1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 71, Issue 7

sp. nov., a hyperthermophilic and piezophilic archaeon isolated from a deep-sea hydrothermal vent at the Mid-Atlantic Ridge No Access

Abstract

A coccoid-shaped, strictly anaerobic, hyperthermophilic and piezophilic organoheterotrophic archaeon, strain Iri35c, was isolated from a hydrothermal chimney rock sample collected at a depth of 2300 m at the Mid-Atlantic Ridge (Rainbow vent field). Cells of strain Iri35c grew at NaCl concentrations ranging from 1–5 % (w/v) (optimum 2.0 %), from pH 5.0 to 9.0 (optimum 7.0–7.5), at temperatures between 50 and 90 °C (optimum 75–80 °C) and at pressures from 0.1 to at least 50 MPa (optimum: 10–30 MPa). The novel isolate grew on complex organic substrates, such as yeast extract, tryptone, peptone or beef extract, preferentially in the presence of elemental sulphur or -cystine; however, these molecules were not necessary for growth. Its genomic DNA G+C content was 54.63 mol%. The genome has been annotated and the metabolic predictions are in accordance with the metabolic characteristics of the strain and of in general. Phylogenetic analyses based on 16S rRNA gene sequences and concatenated ribosomal protein sequences showed that strain Iri35c belongs to the genus and is closer to the species and . Average nucleotide identity scores and DNA–DNA hybridization values between the genome of strain Iri35c and the genomes of the type species of the genus were below the species delineation threshold. Therefore, and considering the phenotypic data presented, strain Iri35c is suggested to represent a novel species, for which the name sp. nov. is proposed, with the type strain Iri35c (=UBOCC M-2026=DSM 111003).

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): hydrothermal , hyperthermophilic , piezophilic and Thermococcus
Funding
This study was supported by the:
  • Sino-French IRP 1211 MicrobSea
    • Principle Award Recipient: KarineAlain
  • LabexMER Axis 3 programs ENDIV and CULTIVENT (Award ANR-10-LABX-1)
    • Principle Award Recipient: KarineAlain
  • Grant from the French Ministry of Higher Education and Research
    • Principle Award Recipient: CourtineDamien
  • Program MERLIN Abyss
    • Principle Award Recipient: AlainKarine
© 2021 The Authors
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004853
2021-07-08
2024-04-25
Loading full text...

Full text loading...

