Skip to main content
Log in

Thermotomaculum hydrothermale gen. nov., sp. nov., a novel heterotrophic thermophile within the phylum Acidobacteria from a deep-sea hydrothermal vent chimney in the Southern Okinawa Trough

  • Original Paper
  • Published:
Extremophiles Aims and scope Submit manuscript

Abstract

A novel heterotrophic, thermophilic bacterium, designated strain AC55T, was isolated from a deep-sea hydrothermal vent chimney at the Hatoma Knoll in the Okinawa Trough, Japan. Cells of strain AC55T were non-motile, long rods (2.0- to 6.8-μm long and 0.3- to 0.6-μm wide). The strain was an obligatory anaerobic heterotroph capable of fermentative growth on complex proteinaceous substances. Elemental sulfur was reduced to hydrogen sulfide but did not stimulate growth. Growth was observed between 37 and 60°C (optimum 55°C), pH 5.5 and 8.5 (optimum pH 6.6), and in the presence of 1.5–4.5% (w/v) NaCl (optimum 2.5%, w/v). Menaquinone-7 and -8 were the major respiratory quinones. The G + C content of the genomic DNA from strain AC55T was 51.6 mol%. The 16S rRNA gene sequence analysis revealed that strain AC55T was the first cultivated representative of Acidobacteria subdivision 10. Based on the physiological and phylogenetic features of the novel isolate, the genus name Thermotomaculum gen. nov. is proposed, with Thermotomaculum hydrothermale sp. nov. as the type species. The type strain is AC55T (=JCM 17643T = DSM 24660T = NBRC 107904T).

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Barns SM, Takala SL, Kuske CR (1999) Wide distribution and diversity of members of the bacterial kingdom Acidobacterium in the environment. Appl Environ Microbiol 65:1731–1737

    PubMed  CAS  Google Scholar 

  • Barns SM, Cain EC, Sommerville L, Kuske CR (2007) Acidobacteria phylum sequences in uranium-contaminated subsurface sediments greatly expand the known diversity within the phylum. Appl Environ Microbiol 73:3113–3116

    Article  PubMed  CAS  Google Scholar 

  • Baross JA (1995) Isolation, growth and maintenance of hyperthermophiles. In: Robb FT, Place RA (eds) Archaea; a laboratory manual, Thermophiles. Cold Spring Harbor Laboratory, New York, pp 15–23

    Google Scholar 

  • Brazelton WJ, Schrenk MO, Kelley DS, Baross JA (2006) Methane- and sulfur-metabolizing microbial communities dominate the lost city hydrothermal field ecosystem. Appl Environ Microbiol 72:6257–6270

    Article  PubMed  CAS  Google Scholar 

  • Bryant DA, Garcia Costas AM, Maresca JA, Chew AG, Klatt CG, Bateson MM, Tallon LJ, Hostetler J, Nelson WC, Heidelberg JF, Ward DM (2007) Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic Acidobacterium. Science 317:523–526

    Article  PubMed  CAS  Google Scholar 

  • Coates JD, Ellis DJ, Gaw CV, Lovley DR (1999) Geothrix fermentans gen. nov., sp. nov., a novel Fe(III)-reducing bacterium from a hydrocarbon-contaminated aquifer. Int J Syst Evol Microbiol 49:1615–1622

    CAS  Google Scholar 

  • Dedysh SN, Kulichevskaya IS, Serkebaeva YM, Mityaeva MA, Sorokin VV, Suzina NE, Rijpstra WI, Damsté JS (2011) Bryocella elongata gen. nov., sp. nov., a novel member of subdivision 1 of the Acidobacteria isolated from a methanotrophic enrichment culture, and emended description of Edaphobacter aggregans Koch et al. 2008. Int J Syst Evol Microbiol. doi:10.1099/ijs.0.031898-0 (in press)

  • Eichorst SA, Breznak JA, Schmidt TM (2007) Isolation and characterization of soil bacteria that define Terriglobus gen. nov., in the phylum Acidobacteria. Appl Environ Microbiol 73:2708–2717

