1887

Abstract

A novel mesophilic bacterium, strain GO25, was isolated from a nest of hydrothermal vent polychaetes, sp., at the Iheya North field in the Mid-Okinawa Trough. Cells were motile short rods with a single polar flagellum. Growth was observed between 4 and 35 °C (optimum 30 °C; 13–16 h doubling time) and between pH 5.4 and 8.6 (optimum pH 6.1). The isolate was a facultatively anaerobic chemolithoautotroph capable of growth using molecular hydrogen, elemental sulfur or thiosulfate as the sole energy source, carbon dioxide as the sole carbon source, ammonium or nitrate as the sole nitrogen source and elemental sulfur, thiosulfate or yeast extract as the sole sulfur source. Strain GO25 represents the first deep-sea epsilonproteobacterium capable of growth by both hydrogen and sulfur oxidation. Nitrate or molecular oxygen (up to 10 % partial pressure) could serve as the sole electron acceptor to support growth. Metabolic products of nitrate reduction shifted in response to the electron donor provided. The G+C content of genomic DNA was 37.6 mol%. Phylogenetic analysis based on 16S rRNA gene sequences indicated that the novel isolate belonged to the genus and was most closely related to OK10 (96.3 % sequence similarity). DNA–DNA hybridization demonstrated that the novel isolate could be differentiated genotypically from OK10. On the basis of the physiological and molecular properties of the novel isolate, the name sp. nov. is proposed, with strain GO25 (=JCM 13212=DSM 17229) as the type strain. DSM 1251 (=ATCC 33889) is phylogenetically associated with OK10 and GO25. Based on the phylogenetic relationship between DSM 1251, OK10 and GO25, we propose the reclassification of as comb. nov. (type strain DSM 1251=ATCC 33889). In addition, an emended description of the genus is proposed.

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2006-08-01
2024-12-10
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References

  1. Alain K., Querellou J., Lesongeur F., Pignet P., Crassous P., Raguenes G., Cueff V., Cambon-Bonavita M. A. 2002; Caminibacter hydrogeniphilus gen. nov., sp. nov. a novel thermophilic, hydrogen-oxidizing bacterium isolated from an East Pacific Rise hydrothermal vent. Int J Syst Evol Microbiol 52:1317–1323 [CrossRef]
    [Google Scholar]
  2. Allen S. E., Grimshaw H. M., Parkinson J. A., Quarmby C. 1974; Inorganic constituents: nitrogen. In Chemical Analysis of Ecological Materials pp  184–206 Edited by Allen S. E. London: Blackwell Scientific;
    [Google Scholar]
  3. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [CrossRef]
    [Google Scholar]
  4. Balch W. E., Fox G. E., Magrum L. J., Woese C. R., Wolfe R. S. 1979; Methanogens: reevaluation of a unique biological group. Microbiol Rev 43:260–296
    [Google Scholar]
  5. Benson D. A., Boguski M. S., Lipman D. J., Ostell J., Ouellette B. F. F. 1998; GenBank. Nucleic Acids Res 26:1–7 [CrossRef]
    [Google Scholar]
  6. Brinkhoff T., Kuever J., Muyzer G., Jannasch H. W. 2005; Genus VI. Thiomicrospira .. In Bergey's Manual of Systematic Bacteriology , 2nd edn. vol 2 part B pp  193–199 Edited by Brenner D. J., Krieg N. R., Staley J. T. New York: Springer;
    [Google Scholar]
  7. Campbell B. J., Jeanthon C., Kostka J. E., Luther G. W. III, Cary S. C. 2001; Growth and phylogenetic properties of novel bacteria belonging to the epsilon subdivision of the Proteobacteria enriched from Alvinella pompejana and deep-sea hydrothermal vents. Appl Environ Microbiol 67:4566–4572 [CrossRef]
    [Google Scholar]
  8. DeLong E. F. 1992; Archaea in coastal marine environments. Proc Natl Acad Sci U S A 89:5685–5689 [CrossRef]
    [Google Scholar]
  9. 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 [CrossRef]
    [Google Scholar]
  10. Gamo T. 1995; Wide variation of chemical characteristics of submarine hydrothermal fluids due to secondary modification process after high temperature water-rock interaction: a review. In Biogeochemical Processes and Ocean Flux in the Western Pacific pp  425–451 Edited by Sakai H., Nozaki Y. Tokyo: Terra Scientific Publishing;
    [Google Scholar]
  11. Gillis M., Vandamme P., De Vos P., Swings J., Kerster K. 2001; Polyphasic taxonomy. In Bergey's Manual of Systematic Bacteriology , 2nd edn. vol1 pp  43–48 Edited by Boone D. R., Castenholz R. W., Garity G. M. London: Springer;
    [Google Scholar]
