Photosynthesis Research

, Volume 99, Issue 1, pp 11–21 | Cite as

Chlorobaculum tepidum regulates chlorosome structure and function in response to temperature and electron donor availability

  • Rachael M. Morgan-Kiss
  • Leong-Keat Chan
  • Shannon Modla
  • Timothy S. Weber
  • Mark Warner
  • Kirk J. Czymmek
  • Thomas E. Hanson
Regular Paper

Abstract

Green sulfur bacteria (GSB) rely on the chlorosome, a light-harvesting apparatus comprised almost entirely of self-organizing arrays of bacteriochlorophyll (BChl) molecules, to harvest light energy and pass it to the reaction center. In Chlorobaculum tepidum, over 97% of the total BChl is made up of a mixture of four BChl c homologs in the chlorosome that differ in the number and identity of alkyl side chains attached to the chlorin ring. C. tepidum has been reported to vary the distribution of BChl c homologs with growth light intensity, with the highest degree of BChl c alkylation observed under low-light conditions. Here, we provide evidence that this functional response at the level of the chlorosome can be induced not only by light intensity, but also by temperature and a mutation that prevents phototrophic thiosulfate oxidation. Furthermore, we show that in conjunction with these functional adjustments, the fraction of cellular volume occupied by chlorosomes was altered in response to environmental conditions that perturb the balance between energy absorbed by the light-harvesting apparatus and energy utilized by downstream metabolic reactions.

Keywords

Bacteriochlorophyll c Chlorobaculum tepidum Chlorosome Green sulfur bacterium Sulfur oxidation Photoacclimation 

