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A novel lineage of sulfate-reducing microorganisms: Thermodesulfobiaceae fam. nov., Thermodesulfobium narugense, gen. nov., sp. nov., a new thermophilic isolate from a hot spring

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Abstract

A novel type of a sulfate-reducing microorganism, represented by strain Na82T, was isolated from a hot spring in Narugo, Japan. The isolate was a moderate thermophilic autotroph that was able to grow on H2/CO2 by sulfate respiration. The isolate could grow with nitrate in place of sulfate, and possessed menaquinone-7 and menaquinone-7(H2) as respiratory quinones. Phylogenetic analysis of the 16S rRNA gene sequence indicated that strain Na82T was a member of the domain Bacteria and distant from any known bacteria, as well as from other sulfate-reducing bacteria (sequence similarities less than 80%). The phylogenetic analysis of the dsrAB gene (alpha and beta subunits of dissimilatory sulfite reductase) sequence also suggested that strain Na82T was not closely related to other sulfate reducers. On the basis of the phenotypic and phylogenetic data, a new taxon is established for the isolate. We proposed the name Thermodesulfobium narugense gen. nov., sp. nov. with strain Na82T (=DSM 14796T=JCM 11510T) as the type strain. Furthermore, a new family, Thermodesulfobiaceae fam. nov., is proposed for the genus.

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References

  • Adachi J, Hasegawa M (1995) Improved dating of the human chimpanzee separation in the mitochondrial-DNA tree: heterogeneity among amino-acid sites. J Mol Evol 40:622–628

    CAS  PubMed  Google Scholar 

  • Beeder J, Torsvik T, Lien TL (1995) Thermodesulforhabdus norvegicus gen. nov., sp. nov., a novel thermophilic sulfate-reducing bacterium from oil field water. Arch Microbiol 164:331–336

    Article  CAS  PubMed  Google Scholar 

  • Bowman JP, Rea SM, McCammon SA, McMeekin TA (2000) Diversity and community structure within anoxic sediment from marine salinity meromictic lakes and a coastal meromictic marine basin, Vestfold Hills, Eastern Antarctica. Environ Microbiol 2:227–237

    Article  CAS  PubMed  Google Scholar 

  • Burggraf S, Jannasch HW, Nicolaus B, Stetter KO (1990) Archaeoglobus profundus sp. nov., represents a new species within the sulfate-reducing archaebacteria. Syst Appl Microbiol 13:24–28

    Google Scholar 

  • Cameron EM (1982) Sulfate and sulfate reduction in early Precambrian oceans. Nature 296:145–148

    CAS  Google Scholar 

  • Cottrell MT, Cary SC (1999) Diversity of dissimilatory bisulfite reductase genes of bacteria associated with the deep-sea hydrothermal vent polychaete annelid Alvinella pompejana. Appl Environ Microbiol 65:1127–1132

    CAS  PubMed  Google Scholar 

  • DSMZ (1993) Catalogue of strains, 5th edn. Gesellschaft fur Biotechnologische Forschung, Braunschweig, Germany

  • Friedrich MW (2002) Phylogenetic analysis reveals multiple lateral transfers of adenosine-5′-phosphosulfate reductase genes among sulfate-reducing microorganisms. J Bacteriol 184:278–289

    CAS  PubMed  Google Scholar 

  • Fry NK, Fredrickson JK, Fishbain S, Wagner M, Stahl DA (1997) Population structure of microbial communities associated with two deep, anaerobic, alkaline aquifers. Appl Environ Microbiol 63:1498–1504

    CAS  PubMed  Google Scholar 

  • Hanada S, Takaichi S, Matsuura K, Nakamura K (2002) Roseiflexus castenholzii gen. nov., sp. nov., a thermophilic, filamentous, photosynthetic bacterium that lacks chlorosomes. Int J Syst Evol Microbiol 52:187–193

    CAS  PubMed  Google Scholar 

  • Hasegawa M, Kishino H (1994) Accuracies of the simple methods for estimating the bootstrap probability of a maximum-likelihood tree. Mol Biol Evol 11:142–145

    CAS  Google Scholar 

  • Hasegawa M, Kishino H, Yano TA (1985) Dating of the human ape splitting by a molecular clock of mitochondrial-DNA. J Mol Evol 22:160–174

