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Volume 70, Issue 8

sp. nov., a novel spherical halotolerant spirochete from a Russian heavy oil reservoir, emended description of the genus , reclassification of to a new genus gen. nov. as comb. nov. and proposal of fam. nov. Free

Abstract

Anaerobic, fermentative, halotolerant bacteria, strains 4-11 and 585, were isolated from production water of two low-temperature petroleum reservoirs (Russia) and were characterized by using a polyphasic approach. Cells of the strains were spherical, non-motile and 0.30–2.5 µm in diameter. Strain 4-11 grew optimally at 35 °C, pH 6.0 and 1.0–2.0% (w/v) NaCl. Both strains grew chemoorganotrophically with mono-, di- and trisaccharides. The major cellular fatty acids of both strains were C, C, C ω9 and C 3-OH. Major polar lipids were glycolipids and phospholipids. The 16S rRNA gene sequences of the strains 4-11 and 585 had 99.9% similarity and were most closely related to the sequence of GLS2 (96.9, and 97.0% similarity, respectively). The G+C content of the genomic DNA of strains 4-11 and 585 were 46.8 and 46.9%, respectively. The average nucleotide identity and digital DNA–DNA hybridization values between the genomes of strain 4-11 and GLS2 were 73.0 and 16.9%, respectively. Results of phylogenomic metrics analysis of the genomes and 120 core proteins of strains 4-11 and 585 and their physiological and biochemical characteristics confirmed that the strains represented a novel species of the genus , for which the name sp. nov. is proposed, with the type strain 4-11 (=VKM B-3269=KCTC 15833). Based on the results of phylogenetic analysis, was reclassified as member of a new genus gen. nov., comb. nov. The genera and form a separate clade, for which a novel family, fam. nov., is proposed.

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Keyword(s): oil field , Parasphaerochaeta gen. nov. , phylogenomic analysis , polyphasic taxonomy , Sphaerochaeta halotolerans sp. nov. and Sphaerochaetaceae fam. nov.
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2020-07-22
2024-04-19
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References

  1. Paster BJ. Order I. Spirochaetales Buchanan 1917, 163. In Krieg NR, Staley JT, Brown DR, Hedlund BP, Paster BJ. (editors) Bergey's Manual of Systematic Bacteriology, 2nd ed., vol. 4. The Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyglomi, Gemmatimonadetes, Lentisphaerae, Verrumicrobia, Chlamydiae, and Planctomycetes New York: Springer-Verlag; 2011 pp 471–.473
     [Google Scholar]
  2. Paster BJ. Family I. Spirochaetaceae Swellengrebel 1907, 581AL. In Krieg NR, Staley JT, Brown DR, Hedlund BP, Paster BJ. (editors) Bergey's Manual of Systematic Bacteriology, 2nd ed., vol. 4. The Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyglomi, Gemmatimonadetes, Lentisphaerae, Verrumicrobia, Chlamydiae, and Planctomycetes New York: Springer-Verlag; 2011 p 473
     [Google Scholar]
  3. Euzeby JP. List of changes in taxonomic opinion no. 17. notification of changes in taxonomic opinion previously published outside the IJSEM. Int J Syst Evol Microbiol 2013; 63:8–9
     [Google Scholar]
  4. 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; 4:217 [View Article][PubMed]
     [Google Scholar]
  5. Abt B, Han C, Scheuner C, Lu M, Lapidus A et al. Complete genome sequence of the termite hindgut bacterium Spirochaeta coccoides type strain (SPN1(T)), reclassification in the genus Sphaerochaeta as Sphaerochaeta coccoides comb. nov. and emendations of the family Spirochaetaceae and the genus Sphaerochaeta . Stand Genomic Sci 2012; 6:194–209 [View Article][PubMed]
     [Google Scholar]
