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Archives of Microbiology

, Volume 194, Issue 9, pp 785–794 | Cite as

Thiofractor thiocaminus gen. nov., sp. nov., a novel hydrogen-oxidizing, sulfur-reducing epsilonproteobacterium isolated from a deep-sea hydrothermal vent chimney in the Nikko Seamount field of the northern Mariana Arc

  • Hiroko MakitaEmail author
  • Satoshi Nakagawa
  • Masayuki Miyazaki
  • Ko-ichi Nakamura
  • Fumio Inagaki
  • Ken Takai
Original Paper

Abstract

A novel chemolithoautotrophic hydrogen-oxidizing and sulfur-reducing bacterium, strain 496ChimT, was isolated from a deep-sea hydrothermal vent chimney collected from the hydrothermal field at the summit of Nikko Seamount field, in the Mariana Arc. Cells were rods or curved rods, motile by means of a single polar flagellum. Growth was observed between 15 and 45 °C (optimum 37 °C; doubling time, 2.1 h) and between pH 5.3 and 8.0 (optimum pH 6.0). The isolate was a strictly anaerobic, obligate chemolithoautotroph capable of growth using molecular hydrogen as the sole energy source, carbon dioxide as the sole carbon source, ammonium or nitrate as the sole nitrogen source, and elemental sulfur as the electron acceptor. The G+C content of genomic DNA was 35 mol%. Phylogenetic analysis based on 16S rRNA gene sequences indicated that the new isolate belonged to the class Epsilonproteobacteria, but the isolate was distantly related to the previously described Epsilonproteobacteria species potentially at the genus level (<90 %). On the basis of its physiological and molecular characteristics, strain 496ChimT (=DSM 22050Τ = JCM 15747Τ = NBRC 105224Τ) represents the sole species of a new genus, Thiofractor, for which the name Thiofractor thiocaminus is proposed.

Keywords

Epsilonproteobacteria Hydrogen-oxidizing Sulfur-reducing Chemolithoautotroph Hydrothermal field Mariana 

Abbreviations

PCE

Perchloroethylene

DMSO

Dimethyl sulfoxide

TMAO

Trimethyl amine oxide

Notes

Acknowledgments

We would like to thank the captain and the crew of R/V Natsushima and ROV Hyper-Dolphin for helping to obtain deep-sea hydrothermal vent samples. We are grateful to Dr. Katsuyuki Uematsu for assistance with the preparation of electron micrographs and to Ms. Akane Tatedou and Mr. Nathan Johncock for help with nomenclature. This work was partially supported by the Institute for fermentation (IFO) and grant-in-aid from the Ministry Education, Culture, Sports, Science & Technology of Japan (No. 22760646).

Supplementary material

203_2012_814_MOESM1_ESM.docx (125 kb)
Supplementary Fig. S1 Time-course of production of hydrogen sulfide in the liquid phase (■) and concomitant bacterial growth (●) of strain 496ChimT. (DOCX 124 kb)
203_2012_814_MOESM2_ESM.docx (538 kb)
Supplementary Fig. S2 Polar lipid profiles of strain 496ChimT after two-dimensional TLC. DPG, diphosphatidylglycerol; PE, phosphatidylethanolamine; PS, phosphatidylserine; PL, phospholipids; and L1-2, unknown lipid. (DOCX 538 kb)

