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Volume 73, Issue 1

gen. nov., sp. nov., a novel thermophilic spirochete isolated from a Tunisian hot spring, and description of the novel family . No Access

Abstract

A novel thermophilic, anaerobic bacterium, strain F1F22, was isolated from hot spring water collected in northern Tunisia. The cells were non-motile, Gram-negative and helical with hooked ends, 0.5×10–32 µm in size. Growth of the strain was observed at 45–70 °C (optimum, 55 °C), in 0.0–1.0 % (w/v) NaCl (optimum without NaCl) and at pH 6.5–8.5 (optimum, pH 7.5). Yeast extract was required for growth, and the strain grew on glucose, sucrose and maltose. The major fatty acids were C (40.2 %), iso-C (30.2 %) and C DMA (14.5 %). The genome consisted of a circular chromosome (2.5 Mb) containing 2672 predicted protein-encoding genes with a G+C content of 43.15 mol %. Based on a comparative 16S rRNA gene sequence analysis, strain F1F22 formed a deeply branching lineage within the phylum , class , order , and had only low sequence similarity to other species of the phylum (lower than 83 %). Genome-based analysis of average nucleotide identity and digital DNA–DNA hybridization of strain F1F22 with DSM 7334, ATCC 43811 and DSM 6578 showed values between 63.26 and 63.52 %, and between 20 and 25 %. Hence, we propose strain F1F22 as a representative of a novel family ( fam. nov.), genus and species of : gen. nov., sp. nov. (type strain F1F22=JCM 31314=DSM 101182).

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Keyword(s): hot spring , novel family , novel genus , thermophilic spirochaetota and Thermospira
© 2023 The Authors
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/content/journal/ijsem/10.1099/ijsem.0.005690
2023-01-25
2024-04-24
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References