References

  1. Bobe FW, Pfennig N, Swansson KL, Smith KM (1990) Red shift of the absorption maxima in Chlorobineae through enzymatic methylation of their antenna bacteriochlorophylls. Biochem 29:4340–4348. doi:10.1021/bi00470a012 CrossRefGoogle Scholar
  2. Borrego CM, Garcia-Gil LJ (1994) Rearrangement of light harvesting bacteriochlorophyll homologs as a response of green sulfur bacteria to low light intensities. Photosynth Res 45:21–30. doi:10.1007/BF00032232 CrossRefGoogle Scholar
  3. Borrego CM, Gerola PD, Miller M, Cox RP (1999) Light intensity effects on pigment composition and organisation in the green sulfur bacterium Chlorobium tepidum. Photosynth Res 59:159–166. doi:10.1023/A:1006161302838 CrossRefGoogle Scholar
  4. Broch-Due M, Ormerod JG (1978) Isolation of a BChl c mutant from Chlorobium with BChl d by cultivation at low light intensities. FEMS Microbiol Lett 3:305–308. doi:10.1111/j.1574-6968.1978.tb01953.x CrossRefGoogle Scholar
  5. Bryant DA, Costas AM, Maresca JA, Chew AG, Klatt CG, Bateson MM et al (2007) Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic Acidobacterium. Science 317:523–526. doi:10.1126/science.1143236 PubMedCrossRefGoogle Scholar
  6. Causgrove DC, Brune J, Wang JL, Wittmershaus BP, Blankenship RE (1990) Energy transfer kinetics in whole cells and isolated chlorosomes of green photosynthetic bacteria. Photosynth Res 26:39–48Google Scholar
  7. Chan LK, Morgan-Kiss RM, Hanson TE (2008a) Genetic and proteomic studies of sulfur oxidation in Chlorobium tepidum (syn. Chlorobaculum tepidum). In: Hell R et al (eds) Sulfur in phototrophic organisms. Springer-Verlag, Berlin, pp 363–379Google Scholar
  8. Chan LK, Weber TS, Morgan-Kiss RM, Hanson TE (2008b) A genomic region required for phototrophic thiosulfate oxidation in the green sulfur bacterium Chlorobium tepidum (syn. Chlorobaculum tepidum). Microbiology 154:818–829. doi:10.1099/mic.0.2007/012583-0 PubMedCrossRefGoogle Scholar
  9. Chew AGM, Frigaard NU, Bryant DA (2007) Bacteriochlorophyllide c C-82 and C-121 methyltransferases are essential for adaptation to low light in Chlorobaculum tepidum. J Bacteriol 189:6176–6184. doi:10.1128/JB.00519-07 CrossRefGoogle Scholar
  10. Chung S, Shen G, Ormerod J, Bryant DA (1998) Insertional inactivation studies of the csmA and csmC genes of the green sulfur bacterium Chlorobium vibrioforme 8327: the chlorosome protein CsmA is required for viability but CsmC is dispensable. FEMS Microbiol Lett 164:353–368. doi:10.1111/j.1574-6968.1998.tb13109.x PubMedCrossRefGoogle Scholar
  11. 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 104:790–795. doi:10.1073/pnas.0605911104 PubMedCrossRefGoogle Scholar
  12. Eisen JA, Nelson KE, Paulsen IT, Heidelberg JF, Wu M, Dodson RJ et al (2002) The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium. Proc Natl Acad Sci USA 99:9509–9514. doi:10.1073/pnas.132181499 PubMedCrossRefGoogle Scholar
  13. Evans MC, Buchanan BB, Arnon DI (1966) A new ferredoxin-dependent carbon reduction cycle in a photosynthetic bacterium. Proc Natl Acad Sci USA 55:928–934. doi:10.1073/pnas.55.4.928 PubMedCrossRefGoogle Scholar
  14. Frigaard NU, Bryant DA (2001) Chromosomal gene inactivation in the green sulfur bacterium Chlorobium tepidum by natural transformation. Appl Environ Microbiol 67:2538–2544. doi:10.1128/AEM.67.6.2538-2544.2001 PubMedCrossRefGoogle Scholar
  15. Frigaard NU, 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. doi:10.1007/s00203-004-0718-9 PubMedCrossRefGoogle Scholar
  16. Frigaard NU, Takaichi S, Hirota M, Shimada K, Matsuura K (1997) Quinones in chlorosomes of green sulfur bacteria and their role in the redox-dependent fluorescence studied in chlorosome-like bacteriochlorophyll c aggregates. Arch Microbiol 167:343–349. doi:10.1007/s002030050453 CrossRefGoogle Scholar
  17. Frigaard NU, Chew AG, Li H, Maresca JA, Bryant DA (2003) Chlorobium tepidum: insights into the structure, physiology, and metabolism of a green sulfur bacterium derived from the complete genome sequence. Photosynth Res 78:93–117. doi:10.1023/B:PRES.0000004310.96189.b4 PubMedCrossRefGoogle Scholar
  18. Hanson TE, Tabita FR (2001) A ribulose-1, 5-bisphosphate carboxylase/oxygenase (RubisCO)-like protein from Chlorobium tepidum that is involved with sulfur metabolism and the response to oxidative stress. Proc Natl Acad Sci USA 98:4397–4402. doi:10.1073/pnas.081610398 PubMedCrossRefGoogle Scholar
  19. Heising S, Richter L, Ludwig W, Schink B (1999) Chlorobium ferrooxidans sp. nov., a phototrophic green sulfur bacterium that oxidizes ferrous iron in coculture with a “Geospirillum” sp. strain. Arch Microbiol 172:116–124. doi:10.1007/s002030050748 PubMedCrossRefGoogle Scholar
  20. Hohmann-Marriott MF, Blankenship RE, Roberson RW (2005) The ultrastructure of Chlorobium tepidum chlorosomes revealed by electron microscopy. Photosynth Res 86:145–154. doi:10.1007/s11120-005-3647-9 PubMedCrossRefGoogle Scholar