    CAS  PubMed  Google Scholar 

  • Hattori S, Kamagata Y, Hanada S, Shoun H (2000) Thermacetogenium phaeum gen. nov., sp. nov., a strictly anaerobic, thermophilic, syntrophic acetate-oxidizing bacterium. Int J Syst Evol Microbiol 50:1601–1609

    CAS  PubMed  Google Scholar 

  • Henry EA, Devereux R, Maki JS, Gilmour CC, Woese CR, Mandelco L, Schauder R, Remsen CC, Mitchell R (1994) Characterization of a new thermophilic sulfate-reducing bacterium – Thermodesulfovibrio yellowstonii, gen. nov. and sp. nov. – its phylogenetic relationship to Thermodesulfobacterium commune and their origins deep within the Bacterial domain. Arch Microbiol 161:62–69

    Article  CAS  PubMed  Google Scholar 

  • Huber H, Jannasch H, Rachel R, Fuchs T, Stetter KO (1997) Archaeoglobus veneficus sp. nov., a novel facultative chemolithoautotrophic hyperthermophilic sulfite reducer, isolated from abyssal black smokers. Syst Appl Microbiol 20:374–380

    CAS  Google Scholar 

  • Hugenholtz P (2002) Exploring prokaryotic diversity in the genomic era. Genome Biol 3:REVIEW003

    Article  Google Scholar 

  • 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  PubMed  Google Scholar 

  • Itoh T, Suzuki K, Sanchez PC, Nakase T (1999) Caldivirga maquilingensis gen. nov., sp. nov., a new genus of rod-shaped crenarchaeote isolated from a hot spring in the Philippines. Int J Syst Bacteriol 49:1157–1163

    CAS  PubMed  Google Scholar 

  • Jeanthon C, L'Haridon S, Cueff V, Banta A, Reysenbach AL, Prieur D (2002) Thermodesulfobacterium hydrogeniphilum sp. nov., a thermophilic, chemolithoautotrophic, sulfate-reducing bacterium isolated from a deep-sea hydrothermal vent at Guaymas Basin, and emendation of the genus Thermodesulfobacterium. Int J Syst Evol Microbiol 52:765–772

    Article  CAS  PubMed  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282

    CAS  PubMed  Google Scholar 

  • Kishino H, Miyata T, Hasegawa M (1990) Maximum-likelihood inference of protein phylogeny and the origin of chloroplasts. J Mol Evol 31:151–160

    CAS  Google Scholar 

  • Klein M, Friedrich M, Roger AJ, Hugenholtz P, Fishbain S, Abicht H, Blackall LL, Stahl DA, Wagner M (2001) Multiple lateral transfers of dissimilatory sulfite reductase genes between major lineages of sulfate-reducing prokaryotes. J Bacteriol 183:6028–6035

    Article  CAS  PubMed  Google Scholar 

  • Li L, Kato C, Horikoshi K (1999) Microbial diversity in sediments collected from the deepest cold-seep area, the Japan Trench. Mar Biotechnol 1:391–400

    CAS  PubMed  Google Scholar 

  • Minz D, Flax JL, Green SJ, Muyzer G, Cohen Y, Wagner M, Rittmann BE, Stahl DA (1999) Diversity of sulfate-reducing bacteria in oxic and anoxic regions of a microbial mat characterized by comparative analysis of dissimilatory sulfite reductase genes. Appl Environ Microbiol 65:4666–4671

    CAS  PubMed  Google Scholar 

  • Mori K, Yamamoto H, Kamagata Y, Hatsu M, Takamizawa K (2000) Methanocalculus pumilus sp. nov., a heavy-metal-tolerant methanogen isolated from a waste-disposal site. Int J Syst Evol Microbiol 50:1723–1729

    CAS  PubMed  Google Scholar 

  • Phelps CD, Kerkhof LJ, Young LY (1998) Molecular characterization of a sulfate-reducing consortium which mineralizes benzene. FEMS Microbiol Ecol 27:269–279

    CAS  Google Scholar 

  • Ravenschlag K, Sahm K, Knoblauch C, Jorgensen BB, Amann R (2000) Community structure, cellular rRNA content, and activity of sulfate-reducing bacteria in marine Arctic sediments. Appl Environ Microbiol 66:3592–3602

