1887

Abstract

A novel thermophilic strain, designated BP5-C20A, was isolated from the shallow hydrothermal field of the Panarea island in the Aeolian archipelago close to Sicily, Italy. Cells are motile rods surrounded with a ‘toga’, Gram-stain-negative and display a straight to curved morphology during the exponential phase. Strain BP5-C20A is thermophilic (optimum 55 °C), moderately acidophilic (optimum pH 5.6) and halotolerant (optimum 25 g l NaCl). It can use yeast extract, peptone and tryptone. It uses the following carbohydrates: cellobiose, fructose, glucose, maltose, starch, sucrose and xylan. Elemental sulphur is used as an electron acceptor and reduced to hydrogen sulphide. The predominant cellular fatty acid is C. Phylogenetic analysis showed that strain BP5-C20A shared 97.3 % 16S rRNA gene sequence identity with the closest related species LG1. The complete genome of strain BP5-C20A is 2.44 Mb in size with a G+C content of 27.3 mol%. The dDDH and ANI values between the genomes of strains BP5-C20A and LG1 are 31.0 and 85.70% respectively. Finally, from its physiological, metabolic and genomic characteristics, strain BP5-C20A (=DSM 112332=JCM 39183 ) is proposed as representative of a novel species of the genus named sp. nov. and belonging to the order , in the phylum .

Funding
This study was supported by the:
  • CNRS (Award X-life - Unknown branches of life)
    • Principle Award Recipient: ErausoGaël
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.006186
2023-11-28
2024-05-07
Loading full text...

Full text loading...

