Photosynthesis Research

, Volume 128, Issue 3, pp 235–241 | Cite as

Glycolipid analyses of light-harvesting chlorosomes from envelope protein mutants of Chlorobaculum tepidum

  • Yusuke Tsukatani
  • Tadashi Mizoguchi
  • Jennifer Thweatt
  • Marcus Tank
  • Donald A. Bryant
  • Hitoshi Tamiaki
Original Article


Chlorosomes are large and efficient light-harvesting organelles in green photosynthetic bacteria, and they characteristically contain large numbers of bacteriochlorophyll c, d, or e molecules. Self-aggregated bacteriochlorophyll pigments are surrounded by a monolayer envelope membrane comprised of glycolipids and Csm proteins. Here, we analyzed glycolipid compositions of chlorosomes from the green sulfur bacterium Chlorobaculum tepidum mutants lacking one, two, or three Csm proteins by HPLC equipped with an evaporative light-scattering detector. The ratio of monogalactosyldiacylglyceride (MGDG) to rhamnosylgalactosyldiacylglyceride (RGDG) was smaller in chlorosomes from mutants lacking two or three proteins in CsmC/D/H motif family than in chlorosomes from the wild-type, whereas chlorosomes lacking CsmIJ showed relatively less RGDG than MGDG. The results suggest that the CsmC, CsmD, CsmH, and other chlorosome proteins are involved in organizing MGDG and RGDG and thereby affect the size and shape of the chlorosome.


Bacteriochlorophyll Chlorosome Glycolipid Green sulfur bacteria Photosynthesis 





Evaporative light-scattering detector


Green sulfur bacteria







This work was partially supported by Grants-in-Aid for Scientific Research (A) (No. 22245030 to H.T.), for Scientific Research (C) (No. 24550065 to T.M.), for Young Scientists (B) (No. 26840099 to Y.T.), and for Scientific Research on Innovative Areas (“Artificial Photosynthesis,” No. 24107002 to H.T.) from the Japan Society for the Promotion of Science (JSPS). This work was also supported by the PRESTO (Precursory Research for Embryonic Science and Technology) program from the Japan Science and Technology Agency (JST). Work in the laboratory of D. A. B. was supported by grant DE-FG02-94ER20137 from the U. S. Department of Energy.