References

  1. Alain K, Querellou J, Lesongeur F, Pignet P, Crassous P, Raguénès G, Cueff V, Cambon-Bonavita MA (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 52:1317–1323PubMedCrossRefGoogle Scholar
  2. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  3. Balch WE, Fox GE, Magrum LJ, Woese CR, Wolfe RS (1979) Methanogens: reevaluation of a unique biological group. Microbiol Rev 43:260–296PubMedGoogle Scholar
  4. Benson DA, Boguski MS, Lipman DJ, Ostell J, Ouellette BF (1998) Genbank. Nucleic Acids Res 26:1–7PubMedCrossRefGoogle Scholar
  5. Campbell BJ, Jeanthon C, Kostka JE, Luther GW 3rd, Cary SC (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 67:4566–4572PubMedCrossRefGoogle Scholar
  6. Campbell BJ, Engel AS, Porter ML, Takai K (2006) The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4:458–468PubMedCrossRefGoogle Scholar
  7. Finster K, Liesack W, Tindall BJ (1997) Sulfurospirillum arcachonense sp. nov., a new microaerophilic sulfur-reducing bacterium. Int J Syst Bacteriol 47:1212–1217PubMedCrossRefGoogle Scholar
  8. Goffredi SK, Jones WJ, Erhlich H, Springer A, Vrijenhoek RC (2008) Epibiotic bacteria associated with the recently discovered Yeti crab, Kiwa hirsuta. Environ Microbiol 10:2623–2634PubMedCrossRefGoogle Scholar
  9. Haddad A, Camacho F, Durand P, Cary SC (1995) Phylogenetic characterization of the epibiotic bacteria associated with the hydrothermal vent polychaete Alvinella pompejana. Appl Environ Microbiol 61:1679–1687PubMedGoogle Scholar
  10. Holliger C, Wohlfarth G, Diekert G (1998) Reductive dechlorination in the energy metabolism of anaerobic bacteria. FEMS Microbiol Rev 22:383–398CrossRefGoogle Scholar
  11. Huber JA, Butterfield DA, Baross JA (2003) Bacterial diversity in a subseafloor habitat following a deep-sea volcanic eruption. FEMS Microbiol Ecol 43:393–409PubMedCrossRefGoogle Scholar
  12. Huber J, Mark Welch DB, Morrison HG, Huse SM, Neal PR, Butterfield DA, Sogin ML (2007) Microbial population structures in the deep marine biosphere. Science 318:97–100PubMedCrossRefGoogle Scholar
  13. Hügler M, Wirsen CO, Fuchs G, Taylor CD, Sievert SM (2005) Evidence for autotrophic CO2 fixation via the reductive tricarboxylic acid cycle by members of the ε subdivision of Proteobacteria. J Bacteriol 187:3020–3027PubMedCrossRefGoogle Scholar
  14. Hügler M, Petersen JM, Dubilier N, Imhoff JF, Sievert SM (2011) Pathways of carbon and energy metabolism of the epibiotic community associated with the deep-sea hydrothermal vent shrimp Rimicaris exoculata. PLoS One 7 6(1):e16018Google Scholar
  15. Inagaki F, Takai K, Nealson KH, 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 53:1801–1805PubMedCrossRefGoogle Scholar
  16. Inagaki F, Takai K, Nealson KH, 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 54:1477–1482PubMedCrossRefGoogle Scholar
  17. Jensen A, Finster K (2005) Isolation and characterization of Sulfurospirillum carboxydovorans sp. nov., a new microaerophilic carbon monoxide oxidizing epsilon Proteobacterium. Antonie Van Leeuwenhoek 87:339–353PubMedCrossRefGoogle Scholar
  18. Kodama Y, le Ha T, Watanabe K (2007) Sulfurospirillum cavolei sp. nov., a facultatively anaerobic sulfur-reducing bacterium isolated from an underground crude oil storage cavity. Int J Syst Evol Microbiol 57:827–831PubMedCrossRefGoogle Scholar
  19. Komagata K, Suzuki K (1987) Lipid and cell-wall analysis in bacterial systematics. Method Microbiol 19:161–207CrossRefGoogle Scholar
  20. Kuenen JG, Robertson LA, Tuovinen OH (1991) The genera Thiobacillus, Thiomicrospira, and Thiosphaera. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes, 2nd edn. Springer, New York, pp 2638–2657Google Scholar
  21. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–175Google Scholar
  22. Luijten ML, de Weert J, Smidt H, Boschker HT, de Vos WM, Schraa G, Stams AJ (2003) Description of Sulfurospirillum halorespirans sp. nov., an anaerobic, tetrachloroethene- respiring bacterium, and transfer of Dehalospirillum multivorans to the genus Sulfurospirillum as Sulfurospirillum multivorans comb. nov. Int J Syst Evol Microbiol 53:787–793PubMedCrossRefGoogle Scholar