References

  1. Oren A, Garrity GM. Valid publication of the names of forty-two phyla of prokaryotes. Int J Syst Evol Microbiol 2021; 71:10 [View Article] [PubMed]
    [Google Scholar]
  2. Reysenbach AL, Boone DR, Castenholz RW, Garrity GM. Phylum BII. Thermotogae phy. nov. In Boone DR, Castenholz RW. eds Bergey’s Manual of Systematic Bacteriology New York: Springer-Verlag; 2001 pp 369–387 [View Article]
    [Google Scholar]
  3. Whitman WB, Oren A, Chuvochina M, da Costa MS, Garrity GM et al. Proposal of the suffix –ota to denote phyla. Addendum to ‘Proposal to include the rank of phylum in the International Code of Nomenclature of Prokaryotes'. Int J Syst Evol Microbiol 2018; 68:967–969 [View Article] [PubMed]
    [Google Scholar]
  4. Bhandari V, Gupta RS. Molecular signatures for the phylum (class) Thermotogae and a proposal for its division into three orders (Thermotogales, Kosmotogales ord. nov. and Petrotogales ord. nov.) containing four families (Thermotogaceae, Fervidobacteriaceae fam. nov., Kosmotogaceae fam. nov. and Petrotogaceae fam. nov.) and a new genus Pseudothermotoga gen. nov. with five new combinations. Antonie van Leeuwenhoek 2014; 105:143–168 [View Article] [PubMed]
    [Google Scholar]
  5. Mori K, Sakurai K, Hosoyama A, Kakegawa T, Hanada S. Vestiges of adaptation to the mesophilic environment in the genome of Tepiditoga spiralis gen. nov., sp. nov. Microb Environ 2020; 35:n [View Article] [PubMed]
    [Google Scholar]
  6. Postec A, Ciobanu M, Birrien J-L, Bienvenu N, Prieur D et al. Marinitoga litoralis sp. nov., a thermophilic, heterotrophic bacterium isolated from a coastal thermal spring on Île Saint-Paul, Southern Indian Ocean. Int J Syst Evol Microbiol 2010; 60:1778–1782 [View Article] [PubMed]
    [Google Scholar]
  7. Steinsbu BO, Røyseth V, Thorseth IH, Steen IH. Marinitoga arctica sp. nov., a thermophilic, anaerobic heterotroph isolated from a Mid-Ocean ridge vent field. Int J Syst Evol Microbiol 2016; 66:5070–5076 [View Article] [PubMed]
    [Google Scholar]
  8. L’Haridon S, Gouhier L, John Es, Reysenbach A-L. Marinitoga lauensis sp. nov., a novel deep-sea hydrothermal vent thermophilic anaerobic heterotroph with a prophage. Syst Appl Microbiol 2019; 42:343–347 [View Article]
    [Google Scholar]
  9. Postec A, Breton CL, Fardeau M-L, Lesongeur F, Pignet P et al. Marinitoga hydrogenitolerans sp. nov., a novel member of the order Thermotogales isolated from a black smoker chimney on the Mid-Atlantic Ridge. Int J Syst Evol Microbiol 2005; 55:1217–1221 [View Article] [PubMed]
    [Google Scholar]
  10. Wery N, Lesongeur F, Pignet P, Derennes V, Cambon-Bonavita MA et al. Marinitoga camini gen. nov., sp. nov., a rod-shaped bacterium belonging to the order Thermotogales, isolated from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 2001; 51:495–504 [View Article] [PubMed]
    [Google Scholar]
  11. Nunoura T, Oida H, Miyazaki M, Suzuki Y, Takai K et al. Marinitoga okinawensis sp. nov., a novel thermophilic and anaerobic heterotroph isolated from a deep-sea hydrothermal field, Southern Okinawa Trough. Int J Syst Evol Microbiol 2007; 57:467–471 [View Article] [PubMed]
    [Google Scholar]
  12. Alain K, Marteinsson VT, Miroshnichenko ML, Bonch-Osmolovskaya EA, 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]
  13. Huber R, Langworthy TA, Konig H, Thomm M, Woese CR et al. Thermotoga maritima sp. nov. represents a new genus of unique extremely thermophilic eubacteria growing up to 90°C. Arch Microbiol 1986; 144:324–333 [View Article]
    [Google Scholar]
  14. Price RE, LaRowe DE, Italiano F, Savov I, Pichler T et al. Subsurface hydrothermal processes and the bioenergetics of chemolithoautotrophy at the shallow-sea vents off Panarea Island (Italy). Chem Geol 2015; 407–408:21–45 [View Article]
    [Google Scholar]
  15. Price RE. A review of the geochemistry and microbiology of shallow-sea hydrothermal vents. In Reference Module in Earth Systems and Environmental Sciences Elsevier; 2017
    [Google Scholar]
  16. Widdel F, Kohring GW, Mayer F. Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids III. characterization of the filamentous gliding Desulfonema limicola gen. nov., and Desulfonema magnum sp. nov. Arch Microbiol 1983; 134:286–294 [View Article]
    [Google Scholar]
  17. Hungate RE. A roll tube method for the cultivation of strict anaerobes. In Norris JR, Ribbons DW. eds Meth Microbiol London: Academic Press; 1969 pp 117–132
    [Google Scholar]
  18. Quéméneur M, Erauso G, Frouin E, Zeghal E, Vandecasteele C et al. Hydrostatic pressure helps to cultivate an original anaerobic bacterium from the atlantis massif subseafloor (IODP Expedition 357): Petrocella atlantisensis gen. nov. sp. nov. Front Microbiol 2019; 10: [View Article] [PubMed]
    [Google Scholar]
  19. Lane DJ. 16S/23S rRNA sequencing. In Stackebrandt E, Goodfellow M. eds Nucleic Acid Techniques in Bacterial Systematics New York: John Wiley and Sons; 1991 pp 115–175
    [Google Scholar]