    Article  PubMed  CAS  Google Scholar 

  • Fukunaga Y, Kurahashi M, Yanagi K, Yokota A, Harayama S (2008) Acanthopleuribacter pedis gen. nov., sp. nov., a marine bacterium isolated from a chiton, and description of Acanthopleuribacteraceae fam. nov., Acanthopleuribacterales ord. nov., Holophagaceae fam. nov., Holophagales ord. nov. and Holophagae classis nov. in the phylum ‘Acidobacteria’. Int J Syst Evol Microbiol 58:2597–2601

    Article  PubMed  CAS  Google Scholar 

  • Garcia Costas AM, Liu Z, Tomsho LP, Schuster SC, Ward DM, Bryant DA (2011) Complete genome of Candidatus Chloracidobacterium thermophilum, a chlorophyll-based photoheterotroph belonging to the phylum Acidobacteria. Environ Microbiol. doi:10.1111/j.1462-2920.2011.02592.x (in press)

  • Hugenholtz P, Pitulle C, Hershberger KL, Pace NR (1998) Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol 180:366–376

    PubMed  CAS  Google Scholar 

  • Imachi H, Sakai S, Hirayama H, Nakagawa S, Nunoura T, Takai K, Horikoshi K (2008) Exilispira thermophila gen. nov., sp. nov., an anaerobic, thermophilic spirochaete isolated from a deep-sea hydrothermal vent chimney. Int J Syst Evol Microbiol 58:2258–2265

    Article  PubMed  CAS  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132

    Google Scholar 

  • Kampe H, Dziallas C, Grossart HP, Kamjunke N (2010) Similar bacterial community composition in acidic mining lakes with different pH and lake chemistry. Microb Ecol 60:618–627

    Article  PubMed  CAS  Google Scholar 

  • Kishimoto N, Kosako Y, Tano T (1991) Acidobacterium capsulatum gen. nov., sp. nov.: an acidophilic chemoorganotrophic bacterium containing menaquinone from acidic mineral environment. Curr Microbiol 22:1–7

    Article  CAS  Google Scholar 

  • Kleinsteuber S, Müller FD, Chatzinotas A, Wendt-Potthoff K, Harms H (2007) Diversity and in situ quantification of Acidobacteria subdivision 1 in an acidic mining lake. FEMS Microbial Ecol 63:107–117

    Article  Google Scholar 

  • Koch IH, Gich F, Dunfield PF, Overmann J (2008) Edaphobacter modestus gen. nov., sp. nov., and Edaphobacter aggregans sp. nov., acidobacteria isolated from alpine and forest soils. Int J Syst Evol Microbiol 58:1114–1122

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kulichevskaya IS, Suzina NE, Liesack W, Dedysh SN (2010) Bryobacter aggregatus gen. nov., sp. nov., a peat-inhabiting, aerobic chemo-organotroph from subdivision 3 of the Acidobacteria. Int J Syst Evol Microbiol 60:301–306

    Article  PubMed  Google Scholar 

  • Kulichevskaya IS, Kostina LA, Valásková V, Rijpstra WI, Damsté JS, Boer W, Dedysh SN (2011) Acidicapsa borealis gen. nov., sp. nov. and A. ligni sp. nov., two novel subdivision 1 Acidobacteria from sphagnum peat and decaying wood. Int J Syst Evol Microbiol. doi:10.1099/ijs.0.034819-0 (in press)

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic Acid Techniques in Bacterial Systematics. Chichester, Wiley, pp 115–175

    Google Scholar 

  • Liesack W, Bak F, Kreft J, Stackebrandt E (1994) Holophaga foetida gen. nov., sp. nov., a new, homoacetogenic bacterium degrading methoxylated aromatic compounds. Arch Microbiol 162:85–90

    PubMed  CAS  Google Scholar 

  • López-García P, Duperron S, Philippot P, Foriel J, Susini J, Moreira D (2003) Bacterial diversity in hydrothermal sediment and epsilonproteobacterial dominance in experimental microcolonizers at the Mid-Atlantic Ridge. Environ Microbiol 5:961–976

