Skip to main content
SpringerLink
Log in

Characterization of Exiguobacterium isolates from the Siberian permafrost. Description of Exiguobacterium sibiricum sp. nov.

  • Original Paper
  • Published:
Extremophiles Aims and scope Submit manuscript

Abstract

Three Gram-positive bacterial strains, 7-3, 255-15 and 190-11, previously isolated from Siberian permafrost, were characterized and taxonomically classified. These microorganisms are rod-shaped, facultative aerobic, motile with peritrichous flagella and their growth ranges are from −2.5 to 40°C. The chemotaxonomic markers indicated that the three strains belong to the genus Exiguobacterium. Their peptidoglycan type was A3α L-Lys-Gly. The predominant menaquinone detected in all three strains was MK7. The polar lipids present were phosphatidyl-glycerol, diphosphatidyl-glycerol and phosphatidyl-ethanolamine. The major fatty acids were iso-C13:0, anteiso-C13:0, iso-C15:0, C16:0 and iso-C17:0. Phylogenetic analysis based on 16S rRNA and six diverse genes, gyrB (gyrase subunit B), rpoB (DNA-directed RNA polymerase beta subunit), recA (homologous recombination), csp (cold shock protein), hsp70 (ClassI-heat shock protein—chaperonin) and citC (isocitrate dehydrogenase), indicated that the strains were closely related to Exiguobacterium undae (DSM 14481T) and Exiguobacterium antarcticum (DSM 14480T). On the basis of the phenotypic characteristics, phylogenetic data and DNA–DNA reassociation data, strain 190-11 was classified as E. undae, while the other two isolates, 7-3 and 255-15, comprise a novel species, for which the name Exiguobacterium sibiricum sp. nov. is proposed.

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

Similar content being viewed by others

References

  • Chen ML, Tsen HY (2002) Discrimination of Bacillus cereus and Bacillus thuringiensis with 16S rRNA and gyrB gene based PCR primers and sequencing of their annealing sites. J Appl Microbiol 92:912–919

    Article  PubMed  CAS  Google Scholar 

  • Collins MD, Pirouz T, Goodfellow M, Minnikin DE (1977) Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol 100:221–230

    PubMed  CAS  Google Scholar 

  • Collins MD, Lund BM, Farrow JAE, Schleifer KH (1983) Chemotaxonomic study of an alkalophilic bacterium, Exiguobacterium aurantiacum gen-nov., sp-nov. J Gen Microbiol 129:2037–2042

    CAS  Google Scholar 

  • Cowan ST, Steel KJ (1965) Manual for the identification of medical bacteria. Cambridge University Press, London

    Google Scholar 

  • Desoete G (1983) On the construction of optimal phylogenetic trees. Z Naturforsch C J Biosci 38:156–158

    CAS  Google Scholar 

  • Eden PA, Schmidt TM, Blakemore RP, Pace NR (1991) Phylogenetic analysis of Aquaspirillum magnetotacticum using polymerase chain reaction-amplified 16S rRNA-specific DNA. Int J Syst Bacteriol 41:324–325

    PubMed  CAS  Google Scholar 

  • Ezaki T, Hashimoto Y, Yabuuchi E (1989) Fluorometric deoxyribonucleic acid deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane-filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int J Syst Bacteriol 39:224–229

    Google Scholar 

  • Francis KP, Stewart GS (1997) Detection and speciation of bacteria through PCR using universal major cold-shock protein primer oligomers. J Ind Microbiol Biotechnol 19:286–293

    Article  PubMed  CAS  Google Scholar 

  • Fruhling A, Schumann P, Hippe H, Straubler B, Stackebrandt E (2002) Exiguobacterium undae sp. nov. and Exiguobacterium antarcticum sp. nov. Int J Syst Evol Microbiol 52:1171–1176

    Article  PubMed  CAS  Google Scholar 

  • Fukushima M, Kakinuma K, Kawaguchi R (2002) Phylogenetic analysis of Salmonella, Shigella, and Escherichia coli strains on the basis of the gyrB gene sequence. J Clin Microbiol 40:2779–2785

    Article  PubMed  CAS  Google Scholar 

  • Gilichinsky D, Rivkina E, Shcherbakova V, Laurinavichuis K, Tiedje J (2003) Supercooled water brines within permafrost—an unknown ecological niche for microorganisms: a model for astrobiology. Astrobiology 3:331–341