  1. Seshadri R, Myers GSA, Tettelin H, Eisen JA, Heidelberg JF et al. Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes. Proc Natl Acad Sci U S A 2004; 101:5646–5651 [View Article] [PubMed]
     [Google Scholar]
  2. Paster BJ. Phylum XV Spirochaetota. In Brenner DJ, Krieg NR, Garrity GM, Staley JT. eds Bergey’s Manual of Systematic Bacteriology New York: Springer; 2011 p 471
     [Google Scholar]
  3. Campbell BJ, Cary SC. Characterization of a novel spirochete associated with the hydrothermal vent polychaete annelid, Alvinella pompejana. Appl Environ Microbiol 2001; 67:110–117 [View Article] [PubMed]
     [Google Scholar]
  4. Inagaki F, Kuypers MMM, Tsunogai U, Ishibashi J-I, Nakamura K-I et al. Microbial community in a sediment-hosted CO2 lake of the southern Okinawa trough hydrothermal system. Proc Natl Acad Sci U S A 2006; 103:14164–14169 [View Article]
     [Google Scholar]
  5. Gupta RS, Mahmood S, Adeolu M. A phylogenomic and molecular signature based approach for characterization of the phylum Spirochaetes and its major clades: proposal for a taxonomic revision of the phylum. Front Microbiol 2013; 4:1–18 [View Article]
     [Google Scholar]
  6. Hördt A, López MG, Meier-Kolthoff JP, Schleuning M, Weinhold L-M et al. Analysis of 1,000+ type-strain genomes substantially improves taxonomic classification of Alphaproteobacteria. Front Microbiol 2020; 11:1–112 [View Article]
     [Google Scholar]
  7. Meier-Kolthoff JP, Carbasse JS, Peinado-Olarte RL, Göker M. TYGS and LPSN: a database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Research 2022; 50:D801–D807 [View Article]
     [Google Scholar]
  8. Momper L, Semler A, Lu GS, Miyazaki M, Imachi H et al. Rectinema subterraneum sp. nov, a chemotrophic spirochaete isolated from the deep terrestrial subsurface. Int J Syst Evol Microbiol 2020; 70:4739–4747 [View Article] [PubMed]
     [Google Scholar]
  9. Koelschbach JS, Mouttaki H, Pickl C, Heipieper HJ, Rachel R et al. Rectinema cohabitans gen. nov., sp. nov., a rod-shaped spirochaete isolated from an anaerobic naphthalene-degrading enrichment culture. Int J Syst Evol Microbiol 2017; 67:1288–1295
     [Google Scholar]
  10. Patel BKC, Morgan HW, Daniel RM. Thermophilic anaerobic spirochetes in New Zealand hot springs. FEMS Microbiol Lett 1985; 26:101–106 [View Article]
     [Google Scholar]
  11. Aksenova HY, Rainey FA, Janssen PH, Zavarzin GA, Morgan HW. Spirochaeta thermophila sp. nov., an obligately anaerobic, polysaccharolytic, extremely thermophilic bacterium. International Journal of Systematic Bacteriology 1992; 42:175–177 [View Article]
     [Google Scholar]
  12. Pohlschroeder M, Leschine SB, Canale-Parola E. Spirochaeta caldaria sp. nov., a thermophilic bacterium that enhances cellulose degradation by Clostridium thermocellum. Arch Microbiol 1994; 161:17–24 [View Article]
     [Google Scholar]
  13. Imachi H, Sakai S, Hirayama H, Nakagawa S, Nunoura T et al. Exilispira thermophila gen. nov., sp. nov., an anaerobic, thermophilic spirochaete isolated from a deep-sea hydrothermal vent chimney. Int J Syst Evol Microbiol 2008; 58:2258–2265 [View Article] [PubMed]
     [Google Scholar]
  14. Karnachuk OV, Lukina AP, Kadnikov VV, Sherbakova VA, Beletsky AV et al. Targeted isolation based on metagenome-assembled genomes reveals a phylogenetically distinct group of thermophilic spirochetes from deep biosphere. Environ Microbiol 2021; 23:3585–3598 [View Article] [PubMed]
     [Google Scholar]
  15. Mechichi T, Labat M, Garcia JL, Thomas P, Patel BKC. Sporobacterium olearium gen. nov. sp. nov., a new aromatic compounds degrading, methanethiol-producing bacterium from an olive mill wastewater treatment digester. Int J Syst Bacteriol 1999; 49:1741–1748
     [Google Scholar]
  16. Hungate RE. A roll tube method for the cultivation of strict anaerobes. Meth Microbiol 1969; 3B:117–132
     [Google Scholar]
  17. Macy JM, Snellen JE, Hungate RE. Use of syringe methods for anaerobiosis. Am J Clin Nutr 1972; 25:1318–1323 [View Article] [PubMed]
     [Google Scholar]
  18. Miller TL, Wolin MJ. A serum bottle modification of the Hungate technique for cultivating obligate anaerobes. Appl Microbiol 1974; 27:985–987 [View Article] [PubMed]
     [Google Scholar]
  19. Widdel F, Pfennig N. Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids. Isolation of new sulfate-reducing bacteria enriched with acetate from saline environments. Description of Desulfobacter postgatei gen. nov., sp. nov. Arch Microbiol 1981; 129:
     [Google Scholar]
  20. Gam ZBA, Daumas S, Casalot L, Bartoli-Joseph M, Necib S et al. Thermanaeromonas burensis sp. nov., a thermophilic anaerobe isolated from a subterranean clay environment. Int J Syst Evol Microbiol 2016; 66:445–449 [View Article] [PubMed]
     [Google Scholar]
  21. 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; 10:1497 [View Article]
     [Google Scholar]
  22. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 1999; 41:95–98
     [Google Scholar]
  23. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article] [PubMed]
     [Google Scholar]
  24. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article] [PubMed]
     [Google Scholar]