References

  1. Godfroy A, François D, Hartunians J, Moalic Y, Alain K. (in press). Vetriani C, Giovannelli D. eds In The Microbiology of Deep-Sea. Physiology, Metabolism and Ecology of Thermophiles from Deep-sea Vents Springer International;
     [Google Scholar]
  2. Bertoldo C, Antranikian G. The order Thermococcales. Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackerbrandt E. eds In The Prokaryotes Vol 3 New York: Springer; 2006 pp 69–81
     [Google Scholar]
  3. Kozhevnikova DA, Taranov EA, Lebedinsky AV, Bonch-Osmolovskaya EA, Sokolova TG. Hydrogenogenic and sulfidogenic growth of Thermococcus archaea on carbon monoxide and formate. Microbiology 2016; 85:400–410 [View Article]
     [Google Scholar]
  4. Sokolova TG, Jeanthon C, Kostrikina NA, Chernyh NA, Lebedinsky A et al. The first evidence of anaerobic CO oxidation coupled with H2 production by a hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent. Extremophiles 2004; 8:317–323 [View Article] [PubMed]
     [Google Scholar]
  5. Atomi H, Reeve J. Microbe Profile: Thermococcus kodakarensis: the model hyperthermophilic archaeon. Microbiol 2019; 165:1166–1168 [View Article]
     [Google Scholar]
  6. Thiel A, Michoud G, Moalic Y, Flament D, Jebbar M. Genetic manipulations of the hyperthermophilic piezophilic archaeon Thermococcus barophilus. Appl Environ Microbiol 2014; 80:2299–2306 [View Article] [PubMed]
     [Google Scholar]
  7. Atomi H, Fukui T, Kanai T, Morikawa M, Imanaka T. Description of Thermococcus kodakaraensis sp. nov., a well studied hyperthermophilic archaeon previously reported as Pyrococcus sp. Archaea 2004; 1:263–267 [View Article] [PubMed]
     [Google Scholar]
  8. González JM, Kato C, Horikoshi K. Thermococcus peptonophilus sp. nov., a fast-growing, extremely thermophilic archaebacterium isolated from deep-sea hydrothermal vents. Arch Microbiol 1995; 164:159–164 [View Article] [PubMed]
     [Google Scholar]
  9. Zhao W, Zeng X, Xiao X. Thermococcus eurythermalis sp. nov., a conditional piezophilic, hyperthermophilic archaeon with a wide temperature range for growth, isolated from an oil-immersed chimney in the Guaymas Basin. Int J Syst Evol Microbiol 2015; 65:30–35 [View Article] [PubMed]
     [Google Scholar]
  10. Jolivet E, L’Haridon S, Corre E, Forterre P, Prieur D. Thermococcus gammatolerans sp. nov., a hyperthermophilic archaeon from a deep-sea hydrothermal vent that resists ionizing radiation. Int J Syst Evol Microbiol 2003; 53:847–851 [View Article]
     [Google Scholar]
  11. Dalmasso C, Oger P, Selva G, Courtine D, L’Haridon S et al. Thermococcus piezophilus sp. nov., a novel hyperthermophilic and piezophilic archaeon with a broad pressure range for growth, isolated from a deepest hydrothermal vent at the Mid-Cayman Rise. Syst Appl Microbiol 2016; 39:440–444 [View Article]
     [Google Scholar]
  12. Marteinsson VT, Birrien JL, Reysenbach AL, Vernet M, Marie D et al. Thermococcus barophilus sp. nov., a new barophilic and hyperthermophilic archaeon isolated under high hydrostatic pressure from a deep-sea hydrothermal vent. Int J Syst Bacteriol 1999; 49:351–359
     [Google Scholar]
  13. Keller M, Braun FJ, Dirmeier R, Burggraf S, Rachel R et al. Thermococcus alcaliphilus sp. nov., a new hyperthermophilic archaeum growing on polysulfide at alkaline pH. Arch Microbiol 1995; 164:390–395 [View Article] [PubMed]
     [Google Scholar]
  14. Zeng X, Birrien JL, Fouquet Y, Cherkashov G, Jebbar M et al. Pyrococcus CH1, an obligate piezophilic hyperthermophile: extending the upper pressure–temperature limits for life. ISME J 2009; 3:873–876 [View Article] [PubMed]
     [Google Scholar]
  15. Eren AM, Vineis JH, Morrison HG, Sogin ML. A filtering method to generate high quality short reads using illumina paired-end technology. PLOS ONE 2013; 8:e66643 [View Article] [PubMed]
     [Google Scholar]
  16. Minoche AE, Dohm JC, Himmelbauer H. Evaluation of genomic high-throughput sequencing data generated on Illumina HiSeq and Genome Analyzer systems. Genome Biol 2011; 12:R112 [View Article] [PubMed]
     [Google Scholar]
  17. Vallenet D, Calteau A, Dubois M, Amours P, Bazin A et al. MicroScope: an integrated platform for the annotation and exploration of microbial gene functions through genomic, pangenomic and metabolic comparative analysis. Nucleic Acids Res 2020; 48:D589
     [Google Scholar]
  18. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M et al. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 2012; 62:716–721 [View Article] [PubMed]
     [Google Scholar]
  19. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7 improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
     [Google Scholar]
  20. Criscuolo A, Gribaldo S. BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol 2010; 10:210 [View Article] [PubMed]