  12. Hügler M., Wirsen C. O., Fuchs G., Taylor C. D., Sievert S. M. 2005; Evidence for autotrophic CO2 fixation via the reductive tricarboxylic acid cycle by members of the ϵ subdivision of Proteobacteria. J Bacteriol 187:3020–3027 [CrossRef]
    [Google Scholar]
  13. Inagaki F., Takai K., Kobayashi H., Nealson K. H., Horikoshi K. 2003; Sulfurimonas autotrophica gen. nov., sp. nov. a novel sulfur-oxidizing ϵ -proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. Int J Syst Evol Microbiol 53:1801–1805 [CrossRef]
    [Google Scholar]
  14. Inagaki F., Takai K., Nealson K. H., Horikoshi K. 2004; Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the ϵ - Proteobacteria isolated from Okinawa Trough hydrothermal sediments. Int J Syst Evol Microbiol 54:1477–1482 [CrossRef]
    [Google Scholar]
  15. Kodama Y., Watanabe K. 2004; Sulfuricurvum kujiense gen. nov., sp. nov., a facultatively anaerobic, chemolithoautotrophic, sulfur-oxidizing bacterium isolated from an underground crude-oil storage cavity. Int J Syst Evol Microbiol 54:2297–2300 [CrossRef]
    [Google Scholar]
  16. Kuenen J. G., Veldkamp H. 1972; Thiomicrospira pelophila , gen. n., sp. n., a new obligately chemolithotrophic colourless sulfur bacterium. Antonie van Leeuwenhoek 38:241–256 [CrossRef]
    [Google Scholar]
  17. Kuenen J. G., Robertson L. A., Tuovinen O. H. 1991; The genera Thiobacillus , Thiomicrospira , and Thiosphaera . In The Prokaryotes , 2nd edn. pp  2638–2657 Edited by Balows A., Trüper H. G., Dworkin M., Harder W., Schleifer K. H. New York: Springer;
    [Google Scholar]
  18. Lane D. J. 1991; 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics pp  115–176 Edited by Stackbrandt E., Goodfellow M. New York: Wiley;
    [Google Scholar]
  19. Ludwig W., Strunk O., Westram R. 28 other authors 2004; arb: a software environment for sequence data. Nucleic Acids Res 32:1363–1371 [CrossRef]
    [Google Scholar]
  20. Marmur J., Doty P. 1962; Determination of the base composition of deoxyribonucleic acid from its thermal denaturation temperature. J Mol Biol 5:109–118 [CrossRef]
    [Google Scholar]
  21. Miroshnichenko M. L., Kostrikina N. A., L'Haridon S., Jeanthon C., Hippe H., Stackebrandt E., Bonch-Osmolovskaya E. A. 2002; Nautilia lithotrophica gen. nov., sp. nov., a thermophilic sulfur-reducing epsilon-proteobacterium isolated from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 52:1299–1304 [CrossRef]
    [Google Scholar]
  22. Miroshnichenko M. L., L'Haridon S., Schumann P., Spring S., Bonch-Osmolovskaya E. A., Jeanthon C., Stackebrandt E. 2004; Caminibacter profundus sp. nov., a novel thermophile of Nautiliales ord. nov. within the class ‘ Epsilonproteobacteria ’, isolated from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 54:41–45 [CrossRef]
    [Google Scholar]
  23. Muyzer G., Teske A., Wirsen C. O., Jannasch H. W. 1995; Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 164:165–172 [CrossRef]
    [Google Scholar]
  24. Nakagawa S., Inagaki F., Takai K., Horikoshi K., Sako Y. 2005a; Thioreductor micantisoli gen. nov., sp. nov., a novel mesophilic, sulfur-reducing chemolithoautotroph within the ϵ - Proteobacteria isolated from the hydrothermal sediments in the Mid-Okinawa Trough. Int J Syst Evol Microbiol 55:599–605 [CrossRef]
    [Google Scholar]
  25. Nakagawa S., Takai K., Inagaki F., Horikoshi K., Sako Y. 2005b; Nitratiruptor tergarcus gen. nov., sp. nov. and Nitratifractor salsuginis gen. nov., sp. nov. nitrate-reducing chemolithoautotrophs of the ϵ - Proteobacteria isolated from a deep-sea hydrothermal system in the Mid-Okinawa Trough. Int J Syst Evol Microbiol 55:925–933 [CrossRef]
    [Google Scholar]
  26. Nakagawa S., Takai K., Inagaki F., Hirayama H., Nunoura T., Horikoshi K., Sako Y. 2005c; Distribution, phylogenetic diversity and physiological characteristics of epsilon- Proteobacteria in a deep-sea hydrothermal field. Environ Microbiol 7:1619–1632 [CrossRef]
    [Google Scholar]
  27. Porter K. G., Feig Y. S. 1980; The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948 [CrossRef]
    [Google Scholar]
  28. Schmidt H. A., Strimmer K., Vingron M., von Haeseler A. 2002; tree-puzzle: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504 [CrossRef]
    [Google Scholar]