  21. Hüner NPA, Öquist G, Melis A (2003) Photostasis in plants, green algae and cyanobacteria: the role of light harvesting antenna complexes. In: Green BR, Parson WW (eds) Advances in photosynthesis and respiration light harvesting antennas in photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 401–421Google Scholar
  22. Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Ann Rev Physiol Plant Mol Biol 42:313–349. doi:10.1146/annurev.pp.42.060191.001525 CrossRefGoogle Scholar
  23. Kusumoto N, Inoue K, Nasu H, Sakuri H (1994) Preparation of a photoactive reaction center complex containing photo-reducible Fe–S centers and photooxidizable cytochrome c from he green sulfur bacterium Chlorobium tepidum. Plant Cell Physiol 35:17–25Google Scholar
  24. Montaño GA, Bowen BP, LaBelle JT, Woodbury NW, Pizziconi VB, Blankenship RE (2003) Characterization of Chlorobium tepidum chlorosomes: a calculation of bacteriochlorophyll c per chlorosome and oligomer modeling. Biophys J 85:2560–2565PubMedCrossRefGoogle Scholar
  25. Mukhopadhyay B, Johnson EF, Ascano MJ (1999) Conditions for vigorous growth on sulfide and reactor-scale cultivation protocols for the thermophilic green sulfur bacterium Chlorobium tepidum. Appl Environ Microbiol 65:301–306PubMedGoogle Scholar
  26. Nozawa T, Ohtomo K, Suzuki M, Morishita Y, Madigan MT (1991) Structures of bacteriochlorophyll c’s in chlorosomes from a new thermophilic bacterium Chlorobium tepidum. Chem Lett 20:1763–1766. doi:10.1246/cl.1991.1763 CrossRefGoogle Scholar
  27. Overmann J, Garcia-Pichel F (2006) The phototrophic way of life. In: Dworkin M et al (eds) The prokaryotes, 3rd edn. New York, Springer, pp 32–85Google Scholar
  28. Overmann J, Cypionka H, Pfennig N (1992) An extremely low-light-adapted phototrophic bacterium from the Black Sea. Limnol Oceanogr 37:150–155CrossRefGoogle Scholar
  29. Persson S, Sonksen CP, Frigaard N-U, Cox RP, Roepstorff P, Miller M (2000) Pigments and proteins in green bacterial chlorosomes studied by matrix-assisted laser desorption ionization mass spectrometry. Eur J Biochem 267:450–456. doi:10.1046/j.1432-1327.2000.01019.x PubMedCrossRefGoogle Scholar
  30. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212. doi:10.1083/jcb.17.1.208 PubMedCrossRefGoogle Scholar
  31. Russ JC, DeHoff RT (2000) Practical stereology, 2nd edn. Plenum Press, New York, pp 39–47Google Scholar
  32. Saga Y, Osumi S, Higuchi H, Tamiaki H (2005) Bacteriochlorophyll-c homolog composition in green sulfur photosynthetic bacterium Chlorobium vibrioforme dependent on the concentration of sodium sulfide in liquid cultures. Photosynth Res 86:123–130. doi:10.1007/s11120-005-5301-y PubMedCrossRefGoogle Scholar
  33. Seo D, Sakurai H (2002) Purification and characterization of ferredoxin-NAD(P)(+) reductase from the green sulfur bacterium Chlorobium tepidum. Biochim Biophys Acta 1597:123–132PubMedGoogle Scholar
  34. Shively JM (1974) Inclusion bodies of prokaryotes. Annu Rev Microbiol 28:167–188. doi:10.1146/annurev.mi.28.100174.001123 PubMedCrossRefGoogle Scholar
  35. Smith KM, Bobe FW (1987) Light adaptation of bacteriochlorophyll-d producing bacteria by enzymatic methylation of their antenna pigments. J Chem Soc Chem Comm :276–277Google Scholar
  36. Stanier RY, Smith JHC (1960) The chlorophylls of green bacteria. Biochim Biophys Acta 41:478–484. doi:10.1016/0006-3002(60)90045-7 PubMedCrossRefGoogle Scholar
  37. Wahlund TM, Madigan MT (1995) Genetic transfer by conjugation in the thermophilic green sulfur bacterium Chlorobium tepidum. J Bacteriol 177:2583–2588PubMedGoogle Scholar
  38. Wahlund TM, Tabita FR (1997) The reductive tricarboxylic acid cycle of carbon dioxide assimilation: initial studies and purification of ATP-citrate lyase from the green sulfur bacterium Chlorobium tepidum. J Bacteriol 179:4859–4867PubMedGoogle Scholar
  39. Wahlund TM, Woese CR, Castenholz R, Madigan MT (1991) A thermophilic green sulfur bacterium from New Zealand hot springs, Chlorobium tepidum sp. nov. Arch Microbiol 156:81–90. doi:10.1007/BF00290978 CrossRefGoogle Scholar
  40. Wilson KE, Ivanov AG, Öquist G, Grodzinski B, Sarhan F, Huner NPA (2006) Energy balance, organellar redox status, and acclimation to environmental stress. Can J Bot 84:1355–1370. doi:10.1139/B06-098 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Rachael M. Morgan-Kiss
    • 1
  • Leong-Keat Chan
    • 2
    • 3
  • Shannon Modla
    • 2
  • Timothy S. Weber
    • 2
  • Mark Warner
    • 3
  • Kirk J. Czymmek
    • 2
  • Thomas E. Hanson
    • 2
    • 3
  1. 1.Department of MicrobiologyMiami UniversityOxfordUSA
  2. 2.Delaware Biotechnology InstituteUniversity of DelawareNewarkUSA
  3. 3.College of Marine and Earth StudiesUniversity of DelawareLewesUSA

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