Skip to main content

Advertisement

SpringerLink
Log in

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

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 26:39–48

    CAS  Google Scholar 

  • 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 363–379

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 401–421

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 35:17–25

    CAS  Google Scholar 

  • 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 85:2560–2565

    Article  PubMed  Google Scholar 

  • 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 65:301–306

    PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 32–85

    Google Scholar 

  • Overmann J, Cypionka H, Pfennig N (1992) An extremely low-light-adapted phototrophic bacterium from the Black Sea. Limnol Oceanogr 37:150–155

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Russ JC, DeHoff RT (2000) Practical stereology, 2nd edn. Plenum Press, New York, pp 39–47

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Seo D, Sakurai H (2002) Purification and characterization of ferredoxin-NAD(P)(+) reductase from the green sulfur bacterium Chlorobium tepidum. Biochim Biophys Acta 1597:123–132

    PubMed  CAS  Google Scholar 

  • Shively JM (1974) Inclusion bodies of prokaryotes. Annu Rev Microbiol 28:167–188. doi:10.1146/annurev.mi.28.100174.001123

    Article  PubMed  CAS  Google Scholar 

  • Smith KM, Bobe FW (1987) Light adaptation of bacteriochlorophyll-d producing bacteria by enzymatic methylation of their antenna pigments. J Chem Soc Chem Comm :276–277

  • Stanier RY, Smith JHC (1960) The chlorophylls of green bacteria. Biochim Biophys Acta 41:478–484. doi:10.1016/0006-3002(60)90045-7

    Article  PubMed  CAS  Google Scholar 

  • Wahlund TM, Madigan MT (1995) Genetic transfer by conjugation in the thermophilic green sulfur bacterium Chlorobium tepidum. J Bacteriol 177:2583–2588

    PubMed  CAS  Google Scholar 

  • 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 179:4859–4867

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology, Miami University, Oxford, OH, 45045, USA

    Rachael M. Morgan-Kiss

  2. Delaware Biotechnology Institute, University of Delaware, 15 Innovation Way, Newark, DE, 19711, USA

    Leong-Keat Chan, Shannon Modla, Timothy S. Weber, Kirk J. Czymmek & Thomas E. Hanson

  3. College of Marine and Earth Studies, University of Delaware, 700 Pilottown Road, Lewes, DE, 19958, USA

    Leong-Keat Chan, Mark Warner & Thomas E. Hanson

Authors
  1. Rachael M. Morgan-Kiss
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Leong-Keat Chan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shannon Modla
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Timothy S. Weber
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mark Warner
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kirk J. Czymmek
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Thomas E. Hanson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thomas E. Hanson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Morgan-Kiss, R.M., Chan, LK., Modla, S. et al. Chlorobaculum tepidum regulates chlorosome structure and function in response to temperature and electron donor availability. Photosynth Res 99, 11–21 (2009). https://doi.org/10.1007/s11120-008-9361-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-008-9361-7

Keywords

Search

Navigation