  6. Ritalahti KM, Justicia-Leon SD, Cusick KD, Ramos-Hernandez N, Rubin M et al. Sphaerochaeta globosa gen. nov., sp. nov. and Sphaerochaeta pleomorpha sp. nov., free-living, spherical spirochaetes. Int J Syst Evol Microbiol 2012; 62:210–216 [View Article][PubMed]
     [Google Scholar]
  7. Shivani Y, Subhash Y, Sasikala C, Ramana CV. Description of 'Candidatus Marispirochaeta associata' and reclassification of Spirochaeta bajacaliforniensis, Spirochaeta smaragdinae and Spirochaeta sinaica to a new genus Sediminispirochaeta gen. nov. as Sediminispirochaeta bajacaliforniensis comb. nov., Sediminispirochaeta smaragdinae comb. nov. and Sediminispirochaeta sinaica comb. nov. Int J Syst Evol Microbiol 2016; 66:5485–5492 [View Article][PubMed]
     [Google Scholar]
  8. Arroua B, Ranchou-Peyruse A, Ranchou-Peyruse M, Magot M, Urios L et al. Pleomorphochaeta caudata gen. nov., sp. nov., an anaerobic bacterium isolated from an offshore oil well, reclassification of Sphaerochaeta multiformis MO-SPC2T as Pleomorphochaeta multiformis MO-SPC2T comb. nov. as the type strain of this novel genus and emended description of the genus Sphaerochaeta . Int J Syst Evol Microbiol 2017; 67:417–424 [View Article][PubMed]
     [Google Scholar]
  9. Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W et al. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 2014; 12:635–645 [View Article][PubMed]
     [Google Scholar]
  10. Dröge S, Fröhlich J, Radek R, König H, Dröge S, Fröhlich J, König H. Spirochaeta coccoides sp. nov., a novel coccoid spirochete from the hindgut of the termite Neotermes castaneus . Appl Environ Microbiol 2006; 72:392–397 [View Article][PubMed]
     [Google Scholar]
  11. Troshina O, Oshurkova V, Suzina N, Machulin A, Ariskina E et al. Sphaerochaeta associata sp. nov., a spherical spirochaete isolated from cultures of Methanosarcina mazei JL01. Int J Syst Evol Microbiol 2015; 65:4315–4322 [View Article][PubMed]
     [Google Scholar]
  12. Miyazaki M, Sakai S, Ritalahti KM, Saito Y, Yamanaka Y et al. Sphaerochaeta multiformis sp. nov., an anaerobic, psychrophilic bacterium isolated from subseafloor sediment, and emended description of the genus Sphaerochaeta . Int J Syst Evol Microbiol 2014; 64:4147–4154 [View Article][PubMed]
     [Google Scholar]
  13. Dahle H, Garshol F, Madsen M, Birkeland N-K. Microbial community structure analysis of produced water from a high-temperature North sea oil-field. Antonie van Leeuwenhoek 2008; 93:37–49 [View Article][PubMed]
     [Google Scholar]
  14. Pham VD, Hnatow LL, Zhang S, Fallon RD, Jackson SC et al. Characterizing microbial diversity in production water from an Alaskan mesothermic petroleum reservoir with two independent molecular methods. Environ Microbiol 2009; 11:176–187 [View Article][PubMed]
     [Google Scholar]
  15. Gray ND, Sherry A, Hubert C, Dolfing J, Head IM. Methanogenic degradation of petroleum hydrocarbons in subsurface environments remediation, heavy oil formation, and energy recovery. Adv Appl Microbiol 2010; 72:137–161 [View Article][PubMed]
     [Google Scholar]
  16. Arroua B, Grimaud R, Hirschler-Réa A, Bouriat P, Magot M et al. Pleomorphochaeta naphthae sp. nov., a new anaerobic fermentative bacterium isolated from an oil field. Int J Syst Evol Microbiol 2018; 68:3747–3753 [View Article][PubMed]
     [Google Scholar]
  17. Magot M, Fardeau ML, Arnauld O, Lanau C, Ollivier B et al. Spirochaeta smaragdinae sp. nov., a new mesophilic strictly anaerobic spirochete from an oil field. FEMS Microbiol Lett 1997; 155:185–191 [View Article][PubMed]
     [Google Scholar]
  18. SKh B, DSh S, Tourova TP, Nazina TN. Bacteria of the genus Sphaerochaeta from low-temperature heavy-oil reservoirs (Russia). Microbiology 2018; 87:757–765
     [Google Scholar]
