Skip to main content
Log in

Thermobaculum terrenum gen. nov., sp. nov.: a non-phototrophic gram-positive thermophile representing an environmental clone group related to the Chloroflexi (green non-sulfur bacteria) and Thermomicrobia

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

A novel bacterium was cultivated from an extreme thermal soil in Yellowstone National Park, Wyoming, USA, that at the time of sampling had a pH of 3.9 and a temperature range of 65–92 °C. This organism was found to be an obligate aerobic, non-spore-forming rod, and formed pink-colored colonies. Phylogenetic analysis of the 16S rRNA gene sequence placed this organism in a clade composed entirely of environmental clones most closely related to the phyla Chloroflexi and Thermomicrobia. This bacterium stained gram-positive, contained a novel fatty-acid profile, had cell wall muramic acid content similar to that of Bacillus subtilis (significantly greater than Escherichia coli), and failed to display a lipopolysaccharide profile in SDS-polyacrylamide gels that would be indicative of a gram-negative cell wall structure. Ultrastructure examinations with transmission electron microscopy showed a thick cell wall (approximately 34 nm wide) external to a cytoplasmic membrane. The organism was not motile under the culture conditions used, and electron microscopic examination showed no evidence of flagella. Genomic G+C content was 56.4 mol%, and growth was optimal at 67 °C and at a pH of 7.0. This organism was able to grow heterotrophically on various carbon compounds, would use only oxygen as an electron acceptor, and its growth was not affected by light. A new species of a novel genus is proposed, with YNP1T (T=type strain) being Thermobaculum terrenum gen. nov., sp. nov. (16S rDNA gene GenBank accession AF391972). This bacterium has been deposited in the American Type Culture Collection (ATCC BAA-798) and the University of Oregon Culture Collection of Microorganisms from Extreme Environments (CCMEE 7001).

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2A, B
Fig. 3A; B
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acid Res 25:3389–3402

    CAS  PubMed  Google Scholar 

  • Amann RI, Ludwig W, Schleifer K-H (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143-169

    CAS  PubMed  Google Scholar 

  • Britton G (1985). General carotenoid methods. In: Law JH, Rillings HC (eds) Methods in enzymology, steroids and isoprenoids. Part B. Academic, Orlando, Florida, 111:113–149

  • Castenholz RW (2001) Class I. “Chloroflexi” In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology, 2nd edn, vol 1. Springer, Berlin, Heidelberg New York, pp 427

  • Chandler DP, Brockman FJ, Bailey TJ, Fredrickson JK (1998) Phylogenetic diversity of archaea and bacteria in a deep subsurface paleosol. Microb Ecol 36:37–50

    CAS  PubMed  Google Scholar 

  • De Jonge BLM, Chang Y-S, Gage D, Tomasz A (1992) Peptidoglycan composition of a highly methicillin-resistant Staphylococcus aureus strain. J Biol Chem 267:11248–11254

    PubMed  Google Scholar 

  • Dojka, M.A., Hugenholtz P, Haack SK, Pace NR (1998) Microbial diversity in a hydrocarbon- and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation. Appl Environ Microbiol 64:3869–3877

    CAS  PubMed  Google Scholar 

  • Ferris MJ, Muyzer G, Ward DM (1996) Denaturing gradient gel electrophoresis profiles of 16S rRNA-defined populations inhabiting a hot spring microbial mat community. Appl Environ Microbiol 62:340–346

    PubMed  Google Scholar 

  • Fliermans CB, Brock, TD (1972). Ecology of sulfur-oxidizing bacteria in hot acid soils. J. Bacteriol. 111:343–350

    Google Scholar 

  • Garrity GM, Holt JG (2001) Phylum BVI. Chloroflexi phy. nov. In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology, 2nd edn, vol 1. Springer, Berlin, Heidelberg New York, pp 427

  • Gupta RS (1998) Protein phylogenies and signature sequences: a reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol Mol Biol Rev 62:1435–1491

    CAS  PubMed  Google Scholar 

  • Hadzija O (1974) A simple method for the quantitative determination of muramic acid. Anal Biochem 60:512–517

    CAS  PubMed  Google Scholar 

  • Holt JG, Castenholz RW (2001) Family I. Herpetosiphonaceae, Genus I. Herpetosiphon Holt and Lewin 968, 2408AL. In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology, 2nd edn, vol 1. Springer, Berlin, Heidelberg New York, pp 445–446

  • Hugenholtz P, Pitulle C, Hershberger KL, Pace NR (1998) Novel division level bacterial diversity in a Yellowstone hot spring J Bacteriol 180:366–376

    CAS  Google Scholar 

  • Jackson TJ, Ramaley RF, Meinschein WG (1973) Thermomicrobium, a new genus of extremely thermophilic bacteria. Int J Syst Bacteriol 23:28–36

    Google Scholar 

  • Jackson CR, Langner HW, Donahoe-Christiansen J, Inskeep WP, McDermott TR (2001) Molecular analysis of microbial community structure in an arsenite-oxidizing acidic thermal spring. Environ Micro 3:532–542

    Article  CAS  Google Scholar 

  • Mazel D, Guglielmi G, Houmard S, Sidler W, Bryant DA, de Marsac NT (1986) Green light induces transcription of the phycoerythrin operon in the cyanobacterium Calothrix 7601. Nucleic Acids Res 14:8279–8290

    CAS  PubMed  Google Scholar 

  • Mesbah M, Premachandran U, Whitman WB (1989) Precise measurement of the G+C content of deoxyribonucleic acid by high-performance liquid chromatography. Int J Syst Bacteriol 39:159–167

    CAS  Google Scholar 

  • Nelson DC (1989) Physiology and biochemistry of filamentous sulfur bacteria. In Schlegel HG, Bowien B (eds) Autotrophic bacteria. Science Tech, Madison Wisconsin, pp 219–238.