    Article  PubMed  CAS  Google Scholar 

  • Goris J, Suzuki K, Vos dP, Nakase T, Kersters K (1998) Evaluation of a microplate DNA–DNA hybridization method compared with the initial renaturation method. Can J Microbiol 44:1148–1153

    Article  CAS  Google Scholar 

  • Groth I, Schumann P, Weiss N, Martin K, Rainey FA (1996) Agrococcus jenensis gen. nov., sp. nov., a new genus of actinomycetes with diaminobutyric acid in the cell wall. Int J Syst Bacteriol 46:234–239

    PubMed  CAS  Google Scholar 

  • Kim W, Song MO, Song W, Kim KJ, Chung SI, Choi CS, Park YH (2003) Comparison of 16S rDNA analysis and rep-PCR genomic fingerprinting for molecular identification of Yersinia pseudotuberculosis. Antonie Van Leeuwenhoek 83:125–133

    Article  PubMed  CAS  Google Scholar 

  • Kim IG, Lee MH, Jung SY, Song JJ, Oh TK, Yoon JH (2005) Exiguobacterium aestuarii sp. nov. and Exiguobacterium marinum sp. nov., isolated from a tidal flat of the Yellow Sea in Korea. Int J Syst Evol Microbiol 55:885–889

    Article  PubMed  CAS  Google Scholar 

  • Ko KS, Lee HK, Park MY, Lee KH, Yun YJ, Woo SY, Miyamoto H, Kook YH (2002) Application of RNA polymerase beta-subunit gene (rpoB) sequences for the molecular differentiation of Legionella species. J Clin Microbiol 40:2653–2658

    Article  PubMed  CAS  Google Scholar 

  • Koneman E, Allen S, Dowell V, Sommers H (1979) Color atlas and text book of diagnostic microbiology. Lippincott, Philadelphia

    Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, West Sussex, England, pp 115–175

    Google Scholar 

  • Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A et al (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371

    Article  PubMed  CAS  Google Scholar 

  • MacKenzie SL (1987) Gas chromatographic analysis of amino acids as the N-heptafluorobutyryl isobutyl esters. J Assoc Off Anal Chem 70:151–160

    PubMed  CAS  Google Scholar 

  • Marmur J (1961) A procedure for the isolation of deoxyribonucleic acid from microorganisms. J Mol Biol 3:208–218

    Article  CAS  Google Scholar 

  • Matsumoto GI, Friedmann EI, Gilichinsky DA (1995) Geochemical characteristics of organic compounds in a permafrost sediment core sample from northeast Siberia, Russia. Proc NIPR Symp Antarct Meteorites 8:258–267

    PubMed  CAS  Google Scholar 

  • McKay CP, Friedmann EI, Meyer MA (1991) From Siberia to Mars. Planet Rep Mar–Apr:8–11

  • Miller L, Berger T (1984) Bacterial identification by gas chromatography and whole cell fatty acids. Hewlett-Packard, Palo Alto, pp. 228–241

    Google Scholar 

  • Minnikin DE, Collins MD, Goodfellow M (1979) Fatty-acid and polar lipid-composition in the classification of Cellulomonas, Oerskovia and related taxa. J Appl Bacteriol 47:87–95

    CAS  Google Scholar 

  • Olsen GJ, Matsuda H, Hagstrom R, Overbeek R (1994) FastDNAml—a tool for construction of phylogenetic trees of DNA-sequences using maximum-likelihood. Comput Appl Biosci 10:41–48

    PubMed  CAS  Google Scholar 

  • Rademaker JLW, Louws FJ, Bruijn FJ (1998) Characterisation of diversity of ecologically important microbes by rep-PCR fingerprinting. In: Akkermans ADL, van Elsas JD, Bruijn FJ (eds) Molecular microbial ecology manual, supplement 3. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 1–26

    Google Scholar 

  • Riley MS, Cooper VS, Lenski RE, Forney LJ, Marsh TL (2001) Rapid phenotypic change and diversification of a soil bacterium during 1000 generations of experimental evolution. Microbiology 147:995–1006

    PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Schleifer KH (1985) Analysis of the chemical composition and primary structure of murein. Methods Microbiol 18:123–156