  19. Kim M, Oh H-S, Park S-C, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [View Article][PubMed]
     [Google Scholar]
  20. Nazina TN, Sokolova DS, Babich TL, Semenova EM, Ershov AP et al. Microorganisms of low-temperature heavy oil reservoirs (Russia) and their possible application for enhanced oil recovery. Microbiology 2017; 86:773–785 [View Article]
     [Google Scholar]
  21. Kevbrin VV, Zavarzin GA. The effect of sulfur compounds on growth of halophilic homoacetic bacterium Acetohalobium arabaticum . Mikrobiologiia 1992; 61:812–817
     [Google Scholar]
  22. Wolin EA, Wolin MJ, Wolfe RS. Formation of methane by bacterial extracts. J Biol Chem 1963; 238:2882–2888[PubMed]
     [Google Scholar]
  23. Ryter A, Kellenberger E. Etude Au microscope electronique de plasmas contenant de l'Acide desoxyribonucleique.. Z Naturforsch 1958; 13b:597–605
     [Google Scholar]
  24. Reynolds ES. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 1963; 17:208–212 [View Article][PubMed]
     [Google Scholar]
  25. Trueper HG, Schlegel HG. Sulphur metabolism in Thiorhodaceae. I. Quantitative measurements on growing cells of Chromatium OKENII. Antonie van Leeuwenhoek 1964; 30::321–:323 [View Article][PubMed]
     [Google Scholar]
  26. Bonch-Osmolovskaya EA, Miroshnichenko ML, Lebedinsky AV, Chernyh NA, Nazina TN et al. Radioisotopic, culture-based, and oligonucleotide microchip analyses of thermophilic microbial communities in a continental high-temperature petroleum reservoir. Appl Environ Microbiol 2003; 69:6143–6151 [View Article][PubMed]
     [Google Scholar]
  27. Minnikin DE, Collins MD, Goodfellow M. Fatty Acid and Polar Lipid Composition in the Classification of Cellulomonas, Oerskovia and Related Taxa. J Appl Bacteriol 1979; 47:87–95 [View Article]
     [Google Scholar]
  28. Minnikin DE, O'Donnell AG, Goodfellow M, Alderson G, Athalye M et al. An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 1984; 2:233–241 [View Article]
     [Google Scholar]
  29. Wilson K. Preparation of genomic DNA from bacteria. Curr Protoc Mol Biol 2001; Chapter 2:2.4.1–2.4.2 [View Article][PubMed]
     [Google Scholar]
  30. Lane DJ. 16S/23S rRNA sequencing. In Stackebrandt E, M Goodfellow. (editors) Nucleic Acid Techniques in Bacterial Systematics New York: John Wiley & Sons.; 1991 pp P. 115–.175
     [Google Scholar]
  31. Edgar RC. Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article][PubMed]
     [Google Scholar]
  32. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 2017; 14:587–589 [View Article][PubMed]
     [Google Scholar]
  33. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article][PubMed]
     [Google Scholar]
  34. 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]
  35. 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; 11:468 [View Article][PubMed]
     [Google Scholar]
  36. 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]
  37. Grouzdev DS, Bidzhieva SK, Sokolova DS, Tourova TP, Patutina EO et al. DraftGenome Sequence of a Fermenting Bacterium, "Sphaerochaeta halotolerans" 4-11T, from a Low-Temperature Petroleum Reservoir in Russia. Microbiol Resour Announc 2018; 7:e01345–18 [View Article][PubMed]
     [Google Scholar]
  38. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article][PubMed]
     [Google Scholar]
  39. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article][PubMed]
     [Google Scholar]
  40. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article][PubMed]
     [Google Scholar]
  41. Varghese NJ, Mukherjee S, Ivanova N, Konstantinidis KT, Mavrommatis K et al. Microbial species delineation using whole genome sequences. Nucleic Acids Res 2015; 43:6761–6771 [View Article][PubMed]
     [Google Scholar]
  42. 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]