    Article  PubMed  Google Scholar 

  • Ludwig W, Bauer SH, Bauer M, Held I, Kirchhof G, Schulze R, Huber I, Spring S, Hartmann A, Schleifer KH (1997) Detection and in situ identification of representatives of a widely distributed new bacterial phylum. FEMS Microbiol Lett 153:181–190

    Article  PubMed  CAS  Google Scholar 

  • Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar Buchner A, Lai T, Steppi S, Jobb G, Förster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, König A, Liss T, Lüssmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371

    Article  PubMed  CAS  Google Scholar 

  • Männistö MK, Rawat S, Starovoytov V, Häggblom MM (2010) Terriglobus saanensis sp. nov., a novel Acidobacterium isolated from tundra soil of Northern Finland. Int J Syst Evol Microbiol. doi:10.1099/ijs.0.026005-0 (in press)

  • Meisinger DB, Zimmermann J, Ludwig W, Schleifer KH, Wanner G, Schmid M, Bennett PC, Engel AS, Lee NM (2007) In situ detection of novel Acidobacteria in microbial mats from a chemolithoautotrophically based cave ecosystem (Lower Kane Cave, WY, USA). Environ Microbiol 9:1523–1534

    Article  PubMed  CAS  Google Scholar 

  • Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett JH (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241

    Article  CAS  Google Scholar 

  • Nakagawa S, Takai K (2006) Methods for the isolation of thermophiles from deep-sea hydrothermal environments. Method Microbiol 35:55–91

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Nakagawa S, Takai K, Horikoshi K, Sako Y (2003) Persephonella hydrogeniphila sp. nov., a novel thermophilic, hydrogen-oxidizing bacterium from a deep-sea hydrothermal vent chimney. Int J Syst Evol Microbiol 53:863–869

    Article  PubMed  CAS  Google Scholar 

  • Nakagawa S, Takai K, Inagaki F, Horikoshi K, Sako Y (2005) 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

    Article  PubMed  CAS  Google Scholar 

  • Nunoura T, Takai K (2009) Comparison of microbial communities associated with phase-separation-induced hydrothermal fluids at the Yonaguni Knoll IV hydrothermal field, the Southern Okinawa Trough. FEMS Microbiol Ecol 67:351–370

    Article  PubMed  CAS  Google Scholar 

  • Nunoura T, Oida H, Miyazaki M, Suzuki Y, Takai K, Horikoshi K (2007) Desulfothermus okinawensis sp. nov., a thermophilic and heterotrophic sulfate-reducing bacterium isolated from a deep-sea hydrothermal field. Int J Syst Evol Microbiol 57:2360–2364

    Article  PubMed  CAS  Google Scholar 

  • Nunoura T, Oida H, Nakaseama M, Kosaka A, Ohkubo SB, Kikuchi T, Kazama H, Hosoi-Tanabe S, Nakamura K, Kinoshita M, Hirayama H, Inagaki F, Tsunogai U, Ishibashi J, Takai K (2010) Archaeal diversity and distribution along thermal and geochemical gradients in hydrothermal sediments at the Yonaguni Knoll IV hydrothermal field in the Southern Okinawa Trough. Appl Environ Microbiol 76:1198–1211

    Article  PubMed  CAS  Google Scholar 

  • Pankratov TA, Dedysh SN (2010) Granulicella paludicola gen. nov., sp. nov., Granulicella pectinivorans sp. nov., Granulicella aggregans sp. nov. and Granulicella rosea sp. nov., acidophilic, polymer-degrading acidobacteria from Sphagnum peat bogs. Int J Syst Evol Microbiol 60:2951–2959

    Article  PubMed  CAS  Google Scholar 

  • Pankratov TA, Kirsanova LA, Kaparullina EN, Kevbrin VV, Dedysh N (2011) Telmatobacter bradus gen. nov., sp. nov., a cellulolytic facultative anaerobe from subdivision 1 of the Acidobacteria and emended description of Acidobacterium capsulatum Kishimoto et al. 1991. Int J Syst Evol Microbiol. doi:10.1099/ijs.0.029629-0 (in press)

