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A molecular and physiological survey of a diverse collection of hydrothermal vent Thermococcus and Pyrococcus isolates

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Abstract

Strains of hyperthermophilic anaerobic hydrothermal vent archaea maintained in the culture collection assembled by Holger Jannasch at the Woods Hole Oceanographic Institution between 1984 and 1998 were identified and partially characterized by Denaturing Gradient Gel Electrophoresis, 16S rRNA gene sequencing, and by growth tests at different temperatures and on different organic carbon and nitrogen sources. All strains were members of the genera Thermococcus and Pyrococcus. The greatest phylogenetic diversity was found in strains from a single Guaymas Basin core isolated by serial dilution from four different depth horizons of heated sediment incubated at the corresponding in situ temperatures. In contrast, geographically distinct vent locations and sample materials yielded a lower diversity of isolates when enriched under uniform temperature regimes and without prior dilution of the source material.

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References

  • Atomi H, Fukui T, Kanai T, Morikawa M, Imanaka T (2004) Description of Thermococcus kodakaraensis sp. nov., a well studied hyperthermophilic archaeon previously reported as Pyrococcus sp. KOD1. Archaea 1:263–267

    Article  CAS  PubMed  Google Scholar 

  • Bazylinski DA, Wirsen CO, Jannasch HW (1989) Microbial utilization of naturally-occurring hydrocarbons at the Guaymas Basin hydrothermal vent site. Appl Environ Microbiol 55:2832–2836

    CAS  PubMed  Google Scholar 

  • Dhillon A, Teske A, Dillon J, Stahl D, Sogin ML (2003) Molecular characterization of sulfate reducing bacteria in the Guaymas Basin. Appl Environ Microbiol 69:2765–2772

    Article  CAS  PubMed  Google Scholar 

  • Dhillon A, Lever M, Lloyd K, Albert DB, Sogin ML, Teske A (2005) Methanogen Diversity Evidenced by Molecular Characterization of Methyl Coenzyme M Reductase A (mcrA) Genes (mcrA) in Hydrothermal Sediments of the Guaymas Basin. Appl Environ Microbiol 71:4592–4601

    Article  CAS  PubMed  Google Scholar 

  • Dirmeier R, Keller M, Hafenbradl D, Braun FJ, Rachel R, Burggraf S, Stetter KO (1998) Thermococcus acidaminovorans sp. nov, a new hyperthermophilic alkalophilic archaeon growing on amino acids. Extremophiles 2:109–114

    Article  CAS  PubMed  Google Scholar 

  • Edgcomb VE, Molyneaux SJ, Saito MA, Lloyd K, Böer S, Wirsen CO, Atkins MS, Teske A (2004) Sulfide ameliorates metal toxicity in deep-sea hydrothermal vent archaea. Appl Environ Microbiol 70:2551–2555

    Article  CAS  PubMed  Google Scholar 

  • Edgcomb VE, Molyneaux SJ, Boer S, Wirsen CO, Atkins MS, Lloyd KG, Teske A (2007) Survival and growth of two heterotrophic hydrothermal vent archaea, Pyrococcus strain GB-D and Thermococcus fumicolans, under low pH and high sulfide concentrations in combination with high temperature and pressure regimes. Extremophiles 11:329–342

    Article  CAS  PubMed  Google Scholar 

  • Fujiwara S, Aki R, Yoshida M, Higashibata H, Imanaka T, Fukuda W (2008) Expression profiles and physiological roles of two types of molecular chaperonins from the hyperthermophilic archaeon Thermococcus kodakarensis. Appl Environ Microbiol 74:7306–7312

    Article  CAS  PubMed  Google Scholar 

  • Fukui T, Atomi H, Kanai T, Matsumi R, Fujiwara S, Imanaka T (2005) Complete genome sequence of the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1 and comparison with Pyrococcus genomes. Genome Res 15:352–363

    Article  CAS  PubMed  Google Scholar 

  • Guezennec JG, Dussauze J, Bian M, Rocchicioli F, Ringelberg D, Hedrick DB, White DC (1996) Bacterial community structure from Guaymas Basin, Gulf of California, as determined by analysis of phospholipid ester-linked fatty acids. J Mar Biotechnol 4:165–175

    CAS  Google Scholar 

  • Holden JF, Takai K, Summit M, Bolton S, Zyskowski J, Baross J (2001) Diversity among three novel groups of hyperthermophilic deep-sea Thermococcus species from three sites in the northeastern Pacific Ocean. FEMS Microbiol Ecol 36:51–60