  23. Luijten ML, Weelink SA, Godschalk B, Langenhoff AA, van Eekert MH, Schraa G, Stams AJ (2004) Anaerobic reduction and oxidation of quinone moieties and the reduction of oxidized metals by halorespiring and related organisms. FEMS Microbiol Ecol 49:145–150PubMedCrossRefGoogle Scholar
  24. Marmur J, Doty P (1962) Determination of the base composition of deoxyribonucleic acid from its thermal denaturation temperature. J Mol Biol 5:109–118PubMedCrossRefGoogle Scholar
  25. Meinersmann RJ, Patton CM, Evins GM, Wachsmuth IK, Fields PI (2002) Genetic diversity and relationships of Campylobacter species and subspecies. Int J Syst Evol Microbiol 52:1789–1797PubMedCrossRefGoogle Scholar
  26. Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M, Schaal K, Parlett JH (1984) An integrated procedure for extracting bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241CrossRefGoogle Scholar
  27. Miroshnichenko ML, Kostrikina NA, L’Haridon S, Jeanthon C, Hippe H, Stackebrandt E, Bonch-Osmolovskaya EA (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 52:1299–1304PubMedCrossRefGoogle Scholar
  28. Miroshnichenko ML, L’Haridon S, Schumann P, Spring S, Bonch-Osmolovskaya EA, 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 54:41–45PubMedCrossRefGoogle Scholar
  29. Nakagawa S, Takai K (2008) Deep-sea vent chemoautotrophs: diversity, biochemistry and ecological significance. FEMS Microbiol Ecol 65:1–14PubMedCrossRefGoogle Scholar
  30. 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 hydrothermal sediments in the Mid-Okinawa Trough. Int J Syst Evol Microbiol 55:599–605PubMedCrossRefGoogle Scholar
  31. 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 e-Proteobacteria isolated from a deep-sea hydrothermal system in the Mid-Okinawa Trough. Int J Syst Evol Microbiol 55:925–933PubMedCrossRefGoogle Scholar
  32. Nakagawa S, Takaki Y, Shimamura S, Reysenbach AL, Takai K, Horikoshi K (2007) Deep-sea vent epsilon-proteobacterial genomes provide insights into emergence of pathogens. Proc Natl Acad Sci USA 104:12146–12150PubMedCrossRefGoogle Scholar
  33. Porter ML, Engel AS (2008) Diversity of uncultured Epsilonproteobacteria from terrestrial sulfidic caves and springs. Appl Environ Microbiol 74:4973–4977PubMedCrossRefGoogle Scholar
  34. Porter KG, Feig YS (1980) The use of DAPI for identifying and counting microflora. Limnol Oceanogr 25:943–948CrossRefGoogle Scholar
  35. Sako Y, Takai K, Ishida Y, Uchida A, Katayama Y (1996) Rhodothermus obamensis sp. nov., a modern lineage of extremely thermophilic marine bacteria. Int J Syst Bacteriol 46:1099–1104PubMedCrossRefGoogle Scholar
  36. Scholz-Muramatsu H, Neumann A, Meßmer M, Moore E, Diekert G (1995) Isolation and characterization of Dehalospirillum multivorans gen. nov., sp. nov., a tetrachloroethene-utilizing, strictly anaerobic bacterium. Arch Microbiol 163:48–56CrossRefGoogle Scholar
  37. Schumacher W, Hole U, Kroneck PM (1992) Comparative systematic study on ‘‘Spirillum’’ 5175, Campylobacter and Wolinella species. Description of ‘‘Spirillum’’ 5175 as Sulfurospirillum deleyianum gen. nov., spec. nov. Arch Microbiol 158:287–293CrossRefGoogle Scholar
  38. Sikorski J, Munk C, Lapidus A, Ngatchou Djao OD, Lucas S, Glavina DRT, Nolan M, Tice H, Han C, Cheng JF, Tapia R, Goodwin L, Pitluck S, Liolios K, Ivanova N, Mavromatis K, Mikhailova N, Pati A, Sims D, Meincke L, Brettin T, Detter JC, Chen A, Palaniappan K, Land M, Hauser L, Chang YJ, Jeffries CD, Rohde M, Lang E, Spring S, Göker M, Woyke T, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk HP (2010) Complete genome sequence of Sulfurimonas autotrophica type strain (OK10). Stand Genomic Sci 3:194–202PubMedGoogle Scholar
  39. Smith JL, Campbell BJ, Hanson TE, Zhang CL, Cary SC (2008) Nautilia profundicola sp. nov., a thermophilic, sulfur-reducing epsilonproteobacterium from deep-sea hydrothermal vents. Int J Syst Evol Microbiol 58:1598–1602PubMedCrossRefGoogle Scholar