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

    Article  Google Scholar 

  • Reysenbach A-L, Liu Y, Banta AB, Beveridge TJ, Kirshtein JD, Schouten S, Tivey MK, Von Damm KL, Voytek MA (2006) A ubiquitous thermoacidophilic archaeon from deep-sea hydrothermal vents. Nature 442:444–447

    Article  PubMed  CAS  Google Scholar 

  • Sait M, Hugenholtz P, Janssen PH (2002) Cultivation of globally distributed soil bacteria from phylogenetic lineages previously only detected in cultivation-independent surveys. Environ Microbiol 4:654–666

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, New York

    Google Scholar 

  • Santelli CM, Orcutt BN, Banning E, Bach W, Moyer CL, Sogin ML, Staudigel H, Edwards KJ (2008) Abundance and diversity of microbial life in ocean crust. Nature 453:653–656

    Article  PubMed  CAS  Google Scholar 

  • Sievert SM, Kuever J, Muyzer G (2000) Identification of 16S ribosomal DNA-defined bacterial populations at a shallow submarine hydrothermal vent near Milos Island (Greece). Appl Environ Microbiol 66:3102–3109

    Article  PubMed  CAS  Google Scholar 

  • Stott MB, Crowe MA, Mountain BW, Smirnova AV, Hou S, Alam M, Dunfield PF (2008) Isolation of novel bacteria, including a candidate division, from geothermal soils in New Zealand. Environ Microbiol 10:2030–2041

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Takai K, Nakagawa S, Reysenbach A-L, Hoek J (2006) Microbial ecology of mid-ocean ridges and back-arc basins. In Back-Arc spreading systems: geological, biological, chemical, geophysical interactions. In: Christie DM, Fisher CR, Sang-Mook L, Givens S (eds) Geophysical Monograph Series 166. American Geophysical Union, Washington, DC, pp 185–213

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Tamaoka J, Katayama-Fujimura Y, Kuraishi H (1983) Analysis of bacterial menaquinone mixtures by high performance lipid chromatography. J Appl Bacteriol 54:31–36

    Article  CAS  Google Scholar 

  • Ward NL, Challacombe JF, Janssen PH, Henrissat B, Coutinho PM, Wu M, Xie G, Haft DH, Sait M, Badger J, Barabote RD, Bradley B, Brettin TS, Brinkac LM, Bruce D, Creasy T, Daugherty SC, Davidsen TM, DeBoy RT, Detter JC, Dodson RJ, Durkin AS, Ganapathy A, Gwinn-Giglio M, Han CS, Khouri H, Kiss H, Kothari SP, Madupu R, Nelson KE, Nelson WC, Paulsen I, Penn K, Ren Q, Rosovitz MJ, Selengut JD, Shrivastava S, Sullivan SA, Tapia R, Thompson LS, Watkins KL, Yang Q, Yu C, Zafar N, Zhou L, Kuske CR (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol 75:2046–2056

    Article  PubMed  CAS  Google Scholar 

  • Zillig W, Holz I, 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 peptide. J Bacteriol 172:3959–3965

    PubMed  CAS  Google Scholar 

  • Zimmermann J, Gonzalez JM, Saiz-Jimenez C (2005) Detection and phylogenetic relationships of highly diverse uncultured acidobacterial communities in Altamira cave using 23S rRNA sequence analyses. Geomicrobiol J 22:379–388

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank the captain and the crew of R/V Natsushima and Hyper Dolphin for helping us to collect deep-sea hydrothermal vent samples. We are grateful to Dr. Katsuyuki Uematsu for assistance with the preparation of electron micrographs. This work was supported by the Institute for Fermentation, Osaka (IFO) and Japan Society for the Promotion of Science (JSPS).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Satoshi Nakagawa.

Additional information

Communicated by A. Oren.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1205 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Izumi, H., Nunoura, T., Miyazaki, M. et al. Thermotomaculum hydrothermale gen. nov., sp. nov., a novel heterotrophic thermophile within the phylum Acidobacteria from a deep-sea hydrothermal vent chimney in the Southern Okinawa Trough. Extremophiles 16, 245–253 (2012). https://doi.org/10.1007/s00792-011-0425-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-011-0425-9

Keywords

Navigation