    Article  CAS  PubMed  Google Scholar 

  • Huber R, Stöhr J, Hohenhaus S, Rachel R, Burggraf S, Jannsch HW, Stetter KO (1995) Thermococcus chitonophagus sp. nov., a novel, chitin-degrading, hyperthermophilic archaeum from a deep-sea hydrothermal vent environment. Arch Microbiol 164:255–264

    Article  CAS  Google Scholar 

  • Jannasch HW, Wirsen CO, Molyneaux SJ, Langworthy TA (1988) Extremely thermophilic fermentative archaebacteria of the genus Desulfurococcus from deep-sea hydrothermal vents. Appl Environ Microbiol 54:1203–1209

    PubMed  CAS  Google Scholar 

  • Jannasch HW, Wirsen CO, Molyneaux SJ, Langworthy TA (1992) Comparative physiological studies on hyperthermophilic archaea isolated from deep-sea hot vents with emphasis on Pyrococcus strain GB-D. Appl Environ Microbiol 58:3472–3481

    CAS  PubMed  Google Scholar 

  • Kelley DS, Baross JA, Delaney JR (2002) Volcanoes, fluids, and life at mid-ocean ridge spreading centers. Ann Rev Earth Planet Sci 30:385–491

    Article  CAS  Google Scholar 

  • Kuwabara T, Minaba M, Ogi N, Kamekura M (2007) Thermococcus celericrescens sp. nov., a fast-growing and cell-fusing hyperthermophilic archaeon from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 57:437–443

    Article  CAS  PubMed  Google Scholar 

  • LaPaglia C, Hartzell PL (1997) Stress-induced production of biofilm in the hyperthermophile Archaeoglobus fulgidus. Appl Environ Microbiol 63:3158–3163

    CAS  PubMed  Google Scholar 

  • Lee HS, Kang SG, Bae SS, Lim JK, Cho Y, Kim YJ, Jeon JH, Cha SS, Kwon KK, Kim HT, Park CJ, Lee HW, Kim SI, Chun J, Colwell RR, Kim SJ, Lee JH (2008) The complete genome sequence of Thermococcus onnurineus NA1 reveals a mixed heterotrophic and carboxydotrophic metabolism. J Bacteriol 190:7491–7499

    Article  CAS  PubMed  Google Scholar 

  • Lepage E, Marguet E, Geslin C, Matte-Tailliez O, Zillig W, Forterre P, Tailliez P (2004) Molecular diversity of new Thermococcales isolates from a single area of hydrothermal deep-sea vents as revealed by randomly amplified polymorphic DNA fingerprinting and 16S rRNA gene sequence analysis. Appl Environ Microbiol 70:1227–1286

    Article  CAS  Google Scholar 

  • Lloyd KG, Edgcomb VP, Molyneaux SJ, Boer S, Wirsen CO, Atkins MS, Teske A (2005) Effect of dissolved sulfide, pH, and temperature on growth and survival of marine hyperthermophilic archaea. Appl Environ Microbiol 71:6383–6387

    Article  CAS  PubMed  Google Scholar 

  • Marteinsson VT, Watrin L, Prieur D, Caprais JC, Raguénès G, Erauso G (1995) Phenotypic characterization, DNA similarities, and protein profiles of twenty sulfur-metabolizing hyperthermophilic anaerobic archaea isolated from hydrothermal vents in the Southwestern Pacific Ocean. Int J Syst Bact 45:623–632

    Article  CAS  Google Scholar 

  • Miroshnichenko ML, Bonch-Osmolovskaya EA (2006) Recent developments in the thermophilic microbiology of deep-sea hydrothermal vents. Extremophiles 10:85–96

    Article  PubMed  Google Scholar 

  • Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie van Leeuwenhoek 73:127–141

    Article  CAS  PubMed  Google Scholar 

  • Reysenbach AL, Shock EL (2002) Merging Genomes with geochemistry in hydrothermal ecosystems. Science 296:1077–1082

    Article  CAS  PubMed  Google Scholar 

  • Rinker KD, Kelly RM (1996) Growth physiology of the hyperthermophilic archaeon Thermococcus litoralis: development of a sulfur-free defined medium, characterization of an exopolysaccharide, and evidence of biofilm formation. Appl Environ Microbiol 62:4478–4485

    CAS  PubMed  Google Scholar 

  • Schouten S, Wakeham SG, Hopmans EC, Sinninghe Damste JS (2003) Biogeochemical evidence that thermophilic archaea mediate the anaerobic oxidation of methane. Appl Environ Microbiol 69:1680–1686