  40. Stolz JF, Ellis DJ, Switzer Blum J, Ahmann D, Lovley DR, Oremland RS (1999) Sulfurospirillum barnesii sp. nov. and Sulfurospirillum arsenophilum sp. nov., new members of the Sulfurospirillum clade of the ε-Proteobacteria. Int J Syst Bacteriol 49:1177–1180PubMedCrossRefGoogle Scholar
  41. Suzuki Y, Sasaki T, Suzuki M, Nogi Y, Miwa T, Takai K, Nealson KH, 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 71:5440–5450PubMedCrossRefGoogle Scholar
  42. Takai K, Inagaki F, Nakagawa S, Hirayama H, Nunoura T, Sako Y, Nealson KH, Horikoshi K (2003) Isolation and phylogenetic diversity of members of previously uncultivated ε-Proteobacteria in deep-sea hydrothermal fields. FEMS Microbiol Lett 218:167–174PubMedGoogle Scholar
  43. Takai K, Nealson KH, Horikoshi K (2004) 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 54:25–32PubMedCrossRefGoogle Scholar
  44. Takai K, Campbell BJ, Cary SC, Suzuki M, Oida H, Nunoura T, Hirayama H, Nakagawa S, Suzuki Y, Inagaki F, Horikoshi K (2005a) Enzymatic and genetic characterization of carbon and energy metabolisms by deep-sea hydrothermal chemolithoautotrophic isolates of Epsilonproteobacteria. Appl Environ Microbiol 71:7310–7320PubMedCrossRefGoogle Scholar
  45. Takai K, Hirayama H, Nakagawa T, Suzuki Y, Nealson KH, Horikoshi K (2005b) 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 55:183–189PubMedCrossRefGoogle Scholar
  46. Takai K, Suzuki M, Nakagawa S, Miyazaki M, Suzuki Y, Inagaki F, Horikoshi K (2006) Sulfurimonas paralvinellae sp. nov., a novel mesophilic, hydrogen- and sulfur-oxidizing chemolithoautotroph within the Epsilonproteobacteria isolated from a deep-sea hydrothermal vent polychaete nest, reclassification of Thiomicrospira denitrificans as Sulfurimonas denitrificans comb. nov. and emended description of the genus Sulfurimonas. Int J Syst Evol Microbiol 56:1725–1733PubMedCrossRefGoogle Scholar
  47. Takai K, Nunoura T, Horikoshi K, Shibuya T, Nakamura K, Suzuki Y, Stott M, Massoth GJ, Christenson BW, deRonde CEJ, Butterfield DA, Ishibashi J, Lupton JE, Evans LJ (2009) Variability in microbial communities in black smoker chimneys at the NW Caldera Vent Field, Brothers Volcano, Kermadec Arc. Geomicrobiol J 26:552–569CrossRefGoogle Scholar
  48. Tamaoka J, Komagata K (1984) Determination of DNA base composition by reverse-phase high-performance liquid chromatography. FEMS Microbiol Lett 25:125–128CrossRefGoogle Scholar
  49. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCrossRefGoogle Scholar
  50. Timmer-ten Hoor A (1975) A new type of thiosulphate oxidizing, nitrate reducing microorganisms: Thiomicrospira denitrificans sp. nov. Neth J Sea Res 9:344–350CrossRefGoogle Scholar
  51. Trüper HG, Schlegel HG (1964) Sulfur metabolism in Thiorhodaceae. Quantitative measurements on growing cells of Chromatium okenii. Antonie Leeuwenhoek 30:225–238CrossRefGoogle Scholar
  52. Yamamoto M, Takai K (2011) Sulfur metabolisms in epsilon- and gamma-proteobacteria in deep-sea hydrothermal fields. Front Microbiol 2:1–8Google Scholar
  53. Zillig W, Holz I, Janekovic D, Janekovic D, Klenk HP, Imsel E, Trent J, Wunderl S, Forjaz VH, Coutinho R, Ferreira T (1990) Hyperthermus butylicus, a hyperthermophilic sulfur-reducing archaebacterium that ferments peptides. J Bacteriol 172:3959–3965PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Hiroko Makita
    • 1
    Email author
  • Satoshi Nakagawa
    • 1
    • 2
  • Masayuki Miyazaki
    • 1
  • Ko-ichi Nakamura
    • 3
  • Fumio Inagaki
    • 4
  • Ken Takai
    • 1
  1. 1.Subsurface Geobiology and Advanced Research Project, Extremobiosphere Research Program, Institute of BiogeosciencesJapan Agency for Marine-Earth Science and Technology (JAMSTEC)YokosukaJapan
  2. 2.Laboratory of Microbiology, Faculty of Fisheries SciencesHokkaido UniversityHakodateJapan
  3. 3.National Institute of Advanced Industrial Science and TechnologyTsukubaJapan
  4. 4.Geomicrobiology Group, Kochi Institute for Core Sample ResearchJapan Agency for Marine-Earth Science and Technology (JAMSTEC)NankokuJapan

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