  43. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009; 10:421 [View Article][PubMed]
     [Google Scholar]
  44. Barco RA, Garrity GM, Scott JJ, Amend JP, Nealson KH et al. A Genus Definition for Bacteria and Archaea Based on a Standard Genome Relatedness Index. mBio 2020; 11:e02475–19 [View Article][PubMed]
     [Google Scholar]
  45. Chaudhari NM, Gupta VK, Dutta C. BPGA- an ultra-fast pan-genome analysis pipeline. Sci Rep 2016; 6:24373 [View Article][PubMed]
     [Google Scholar]
  46. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010; 26:2460–2461 [View Article][PubMed]
     [Google Scholar]
  47. Kraegeloh A, Amendt B, Kunte HJ. Potassium transport in a halophilic member of the bacteria domain: identification and characterization of the K+ uptake systems TrkH and TrkI from Halomonas elongata DSM 2581T. J Bacteriol 2005; 187:1036–1043 [View Article][PubMed]
     [Google Scholar]
  48. Holtmann G, Bremer E. Thermoprotection of Bacillus subtilis by exogenously provided glycine betaine and structurally related compatible solutes: involvement of Opu transporters. J Bacteriol 2004; 186:1683–1693 [View Article][PubMed]
     [Google Scholar]
  49. Ueki A, Goto K, Ohtaki Y, Kaku N, Ueki K. Description of Anaerotignum aminivorans gen. nov., sp. nov., a strictly anaerobic, amino-acid-decomposing bacterium isolated from a methanogenic reactor, and reclassification of Clostridium propionicum, Clostridium neopropionicum and Clostridium lactatifermentans as species of the genus Anaerotignum . Int J Syst Evol Microbiol 2017; 67:4146–4153 [View Article][PubMed]
     [Google Scholar]
  50. Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the genome taxonomy database. Bioinformatics 2019btz848 [View Article][PubMed]
     [Google Scholar]
  51. Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 2018; 35:518–522 [View Article][PubMed]
     [Google Scholar]
  52. Pantiukh K, Grouzdev D. POCP-Matrix calculation for a number of genomes. FigShare 2017
     [Google Scholar]
  53. Grouzdev DS, Rysina MS, Bryantseva IA, Gorlenko VM, Gaisin VA. Draft genome sequences of 'Candidatus Chloroploca asiatica' and 'Candidatus Viridilinea mediisalina', candidate representatives of the Chloroflexales order: phylogenetic and taxonomic implications. Stand Genomic Sci 2018; 13:24 [View Article][PubMed]
     [Google Scholar]
  54. 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]
  55. Konstantinidis KT, Rosselló-Móra R, Amann R. Uncultivated microbes in need of their own taxonomy. Isme J 2017; 11:2399–2406 [View Article][PubMed]
     [Google Scholar]
  56. Orata FD, Meier-Kolthoff JP, Sauvageau D, Stein LY. Phylogenomic Analysis of the Gammaproteobacterial Methanotrophs (Order Methylococcales) Calls for the Reclassification of Members at the Genus and Species Levels. Front Microbiol 2018; 9:3162 [View Article][PubMed]
     [Google Scholar]
  57. Koziaeva V, Dziuba M, Leão P, Uzun M, Krutkina M et al. Genome-Based Metabolic Reconstruction of a Novel Uncultivated Freshwater Magnetotactic coccus "Ca. Magnetaquicoccus inordinatus" UR-1, and Proposal of a Candidate Family "Ca. Magnetaquicoccaceae". Front Microbiol 2019; 10:2290 [View Article][PubMed]
     [Google Scholar]
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Sphaerochaeta halotolerans sp. nov., a novel spherical halotolerant spirochete from a Russian heavy oil reservoir, emended description of the genus Sphaerochaeta, reclassification of Sphaerochaeta coccoides to a new genus Parasphaerochaeta gen. nov. as Parasphaerochaeta coccoides comb. nov. and proposal of Sphaerochaetaceae fam. nov.
Int J Syst Evol Microbiol 70, 4748 (2020); https://doi.org/10.1099/ijsem.0.004340
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