  • Norris TB, Wraith JM, Castenholz RW, McDermott TR (2002) Soil microbial community structure across a thermal gradient following a geothermal heating event. Appl Environ Microbiol 68:6300–6309

    Article  CAS  PubMed  Google Scholar 

  • Oyaizu H, Debrunner-Vossbrinck B, Mandelco L, Studier JA, Woese CR (1987) The green non-sulfur bacteria: a deep branching in the eubacterial line of descent. System Appl Microbiol 9:47–53

    CAS  Google Scholar 

  • Page AL, Miller RH, Keeney DR (1982) Methods of soil analysis, 2nd edn. Soil Science Society of America, Madison, Wisonsin

  • Perry JJ (2001) Genus I. Thermomicrobium Jackson, Ramaley and Meinschein 1973, 34AL In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology, 2nd edn, vol 1. Springer, Berlin, Heidelberg New York, pp 448–450

  • Pfennig N, Trüper HG (1992) The Family Chromatiaceae. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-H (eds) The prokaryotes. A Handbook on the biology of bacteria: ecophysiology, isolation, identification, applications, vol. 4. Springer, Berlin Heidelberg New York pp 3320–3221

    Google Scholar 

  • Pierson BK (2001) Family I. Chloroflexaceae. Filamentous anoxygenic phototrophic bacteria. In: Boone DR Castenholz RW (eds) Bergey’s manual of systematic bacteriology, 2nd edn, vol 1. Springer, Berlin Heidelberg New York, pp 427–429

  • Pierson BK, Castenholz RW (1974a) A phototrophic gliding filamentous bacterium of hot springs, Chloroflexus aurantiacus, gen. and sp. nov. Arch Microbiol 100:5–24

    CAS  PubMed  Google Scholar 

  • Pierson BK, Castenholz RW (1974b) Studies of pigments and growth in Chloroflexus aurantiacus, a phototrophic filamentous bacterium. Arch Microbiol 100:283–305

    CAS  Google Scholar 

  • Pierson BK, Castenholz RW (2001) Genus I. Chloroflexus Pierson and Castenholz 1974a, 7AL In: Boone DR Castenholz RW (eds) Bergey’s manual of systematic bacteriology, 2nd edn, vol 1. Springer, Berlin Heidelberg New York. pp 429–437

  • Reynolds ES (1963) The use of lead citrate at high pH as electron opaque stain in electron microscopy. J Cell Biol 17:298–342

    Google Scholar 

  • Sambrook J, Frisch, EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York

    Google Scholar 

  • Smibert RM, Krieg NR (1994) Phenotypic characterization, In Gerhardt P, Murry RGE, Wood WA, Krieg (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington DC, pp 607–654.

  • Somerville JE, Kahn ML (1983) Cloning of the glutamine synthetase I gene from Rhizobium meliloti. J Bacteriol 156:168–176

    CAS  PubMed  Google Scholar 

  • Sparks DL, Page AL, Helmke PA, Loeppert RH (1996) Methods of soil analysis. Part 3. Soil Science Society of America, Madison, Wisconsin

  • Sprott GD, Koval SF, Schnaitman CA (1994) Cell fractionation, In Gerhardt P, Murry RGE, Wood WA, Krieg (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington DC pp 72–109

  • Spurr AR (1969) A low viscosity epoxy resin embedding medium for electron microscopy. J Ultrastr Res 26:31–43

    CAS  Google Scholar 

  • Summers ML, Botero LM, Busse SC, McDermott TR (2000) The Sinorhizobium meliloti Lon protease is involved in regulating exopolysaccharide synthesis and is required for nodulation of alfalfa. J Bacteriol 182:2551–2558.

    Article  CAS  PubMed  Google Scholar 

  • Teske A, Hinrichs K-U, Edgcomb V, de Vera Gomez A, Kysela D, Sylva SP, Sogin ML, Jannasch HW (2002) Microbial diversity of hydrothermal sediments in the Guaymas basin: evidence for anaerobic methanotrophic communities. Appl Environ Microbiol 68:1994–2007

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    PubMed  Google Scholar 

  • von Wintzingerode F, Selent B, Hegemann W, Gobel UB (1999) Phylogenetic analysis of an anaerobic, trichlorobenzene-transforming microbial consortium Appl Environ Microbiol 65:283–286

    Google Scholar 

Download references

Acknowledgements

The authors express gratitude for the enthusiastic help from Anne Deutch, Christie Hendrix, and John Varley, Yellowstone Center for Resources, Yellowstone National Park, Wyoming. The authors thank Bill Franck for help in temperature experiments, and in particular gratefully acknowledge Dr. Hans G. Trüper for assistance with nomenclature and Dr. Marci McClure for helpful discussion regarding in-depth sequence analysis. Funding to support this work was from the National Science Foundation (DEB-9809360) and the National Aeronautics and Space Administration (NAG5-8807).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Timothy R. McDermott.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Botero, L.M., Brown, K.B., Brumefield, S. et al. Thermobaculum terrenum gen. nov., sp. nov.: a non-phototrophic gram-positive thermophile representing an environmental clone group related to the Chloroflexi (green non-sulfur bacteria) and Thermomicrobia. Arch Microbiol 181, 269–277 (2004). https://doi.org/10.1007/s00203-004-0647-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-004-0647-7

Keywords

Navigation