     [Google Scholar]
  21. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article] [PubMed]
     [Google Scholar]
  22. Lefort V, Longueville J-E, Gascuel O. SMS: Smart Model Selection in PhyML. Mol Biol Evol 2017; 34:2422–2424 [View Article] [PubMed]
     [Google Scholar]
  23. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W259 [View Article]
     [Google Scholar]
  24. Yoon SH, Ha SM, Lim JM, Kwon SJ, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article] [PubMed]
     [Google Scholar]
  25. Richter M, Rosselló-Móra R, Glöckner FO, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 2016; 32:929–931 [View Article]
     [Google Scholar]
  26. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article] [PubMed]
     [Google Scholar]
  27. Richter M, Rossello-Mora R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009; 106:19126–19131 [View Article] [PubMed]
     [Google Scholar]
  28. Wayne LG, Stackebrandt E, Kandler O, Colwell RR, Krichevsky M et al. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 1987; 37:463–464
     [Google Scholar]
  29. Rosselló-Móra R, Whitman WB. Dialogue on the nomenclature and classification of prokaryotes. Syst Appl Microbiol 2019; 42:5–14 [View Article] [PubMed]
     [Google Scholar]
  30. Alain K, Marteinsson VT, Miroshnichenko M, Bonch-Osmolovskaya E, Prieur D et al. Marinitoga piezophila, sp. nov., a rod-shaped thermo-piezophilic bacterium isolated under high hydrostatic pressure from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 2002; 52:1331–1339 [View Article] [PubMed]
     [Google Scholar]
  31. Cord-Ruwisch R. A quick method for the determination of dissolved and precipitated sulfides in cultures of sulfate-reducing bacteria. Journal of Microbiological Methods 1985; 4:33–36 [View Article]
     [Google Scholar]
  32. Miroshnichenko ML, Gongadze GM, Rainey FA, Kostyukova AS, Lysenko AM et al. Thermococcus gorgonarius sp. nov. and Thermococcus pacificus sp. nov.: heterotrophic extremely thermophilic archaea from New Zealand submarine hot vents. Int J Syst Bacteriol 1998; 48:23–29 [View Article]
     [Google Scholar]
  33. Kengen SWM, Stams AJM. Formation of l-alanine as a reduced end product in carbohydrate fermentation by the hyperthermophilic archaeon Pyrococcus furiosus. Arch Microbiol 1994; 161:168–175 [View Article]
     [Google Scholar]
  34. Ward DE, Kengen SW, van Der Oost J, de Vos WM. Purification and characterization of the alanine aminotransferase from the hyperthermophilic archaeon Pyrococcus furiosus and its role in alanine production. J Bacteriol 2000; 182:2559–2566 [View Article] [PubMed]
     [Google Scholar]
  35. Sakuraba H, Goda S, Ohshima T. Unique sugar metabolism and novel enzymes of hyperthermophilic archaea. Chem Record 2004; 3:281–287 [View Article]
     [Google Scholar]
  36. Lipscomb GL, Schut GJ, Scott RA, Adams MWW. SurR is a master regulator of the primary electron flow pathways in the order Thermococcales. Mol Microbiol 2017; 104:869–881 [View Article] [PubMed]
     [Google Scholar]
  37. Topçuoğlu BD, Meydan C, Orellana R, Holden JF. Formate hydrogenlyase and formate secretion ameliorate H2 inhibition in the hyperthermophilic archaeon Thermococcus paralvinellae. Environ Microbiol 2018; 20:949–957 [View Article] [PubMed]
     [Google Scholar]
  38. Kuwabara T, Minaba M, Ogi N, Kamekura M. Thermococcus celericrescens sp. nov., a fast-growing and cell-fusing hyperthermophilic archaeon from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 2007; 57:437–443 [View Article] [PubMed]
     [Google Scholar]
  39. Grote R, Li L, Tamaoka J, Kato C, Horikoshi K et al. Thermococcus siculi sp. nov., a novel hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent at the Mid-Okinawa Trough. Extremophiles 1999; 3:55–62 [View Article] [PubMed]
     [Google Scholar]
  40. Hensley SA, Jung JH, Park CS, Holden JF. Thermococcus paralvinellae sp. nov. and Thermococcus cleftensis sp. nov. of hyperthermophilic heterotrophs from deep-sea hydrothermal vents. Int J Syst Evol Microbiol 2014; 64:3655–3659 [View Article] [PubMed]
     [Google Scholar]
  41. Holden JF, Takai K, Summit M, Bolton S, Zyskowski J et al. Diversity among three novel groups of hyperthermophilic deep-sea Thermococcus species from three sites in the northeastern Pacific Ocean. FEMS Microbiol Ecol 2001; 36:51–60 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004853
Loading
Thermococcus camini sp. nov., a hyperthermophilic and piezophilic archaeon isolated from a deep-sea hydrothermal vent at the Mid-Atlantic Ridge
Int J Syst Evol Microbiol 71, 004853 (2021); https://doi.org/10.1099/ijsem.0.004853
/content/journal/ijsem/10.1099/ijsem.0.004853
/content/journal/ijsem/10.1099/ijsem.0.004853
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error