    Article  CAS  PubMed  Google Scholar 

  • Schrenk MO, Kelley DS, Delaney JR, Baross JA (2003) Incidence and diversity of microorganisms within the walls of an active deep-sea sulfide chimney. Appl Environ Microbiol 69:3580–3592

    Article  CAS  PubMed  Google Scholar 

  • Summit M, Baross J (1998) Thermophilic subseafloor microorganisms from the 1996 North Gorda Ridge eruption. Deep Sea Res II 45:2751–2766

    Article  Google Scholar 

  • Swofford DL (2000) PAUP* Phylogenetic analysis using parsimony (and other methods), version 4. Sinauer Associates, Sunderland, Massachusetts

    Google Scholar 

  • Teske A, Sigalevich P, Cohen Y, Muyzer G (1996) Molecular identification of bacteria from a coculture by denaturing gradient gel electrophoresis of 16S ribosomal DNA fragments as a tool for isolation in pure culture. Appl Environ Microbiol 62:4210–4215

    CAS  PubMed  Google Scholar 

  • Teske A, Brinkhoff T, Muyzer G, Moser DP, Rethmeier J, Jannasch HW (2000) Diversity of thiosulfate-oxidizing bacteria from marine sediments and hydrothermal vents. Appl Environ Microbiol 66:3125–3133

    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 in hydrothermal sediments in the Guaymas Basin: evidence for anaerobic methanotrophic communities. Appl Environ Microbiol 68:1994–2007

    Article  CAS  Google Scholar 

  • Weber A, Jørgensen BB (2002) Bacterial sulfate reduction in hydrothermal sediments of the Guaymas Basin, Gulf of California, Mexico. Deep Sea Res I 49:827–841

    Article  CAS  Google Scholar 

  • White JR, Escobar-Paramo P, Mongodin EF, Nelson KE, DiRuggiero J (2008) Extensive genome rearrangements and multiple horizontal gene transfers in a population of Pyrococcus isolates from Volcano Island, Italy. Appl Environ Microbiol 74:6447–6451

    Article  CAS  PubMed  Google Scholar 

  • Wirsen CO, Brinkhoff T, Küver J, Muyzer G, Molyneaux SJ, Jannasch HW (1998) Comparison of a new Thiomicrospira strain from the Mid-Atlantic Ridge with known hydrothermal vent isolates. Appl Environ Microbiol 64:4057–4059

    CAS  PubMed  Google Scholar 

  • Wolin EA, Wolin MJ, Wolfe RS (1963) Formation of methane by bacterial extracts. J Biol Chem 238:2882–2886

    CAS  PubMed  Google Scholar 

  • Zillig W, Reysenbach AL (2001) Thermococcaceae fam. nov. In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology, 2nd edition, volume 1: the archaea and the deeply branching and phototrophic bacteria. Springer, New York, pp 341–348

    Google Scholar 

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Acknowledgments

AT was supported by NSF (Lexen 9714195 and Bio-Oce 0647633). ARR was supported by an Allan Vining Davis fellowship. JRT was supported by a NSF graduate research fellowship. AdVG and VE were supported by the NASA Astrobiology Institute. SJM and CW were supported by NSF (Lexen 9714195).

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Author notes

  1. Adam R. Rivers & Janelle R. Thompson

    Present address: Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA

  2. Alvin de Vera Gomez

    Present address: Department of Cell Biology, University of Massachusetts Medical School, Worcester, MA, 01655, USA

Authors and Affiliations

  1. Department of Marine Sciences, University of North Carolina at Chapel Hill, 351 Chapman Hall, CB 3300, Chapel Hill, NC, 27599, USA

    Andreas Teske

  2. Department of Geology and Geophysics, Woods Hole Oceanographic Institution, Woods Hole, MA, 02453, USA

    Virginia Edgcomb

  3. Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA, 02453, USA

    Adam R. Rivers, Janelle R. Thompson, Alvin de Vera Gomez, Stephen J. Molyneaux & Carl O. Wirsen

Authors
  1. Andreas Teske
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  2. Virginia Edgcomb
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  3. Adam R. Rivers
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  6. Stephen J. Molyneaux
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  7. Carl O. Wirsen
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Corresponding author

Correspondence to Andreas Teske.

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Communicated by H. Santos.

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Teske, A., Edgcomb, V., Rivers, A.R. et al. A molecular and physiological survey of a diverse collection of hydrothermal vent Thermococcus and Pyrococcus isolates. Extremophiles 13, 905–915 (2009). https://doi.org/10.1007/s00792-009-0278-7

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  • DOI: https://doi.org/10.1007/s00792-009-0278-7

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