    Article  CAS  PubMed  Google Scholar 

  • Rees GN, Grassia GS, Sheehy AJ, Dwivedi PP, Patel BKC (1995) Desulfacinum infernum gen. nov., sp. nov., a thermophilic sulfate-reducing bacterium from a petroleum reservoir. Int J Syst Bacteriol 45:85–89

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Shintani T, Liu WT, Hanada S, Kamagata Y, Miyaoka S, Suzuki T, Nakamura K (2000) Micropruina glycogenica gen. nov., sp. nov., a new Gram-positive glycogen-accumulating bacterium isolated from activated sludge. Int J Syst Evol Microbiol 50:201–207

    CAS  PubMed  Google Scholar 

  • Sievert SM, Kuever J (2000) Desulfacinum hydrothermale sp. nov., a thermophilic, sulfate-reducing bacterium from geothermally heated sediments near Milos Island (Greece). Int J Syst Evol Microbiol 50:1239–1246

    CAS  PubMed  Google Scholar 

  • Sonne-Hansen J, Ahring BK (1999) Thermodesulfobacterium hveragerdense sp. nov. and Thermodesulfovibrio islandicus sp. nov., two thermophilic sulfate-reducing bacteria isolated from a Icelandic hot spring. Syst Appl Microbiol 22:559–564

    CAS  PubMed  Google Scholar 

  • Stackebrandt E, Sproer C, Rainey FA, Burghardt J, Pauker O, Hippe H (1997) Phylogenetic analysis of the genus Desulfotomaculum: evidence for the misclassification of Desulfotomaculum guttoideum and description of Desulfotomaculum orientis as Desulfosporosinus orientis gen. nov., comb. nov. Int J Syst Bacteriol 47:1134–1139

    CAS  PubMed  Google Scholar 

  • Stetter KO, Lauerer G, Thomm M, Neuner A (1987) Isolation of extremely thermophilic sulfate reducers: evidence for a novel branch of archaebacteria. Science 236:822–824

    CAS  Google Scholar 

  • Swofford DL (1998) PAUP*. In: Phylogenetic analysis using parsimony (* and other methods), version 4. Sinauer Associates, Sunderland, MA

  • Takai K, Horikoshi K (1999) Genetic diversity of archaea in deep-sea hydrothermal vent environments. Genetics 152:1285–1297

    CAS  PubMed  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 

  • Thomsen TR, Finster K, Ramsing NB (2001) Biogeochemical and molecular signatures of anaerobic methane oxidation in a marine sediment. Appl Environ Microbiol 67:1646–1656

    Article  CAS  PubMed  Google Scholar 

  • Wagner M, Roger AJ, Flax JL, Brusseau GA, Stahl DA (1998) Phylogeny of dissimilatory sulfite reductases supports an early origin of sulfate respiration. J Bacteriol 180:2975–2982

    CAS  PubMed  Google Scholar 

  • Wiegel J, Quandt L (1982) Determination of Gram type using the reaction between polymyxin B and lipopolysaccharides of the outer cell wall of whole bacteria. J Gen Microbiol 128:2261–2270

    CAS  PubMed  Google Scholar 

  • Zeikus JG, Dawson MA, Thompson TE, Ingvorsen K, Hatchikian EC (1983) Microbial ecology of volcanic sulphidogenesis: isolation and characterization of Thermodesulfobacterium commune gen. nov. and sp. nov. J Gen Microbiol 129:1159–1169

    CAS  Google Scholar 

Download references

Acknowledgments

We thank Xian-Ying Meng (National Institute of Advanced Industrial Science and Technology) for electron microscopy. The research was supported by the Ministry of Education, Science and Technology (MEST), Japan, through Special Coordination Fund "Archaean Park Project" (International Research Project on Interaction Between Sub-Vent Biosphere and Geo-Environments).

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Correspondence to Satoshi Hanada.

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Communicated by J. Wiegel

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Mori, K., Kim, H., Kakegawa, T. et al. A novel lineage of sulfate-reducing microorganisms: Thermodesulfobiaceae fam. nov., Thermodesulfobium narugense, gen. nov., sp. nov., a new thermophilic isolate from a hot spring. Extremophiles 7, 283–290 (2003). https://doi.org/10.1007/s00792-003-0320-0

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  • DOI: https://doi.org/10.1007/s00792-003-0320-0

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