  29. Suzuki Y., Sasaki T., Suzuki M., Nogi Y., Miwa T., Takai K., Nealson K. H., Horikoshi K. 2005; Novel chemoautotrophic endosymbiosis between a member of the epsilonproteobacteria and the hydrothermal-vent gastropod Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean. Appl Environ Microbiol 71, 5440–5450 [CrossRef]
  30. Takai K., Horikoshi K. 2000; Thermosipho japonicus sp. nov., an extremely thermophilic bacterium isolated from a deep-sea hydrothermal vent in Japan. Extremophiles 4:9–17 [CrossRef]
    [Google Scholar]
  31. Takai K., Komatsu T., Horikoshi K. 2001; Hydrogenobacter subterraneus sp. nov., an extremely thermophilic, heterotrophic bacterium unable to grow on hydrogen gas, from deep subsurface geothermal water. Int J Syst Evol Microbiol 51:1425–1435
    [Google Scholar]
  32. Takai K., Inagaki F., Nakagawa S., Hirayama H., Nunoura T., Sako Y., Nealson K. H., Horikoshi K. 2003; Isolation and phylogenetic diversity of members of previously uncultivated ϵ - Proteobacteria in deep-sea hydrothermal fields. FEMS Microbiol Lett 218:167–174
    [Google Scholar]
  33. Takai K., Gamo T., Tsunogai U., Nakayama N., Hirayama H., Nealson K. H., Horikoshi K. 2004a; Geochemical and microbiological evidence for a hydrogen-based, hyperthermophilic subsurface lithoautotrophic microbial ecosystem (HyperSLiME) beneath an active deep-sea hydrothermal field. Extremophiles 8:269–282
    [Google Scholar]
  34. Takai K., Oida H., Suzuki Y., Hirayama H., Nakagawa S., Nunoura T., Inagaki F., Nealson K. H., Horikoshi K. 2004b; Spatial distribution of marine crenarchaeota group I in the vicinity of deep-sea hydrothermal systems. Appl Environ Microbiol 70:2404–2413 [CrossRef]
    [Google Scholar]
  35. Takai K., Nealson K. H., Horikoshi K. 2004c; Hydrogenimonas thermophila gen. nov., sp. nov., a novel thermophilic, hydrogen-oxidizing chemolithoautotroph within the ϵ -Proteobacteria, isolated from a black smoker in a Central Indian Ridge hydrothermal field. Int J Syst Evol Microbiol 54:25–32 [CrossRef]
    [Google Scholar]
  36. Takai K., Hirayama H., Nakagawa T., Suzuki Y., Nealson K. H., Horikoshi K. 2004d; Thiomicrospira thermophila sp. nov., a novel microaerobic, thermotolerant, sulfur-oxidizing chemolithomixotroph isolated from a deep-sea hydrothermal fumarole in the TOTO caldera, Mariana Arc, Western Pacific. Int J Syst Evol Microbiol 54:2325–2333 [CrossRef]
    [Google Scholar]
  37. Takai K., Hirayama H., Nakagawa T., Suzuki Y., Nealson K. H., Horikoshi K. 2005a; Lebetimonas acidiphila gen. nov., sp. nov., a novel thermophilic, acidophilic, hydrogen-oxidizing chemolithoautotroph within the ‘ Epsilonproteobacteria ’, isolated from a deep-sea hydrothermal fumarole in the Mariana Arc. Int J Syst Evol Microbiol 55:183–189 [CrossRef]
    [Google Scholar]
  38. Takai K., Campbell B. J., Cary S. C. 8 other authors 2005b; Enzymatic and genetic characterization of carbon and energy metabolisms by deep-sea hydrothermal chemolithoautotrophic isolates of Epsilonproteobacteria . Appl Environ Microbiol 71:7310–7320 [CrossRef]
    [Google Scholar]
  39. Tamaoka J., Komagata K. 1984; Determination of DNA base composition by reversed-phase high-performance liquid chromatography. FEMS Microbiol Lett 25:125–128 [CrossRef]
    [Google Scholar]
  40. Timmer-ten Hoor A. 1975; A new type of thiosulphate oxidizing, nitrate reducing microorganisms: Thiomicrospira denitrificans sp. nov. Neth J Sea Res 9:344–350 [CrossRef]
    [Google Scholar]
  41. Urakawa H., Dubilier N., Fujiwara Y., Cunningham D. E., Kojima S., Stahl D. A. 2005; Hydrothermal vent gastropods from the same family (Provannidae) harbour ϵ - and γ -proteobacterial endosymbionts. Environ Microbiol 7:750–754 [CrossRef]
    [Google Scholar]
  42. Voordeckers J. W., Starovoytov V., Vetriani C. 2005; Caminibacter mediatlanticus sp. nov., a thermophilic, chemolithoautotrophic, nitrate-ammonifying bacterium isolated from a deep-sea hydrothermal vent on the Mid Atlantic Ridge. Int J Syst Evol Microbiol 55:773–779 [CrossRef]
    [Google Scholar]
  43. Wayne L. G., Brenner D. J., Colwell R. R. 9 other authors 1987; International Committee on Systematic Bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464 [CrossRef]
    [Google Scholar]
  44. Zillig W., Holz I., Janekovic D. 7 other authors 1990; Hyperthermus butylicus , a hyperthermophilic sulfur-reducing archaebacterium that ferments peptides. J Bacteriol 172:3959–3965
    [Google Scholar]
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