  1. Blankenship RE, Matsuura K (2003) Antenna complexes in green photosynthetic bacteria. In: Green BR, Parson WW (eds) Light-harvesting antennas in photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 195–217CrossRefGoogle Scholar
  2. Bryant DA, Vassilieva EV, Frigaard NU, Li H (2002) Selective protein extraction from Chlorobium tepidum chlorosomes using detergents: Evidence that CsmA forms multimers and binds bacteriochlorophyll a. Biochemistry 41:14403–14411CrossRefPubMedGoogle Scholar
  3. Bryant DA, Garcia Costas AM, Maresca JA, Chew AG, Klatt CG, Bateson MM, Tallon LJ, Hostetler J, Nelson WC, Heidelberg JF, Ward DM (2007) Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic acidobacterium. Science 317:523–526CrossRefPubMedGoogle Scholar
  4. Frigaard NU, Bryant DA (2001) Chromosomal gene inactivation in the green sulfur bacterium Chlorobium tepidum by natural transformation. Appl Environ Microbiol 67:2538–2544CrossRefPubMedPubMedCentralGoogle Scholar
  5. Frigaard NU, Bryant DA (2006) Chlorosomes: antenna organelles in photosynthetic green bacteria. In: Shively JM (ed) Complex structures in prokaryotes, vol 2. Springer, Berlin, pp 79–114CrossRefGoogle Scholar
  6. Frigaard NU, Matsuura K (1999) Oxygen uncouples light absorption by the chlorosome antenna and photosynthetic electron transfer in the green sulfur bacterium Chlorobium tepidum. Biochim Biophys Acta 1412:108–117CrossRefPubMedGoogle Scholar
  7. Frigaard NU, Voigt GD, Bryant DA (2002) Chlorobium tepidum mutant lacking bacteriochlorophyll c made by inactivation of the bchK gene, encoding bacteriochlorophyll c synthase. J Bacteriol 184:3368–3376CrossRefPubMedPubMedCentralGoogle Scholar
  8. Frigaard NU, Li H, Milks KJ, Bryant DA (2004) Nine mutants of Chlorobium tepidum each unable to synthesize a different chlorosome protein still assemble functional chlorosomes. J Bacteriol 186:646–653CrossRefPubMedPubMedCentralGoogle Scholar
  9. Frigaard NU, Li H, Martinsson P, Das SK, Frank HA, Aartsma TJ, Bryant DA (2005) Isolation and characterization of carotenosomes from a bacteriochlorophyll c-less mutant of Chlorobium tepidum. Photosynth Res 86:101–111CrossRefPubMedGoogle Scholar
  10. Ganapathy S, Oostergetel GT, Wawrzyniak PK, Reus M, Gomez Maqueo Chew A, Buda F, Boekema EJ, Bryant DA, Holzwarth AR, de Groot HJ (2009) Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes. Proc Natl Acad Sci USA 106:8525–8530CrossRefPubMedPubMedCentralGoogle Scholar
  11. Garcia Costas AM, Tsukatani Y, Romberger SP, Oostergetel GT, Boekema EJ, Golbeck JH, Bryant DA (2011) Ultrastructural analysis and identification of envelope proteins of “Candidatus Chloracidobacterium thermophilum” chlorosomes. J Bacteriol 193:6701–6711CrossRefPubMedPubMedCentralGoogle Scholar
  12. Garcia Costas AM, Tsukatani Y, Rijpstra WIC, Schouten S, Welander PV, Summons RE, Bryant DA (2012) Identification of the bacteriochlorophylls, carotenoids, quinones, lipids, and hopanoids of “Candidatus Chloracidobacterium thermophilum”. J Bacteriol 194:1158–1168CrossRefPubMedPubMedCentralGoogle Scholar
  13. Hanada S (2003) Filamentous anoxygenic phototrophs in hot springs. Microbes Environ 18:51–61CrossRefGoogle Scholar
  14. Holo H, Broch-Due M, Ormerod JG (1985) Glycolipids and the structure of chlorosomes in green bacteria. Arch Microbiol 143:94–99CrossRefGoogle Scholar
  15. Johnson TW, Li H, Frigaard NU, Golbeck JH, Bryant DA (2013) [2Fe-2S] proteins in chlorosomes: redox properties of CsmI, CsmJ, and CsmX of the chlorosome envelope of Chlorobaculum tepidum. Biochemistry 52:1331–1343CrossRefPubMedGoogle Scholar
  16. Li H, Bryant DA (2009) Envelope proteins of the CsmB/CsmF and CsmC/CsmD motif families influence the size, shape, and composition of chlorosomes in Chlorobaculum tepidum. J Bacteriol 191:7109–7120CrossRefPubMedPubMedCentralGoogle Scholar
  17. Li H, Frigaard NU, Bryant DA (2006) Molecular contacts for chlorosome envelope proteins revealed by cross-linking studies with chlorosomes from Chlorobium tepidum. Biochemistry 45:9095–9103CrossRefPubMedGoogle Scholar
  18. Li H, Frigaard NU, Bryant DA (2013) [2Fe-2S] proteins in chlorosomes: CsmI and CsmJ participate in light-dependent control of energy transfer in chlorosomes of Chlorobaculum tepidum. Biochemistry 52:1321–1330CrossRefPubMedGoogle Scholar
  19. Mizoguchi T, Yoshitomi T, Harada J, Tamiaki H (2011) Temperature- and time-dependent changes in the structure and composition of glycolipids during the growth of the green sulfur photosynthetic bacterium Chlorobaculum tepidum. Biochemistry 50:4504–4512CrossRefPubMedGoogle Scholar
  20. Mizoguchi T, Harada J, Yoshitomi T, Tamiaki H (2013a) A variety of glycolipids in green photosynthetic bacteria. Photosynth Res 114:179–188CrossRefPubMedGoogle Scholar
  21. Mizoguchi T, Tsukatani Y, Harada J, Takasaki S, Yoshitomi T, Tamiaki H (2013b) Cyclopropane-ring formation in the acyl groups of chlorosome glycolipids is crucial for acid resistance of green bacterial antenna systems. Bioorg Med Chem 21:3689–3694CrossRefPubMedGoogle Scholar
  22. Montaño 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 42:10246–10251CrossRefPubMedGoogle Scholar
  23. 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 104:233–243CrossRefPubMedGoogle Scholar
  24. Sørensen PG, Cox RP, Miller M (2008) Chlorosome lipids from Chlorobium tepidum: characterization and quantification of polar lipids and wax esters. Photosynth Res 95:191–196CrossRefPubMedGoogle Scholar
  25. Tamiaki H (1996) Supramolecular structure in extramembraneous antennae of green photosynthetic bacteria. Coord Chem Rev 148:183–197CrossRefGoogle Scholar
  26. Tamiaki H, Amakawa M, Shimono Y, Tanikaga R, Holzwarth AR, Schaffner K (1996) Synthetic zinc and magnesium chlorin aggregates as models for supramolecular antenna complexes in chlorosomes of green photosynthetic bacteria. Photochem Photobiol 63:92–99CrossRefGoogle Scholar
  27. Vassilieva EV, Stirewalt VL, Jakobs CU, Frigaard NU, Inoue-Sakamoto K, Baker MA, Sotak A, Bryant DA (2002) Subcellular localization of chlorosome proteins in Chlorobium tepidum and characterization of three new chlorosome proteins: CsmF, CsmH and CsmX. Biochemistry 41:4358–4370CrossRefPubMedGoogle Scholar
  28. Yoshitomi T, Mizoguchi T, Tamiaki H (2011) Characterization of glycolipids in light-harvesting chlorosomes from the green photosynthetic bacterium Chlorobium tepidum. Bull Chem Soc Jpn 84:395–402CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Earth-Life Science InstituteTokyo Institute of TechnologyTokyoJapan
  2. 2.PRESTO, Japan Science and Technology AgencySaitamaJapan
  3. 3.Graduate School of Life SciencesRitsumeikan UniversityShigaJapan
  4. 4.Department of Biochemistry and Molecular BiologyThe Pennsylvania State UniversityPennsylvaniaUSA
  5. 5.Department of Chemistry and BiochemistryMontana State UniversityMontanaUSA

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