  20. Bes M, Merrouch M, Joseph M, Quéméneur M, Payri C et al. Acetoanaerobium pronyense sp. nov., an anaerobic alkaliphilic bacterium isolated from a carbonate chimney of the Prony Hydrothermal Field (New Caledonia). Int J Syst Evol Microbiol 2015; 65:2574–2580 [View Article]
    [Google Scholar]
  21. Zhang Z, Schwartz S, Wagner L, Miller W. A greedy algorithm for aligning DNA sequences. J Comput Biol 2000; 7:203–214 [View Article] [PubMed]
    [Google Scholar]
  22. Kumar S, Stecher G, Li M, Knyaz C, Tamura K et al. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article] [PubMed]
    [Google Scholar]
  23. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 2004; 32:1792–1797 [View Article] [PubMed]
    [Google Scholar]
  24. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article] [PubMed]
    [Google Scholar]
  25. Rzhetsky A, Nei M. Statistical properties of the ordinary least-squares, generalized least-squares, and minimum-evolution methods of phylogenetic inference. J Mol Evol 1992; 35:367–375 [View Article] [PubMed]
    [Google Scholar]
  26. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425
    [Google Scholar]
  27. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980; 16:111–120 [View Article] [PubMed]
    [Google Scholar]
  28. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article] [PubMed]
    [Google Scholar]
  29. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617 [View Article] [PubMed]
    [Google Scholar]
  30. Parte AC, Sardà Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M. List of Prokaryotic names with Standing in Nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 2020; 70:5607–5612 [View Article] [PubMed]
    [Google Scholar]
  31. Wick RR, Judd LM, Gorrie CL, Holt KE, Phillippy AM. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
    [Google Scholar]
  32. 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. Nucl Acids Res 2019; 48:D579–D589 [View Article] [PubMed]
    [Google Scholar]
  33. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10: [View Article] [PubMed]
    [Google Scholar]
  34. Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH et al. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol 2016; 17: [View Article] [PubMed]
    [Google Scholar]
  35. Lefort V, Desper R, Gascuel O. FastME 2.0: a comprehensive, accurate, and fast distance-based phylogeny inference program: Table 1. Mol Biol Evol 2015; 32:2798–2800 [View Article] [PubMed]
    [Google Scholar]
  36. Farris JS. Estimating phylogenetic trees from distance matrices. Am Nat 1972; 106:645–668 [View Article]
    [Google Scholar]
  37. 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: [View Article] [PubMed]
    [Google Scholar]
  38. Hitch TCA, Riedel T, Oren A, Overmann J, Lawley TD et al. Automated analysis of genomic sequences facilitates high-throughput and comprehensive description of bacteria. ISME Com 2021; 1: [View Article] [PubMed]
    [Google Scholar]
  39. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article] [PubMed]
    [Google Scholar]
  40. Kuhns M, Trifunović D, Huber H, Müller V. The Rnf complex is a NA. Commun Biol 2020; 3:431 [View Article]
    [Google Scholar]
  41. Perzov N, Padler-Karavani V, Nelson H, Nelson N. Features of V‐ATPases that distinguish them from F‐ATPases. FEBS Letters 2001; 504:223–228 [View Article] [PubMed]
    [Google Scholar]
  42. Kuykendall LD, Roy MA, O’neill JJ, Devine TE. Fatty acids, antibiotic resistance, and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum. Int J Syst Bacteriol 1988; 38:358–361 [View Article]
    [Google Scholar]
  43. Miller LT. Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxy acids. J Clin Microbiol 1982; 16:584–586 [View Article] [PubMed]
    [Google Scholar]
  44. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. In MIDI Technical Note vol 101 Newark, DE, USA: Microbial ID, Inc; 1990
    [Google Scholar]
  45. Cord-Ruwisch R. A quick method for the determination of dissolved and precipitated sulfides in cultures of sulfate-reducing bacteria. J Microbiol Methods 1985; 4:33–36 [View Article]
    [Google Scholar]
  46. L’Haridon S, Gouhier L, John ES, Reysenbach A-L. Marinitoga lauensis sp. nov., a novel deep-sea hydrothermal vent thermophilic anaerobic heterotroph with a prophage. Syst Appl Microbiol 2019; 42:343–347 [View Article]
    [Google Scholar]
  47. Mercier C, Lossouarn J, Haverkamp T, Bienvenu N, Godfroy A et al. Draft genome sequences of two Marinitoga camini isolates producing bacterioviruses. Genome Announc 2016; 4:e01261–01216 [View Article] [PubMed]
    [Google Scholar]
  48. Lucas S, Han J, Lapidus A, Cheng J-F, Goodwin LA et al. Complete genome sequence of the thermophilic, piezophilic, heterotrophic bacterium Marinitoga piezophila KA3. J Bacteriol 2012; 194:5974–5975 [View Article] [PubMed]
    [Google Scholar]
  49. Yoon S-H, Ha S, Lim J, Kwon S, 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]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.006186
Loading
/content/journal/ijsem/10.1099/ijsem.0.006186
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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