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

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.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

Abbreviations

PCE:

Perchloroethylene

DMSO:

Dimethyl sulfoxide

TMAO:

Trimethyl amine oxide

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 52:1317–1323

    PubMed  Article  CAS  Google 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 25:3389–3402

    PubMed  Article  CAS  Google Scholar 

  3. Balch WE, Fox GE, Magrum LJ, Woese CR, Wolfe RS (1979) Methanogens: reevaluation of a unique biological group. Microbiol Rev 43:260–296

    PubMed  CAS  Google Scholar 

  4. Benson DA, Boguski MS, Lipman DJ, Ostell J, Ouellette BF (1998) Genbank. Nucleic Acids Res 26:1–7

    PubMed  Article  CAS  Google 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 67:4566–4572

    PubMed  Article  CAS  Google Scholar 

  6. Campbell BJ, Engel AS, Porter ML, Takai K (2006) The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4:458–468

    PubMed  Article  CAS  Google Scholar 

  7. Finster K, Liesack W, Tindall BJ (1997) Sulfurospirillum arcachonense sp. nov., a new microaerophilic sulfur-reducing bacterium. Int J Syst Bacteriol 47:1212–1217

    PubMed  Article  CAS  Google 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 10:2623–2634

    PubMed  Article  CAS  Google 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 61:1679–1687

    PubMed  CAS  Google Scholar 

  10. Holliger C, Wohlfarth G, Diekert G (1998) Reductive dechlorination in the energy metabolism of anaerobic bacteria. FEMS Microbiol Rev 22:383–398

    Article  CAS  Google Scholar 

  11. Huber JA, Butterfield DA, Baross JA (2003) Bacterial diversity in a subseafloor habitat following a deep-sea volcanic eruption. FEMS Microbiol Ecol 43:393–409

    PubMed  Article  CAS  Google 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 318:97–100

    PubMed  Article  CAS  Google 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 187:3020–3027

    PubMed  Article  Google 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):e16018

    Google 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 53:1801–1805

    PubMed  Article  CAS  Google 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 54:1477–1482

    PubMed  Article  CAS  Google 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 87:339–353

    PubMed  Article  CAS  Google 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 57:827–831

    PubMed  Article  CAS  Google Scholar 

  19. Komagata K, Suzuki K (1987) Lipid and cell-wall analysis in bacterial systematics. Method Microbiol 19:161–207

    Article  CAS  Google 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 2638–2657

    Google Scholar 

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

    Google 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 53:787–793

    PubMed  Article  CAS  Google 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 49:145–150

    PubMed  Article  CAS  Google Scholar 

  24. Marmur J, Doty P (1962) Determination of the base composition of deoxyribonucleic acid from its thermal denaturation temperature. J Mol Biol 5:109–118

    PubMed  Article  CAS  Google 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 52:1789–1797

    PubMed  Article  CAS  Google 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 2:233–241

    Article  CAS  Google 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 52:1299–1304

    PubMed  Article  CAS  Google 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 54:41–45

    PubMed  Article  CAS  Google Scholar 

  29. Nakagawa S, Takai K (2008) Deep-sea vent chemoautotrophs: diversity, biochemistry and ecological significance. FEMS Microbiol Ecol 65:1–14

    PubMed  Article  CAS  Google 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 55:599–605

    PubMed  Article  CAS  Google 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 55:925–933

    PubMed  Article  CAS  Google 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 104:12146–12150

    PubMed  Article  CAS  Google Scholar 

  33. Porter ML, Engel AS (2008) Diversity of uncultured Epsilonproteobacteria from terrestrial sulfidic caves and springs. Appl Environ Microbiol 74:4973–4977

    PubMed  Article  CAS  Google Scholar 

  34. Porter KG, Feig YS (1980) The use of DAPI for identifying and counting microflora. Limnol Oceanogr 25:943–948

    Article  Google 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 46:1099–1104

    PubMed  Article  CAS  Google 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 163:48–56

    Article  CAS  Google 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 158:287–293

    Article  CAS  Google 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 3:194–202

    PubMed  Google 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 58:1598–1602

    PubMed  Article  CAS  Google 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 49:1177–1180

    PubMed  Article  CAS  Google 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 71:5440–5450

    PubMed  Article  CAS  Google 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 218:167–174

    PubMed  CAS  Google 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 54:25–32

    PubMed  Article  CAS  Google 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 71:7310–7320

    PubMed  Article  CAS  Google 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 55:183–189

    PubMed  Article  CAS  Google 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 56:1725–1733

    PubMed  Article  CAS  Google 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 26:552–569

    Article  CAS  Google Scholar 

  48. Tamaoka J, Komagata K (1984) Determination of DNA base composition by reverse-phase high-performance liquid chromatography. FEMS Microbiol Lett 25:125–128

    Article  CAS  Google 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 28:2731–2739

    PubMed  Article  CAS  Google Scholar 

  50. Timmer-ten Hoor A (1975) A new type of thiosulphate oxidizing, nitrate reducing microorganisms: Thiomicrospira denitrificans sp. nov. Neth J Sea Res 9:344–350

    Article  CAS  Google Scholar 

  51. Trüper HG, Schlegel HG (1964) Sulfur metabolism in Thiorhodaceae. Quantitative measurements on growing cells of Chromatium okenii. Antonie Leeuwenhoek 30:225–238

    Article  Google Scholar 

  52. Yamamoto M, Takai K (2011) Sulfur metabolisms in epsilon- and gamma-proteobacteria in deep-sea hydrothermal fields. Front Microbiol 2:1–8

    Google 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 172:3959–3965

    PubMed  CAS  Google Scholar 

Download references

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).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Hiroko Makita.

Additional information

Communicated by Harald Huber.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Makita, H., Nakagawa, S., Miyazaki, M. et al. 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. Arch Microbiol 194, 785–794 (2012). https://doi.org/10.1007/s00203-012-0814-1

Download citation

Keywords

  • Epsilonproteobacteria
  • Hydrogen-oxidizing
  • Sulfur-reducing
  • Chemolithoautotroph
  • Hydrothermal field
  • Mariana