriochlorophyll c as a tool for investigation of the oligomeric structure of chlorosomes of the green photosynthetic bacterium Chloroflexus aurantiacus. Photosynth Res (2020).

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  • Bacterial photosynthesis
  • Green bacteria
  • Chloroflexus aurantiacus
  • Chlorosome
  • Bacteriochlorophyll c antenna