    Article  CAS  Google Scholar 

  • Schleifer KH, Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36:407–477

    PubMed  CAS  Google Scholar 

  • Seurinck S, Verstraete W, Siciliano SD (2003) Use of 16S-23S rRNA intergenic spacer region PCR and repetitive extragenic palindromic PCR analyses of Escherichia coli isolates to identify nonpoint fecal sources. Appl Environ Microbiol 69:4942–4950

    Article  PubMed  CAS  Google Scholar 

  • Shi T, Reeves RH, Gilichinsky DA, Friedmann EI (1997) Characterization of viable bacteria from Siberian permafrost by 16S rDNA sequencing. Microb Ecol 33:169–179

    Article  PubMed  CAS  Google Scholar 

  • Versalovic J, Koeuth T, Lupski JR (1991) Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 19:6823–6831

    Article  PubMed  CAS  Google Scholar 

  • Vishnivetskaya T, Kathariou S, McGrath J, Gilichinsky D, Tiedje JM (2000) Low-temperature recovery strategies for the isolation of bacteria from ancient permafrost sediments. Extremophiles 4:165–173

    Article  PubMed  CAS  Google Scholar 

  • Watanabe K, Nelson J, Harayama S, Kasai H (2001) ICB database: the gyrB database for identification and classification of bacteria. Nucleic Acids Res 29:344–345

    Article  PubMed  CAS  Google Scholar 

  • Whitaker RJ, Grogan DW, Taylor JW (2003) Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301:976–978

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto S, Harayama S (1998) Phylogenetic relationships of Pseudomonas putida strains deduced from the nucleotide sequences of gyrB, rpoD and 16S rRNA genes. Int J Syst Bacteriol 48:813–819

    PubMed  CAS  Google Scholar 

  • Yamamoto S, Bouvet PJ, Harayama S (1999) Phylogenetic structures of the genus Acinetobacter based on gyrB sequences: comparison with the grouping by DNA–DNA hybridization. Int J Syst Bacteriol 49:87–95

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto S, Kasai H, Arnold DL, Jackson RW, Vivian A, Harayama S (2000) Phylogeny of the genus Pseudomonas: intrageneric structure reconstructed from the nucleotide sequences of gyrB and rpoD genes. Microbiology 146:2385–2394

    PubMed  CAS  Google Scholar 

  • Yumoto I, Hishinuma-Narisawa M, Hirota K, Shingyo T, Takebe F, Nodasaka Y, Matsuyama H, Hara I (2004) Exiguobacterium oxidotolerans sp. nov., a novel alkaliphile exhibiting high catalase activity. Int J Syst Evol Microbiol 54:2013–2017

    Article  PubMed  CAS  Google Scholar 

  • Zvyagintsev DG, Gilichinsky DA, Blagodatskii SA, Vorobyeva EA, Khlenikovan GM, Arkhangelov AA, Kudryavtseva NN (1985) Survival time of microorganisms in permanently frozen sedimentary rock and buried soils. Microbiology 54:155–161

    Google Scholar 

Download references

Acknowledgment

This work was supported by a cooperative agreement with NASA Astrobiology Institute number NCC2-1274.

Author information

Author notes

  1. Tatiana Vishnivetskaya

    Present address: Food Science Department, North Carolina State University, Schaub Hall Room 338, Box 7624, Raleigh, NC, 27695-7624, USA

Authors and Affiliations

  1. NASA Astrobiology Institute, Center for Microbial Ecology, Michigan State University, 540 Plant and Soil Science Building, East Lansing, MI, USA

    Debora Frigi Rodrigues, Johan Goris & James M. Tiedje

  2. Institute for Physicochemical and Biological Problems in Soil Science, Russian Academy of Sciences, 142290, Pushchino, Moscow Region, Russia

    Tatiana Vishnivetskaya & David Gilichinsky

  3. DOE Plant Research Laboratory, NASA Astrobiology Institute, Michigan State University, East Lansing, MI, 48824, USA

    Michael F. Thomashow

Authors
  1. Debora Frigi Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Johan Goris
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tatiana Vishnivetskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David Gilichinsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michael F. Thomashow
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. James M. Tiedje
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Debora Frigi Rodrigues.

Additional information

Communicated by K. Horikoshi

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rodrigues, D.F., Goris, J., Vishnivetskaya, T. et al. Characterization of Exiguobacterium isolates from the Siberian permafrost. Description of Exiguobacterium sibiricum sp. nov.. Extremophiles 10, 285–294 (2006). https://doi.org/10.1007/s00792-005-0497-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-005-0497-5

Keywords

Search

Navigation