  25. Jukes TH, Cantor CR. Evolution of protein molecules. Munro HN. Mammalian Protein Metabolism New York: Academic press; 196921–132
     [Google Scholar]
  26. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article] [PubMed]
     [Google Scholar]
  27. Fitch WM. Toward defining the course of evolution: minimum change for a specific tree topology. Systematic Zoology 1971; 20:406 [View Article]
     [Google Scholar]
  28. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article] [PubMed]
     [Google Scholar]
  29. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLOS Comput Biol 2017; 13:1005595–22 [View Article]
     [Google Scholar]
  30. 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:D579–D589 [View Article] [PubMed]
     [Google Scholar]
  31. Chen I-MA, Chu K, Palaniappan K, Pillay M, Ratner A et al. IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes. Nucleic Acids Res 2019; 47:D666–D677 [View Article] [PubMed]
     [Google Scholar]
  32. 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 Commun 2021; 1:1–16 [View Article]
     [Google Scholar]
  33. Lee I, Ouk Kim Y, Park S-C, Chun J. OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 2016; 66:1100–1103 [View Article] [PubMed]
     [Google Scholar]
  34. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article] [PubMed]
     [Google Scholar]
  35. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newsletter 1990; 20:1–6
     [Google Scholar]
  36. 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]
  37. Kuykendall LD, Roy MA, O’neill JJ, Devine TE. Fatty acids, antibiotic resistance, and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum. International Journal of Systematic Bacteriology 1988; 38:358–361 [View Article]
     [Google Scholar]
  38. Defosse DL, Johnson RC, Paster BJ, Dewhirst FE, Fraser GJ. Brevinema andersonii gen. nov., sp. nov., an infectious spirochete isolated from the short-tailed shrew (Blarina brevicauda) and the white-footed mouse (Peromyscus leucopus). Int J Syst Bacteriol 1995; 45:78–84
     [Google Scholar]
  39. Qin Q-L, Xie B-B, Zhang X-Y, Chen X-L, Zhou B-C et al. A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 2014; 196:2210–2215 [View Article] [PubMed]
     [Google Scholar]
  40. 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]
  41. Drula E, Garron M-L, Dogan S, Lombard V, Henrissat B et al. The carbohydrate-active enzyme database: functions and literature. Nucleic Acids Res 2022; 50:D571–D577 [View Article] [PubMed]
     [Google Scholar]
  42. Pitson SM, Mendz GL, Srinivasan S, Hazell SL. The tricarboxylic acid cycle of Helicobacter pylori. Eur J Biochem 1999; 260:258–267 [View Article] [PubMed]
     [Google Scholar]
  43. Hughes NJ, Clayton CL, Chalk PA, Kelly DJ. Helicobacter pylori porCDAB and oorDABC genes encode distinct pyruvate:flavodoxin and 2-oxoglutarate:acceptor oxidoreductases which mediate electron transport to NADP. J Bacteriol 1998; 180:1119–1128 [View Article] [PubMed]
     [Google Scholar]
  44. Müller V, Biegel E. Electron transport in strict anaerobes. In Encyclopedia of Biophysics 2013 pp 633–640
     [Google Scholar]
  45. Buckel W, Thauer RK. Flavin-based electron bifurcation, ferredoxin, flavodoxin, and anaerobic respiration with protons (Ech) or NAD+ (Rnf) as electron acceptors: a historical review. Front Microbiol 2018; 9:401 [View Article]
     [Google Scholar]
  46. Hirata T, Nakamura N, Omote H, Wada Y, Futai M. Regulation and reversibility of vacuolar H(+)-ATPase. J Biol Chem 2000; 275:386–389 [View Article] [PubMed]
     [Google Scholar]
  47. Adler B, Faine S. The genus Leptospira. Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E. The Prokaryotes New York: Springer; 2006294–317
     [Google Scholar]
  48. Faine S. Genus I. Leptospira. Krieg NR, Holt JG. Bergey’s Manual of Systematic Bacteriology Baltimore: Williams & Wilkins; 198462–67
     [Google Scholar]
  49. Schrank K, Choi BK, Grund S, Moter A, Heuner K et al. Treponema brennaborense sp. nov., a novel spirochaete isolated from a dairy cow suffering from digital dermatitis. Int J Syst Bacteriol 1999; 49 Pt 1:43–50 [View Article] [PubMed]
     [Google Scholar]
  50. Ben Hania W, Joseph M, Schumann P, Bunk B, Fiebig A et al. Complete genome sequence and description of Salinispira pacifica gen. nov., sp. nov., a novel spirochaete isolated form a hypersaline microbial mat. Stand Genomic Sci 2015; 10:1–14 [View Article] [PubMed]
     [Google Scholar]
  51. Zhilina TN, Zavarzin GA, Rainey F, Kevbrin VV, Kostrikina NA et al. Spirochaeta alkalica sp. nov., Spirochaeta africana sp. nov., and Spirochaeta asiatica sp. nov., alkaliphilic anaerobes from the Continental Soda Lakes in Central Asia and the East African Rift. Int J Syst Bacteriol 1996; 46:305–312 [View Article] [PubMed]
     [Google Scholar]
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Thermospira aquatica gen. nov., sp. nov., a novel thermophilic spirochete isolated from a Tunisian hot spring, and description of the novel family Thermospiraceae.
Int J Syst Evol Microbiol 73, 005690 (2023); https://doi.org/10.1099/ijsem.0.005690
/content/journal/ijsem/10.1099/ijsem.0.005690
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