1887

Abstract

A Gram-stain-negative, rod-shaped, chemoorganotrophic and anaerobic bacterium, strain SK-G1, was isolated from oily sludge sampled at the Shengli oilfield in PR China. Growth occurred with 0–30 g l NaCl, at 40–65 °C and at pH 6.0–8.5. The predominant fatty acids were C and C, and the major cellular polar lipids were phosphatidylglycerol and phosphatidylethanolamine. No respiratory quinone was detected. The genomic G+C content was 43.9 mol%. The strain had highest 16S rRNA gene sequence similarity (93.2 % identity) to DSM 15584. The phylogenetic, phenotypic and chemotaxonomic data showed that strain SK-G1 (=CCAM 530=KCTC 15783=JCM 33158) represents a novel species of a new genus gen. nov., sp. nov. The results of phylogenetic and phylogenomic analyses indicated that the genera , , , , , and formed a clade with high bootstrap support distinguishing to other taxon within the order Thermoanaerobacterales. This clade is proposed as ord. nov. and includes fam. nov. and fam. nov. Emended descriptions of the order and family are also provided.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.003701
2019-12-01
2020-11-28
Loading full text...

Full text loading...

References

  1. Ludwig W, Schleifer K-H, Whitman WB. Revised road map to the phylum Firmicutes. In De Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W et al. (editors) Bergey’s Manual® of Systematic Bacteriology New York, NY: Springer New York: Volume Three The Firmicutes; 2009; pp.1–13
    [Google Scholar]
  2. Lauber CL, Hamady M, Knight R, Fierer N. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 2009;75:5111–5120 [CrossRef][PubMed]
    [Google Scholar]
  3. Hubert C, Loy A, Nickel M, Arnosti C, Baranyi C et al. A constant flux of diverse thermophilic bacteria into the cold Arctic seabed. Science 2009;325:1541–1544 [CrossRef][PubMed]
    [Google Scholar]
  4. Gittel A, Sørensen KB, Skovhus TL, Ingvorsen K, Schramm A. Prokaryotic community structure and sulfate reducer activity in water from high-temperature oil reservoirs with and without nitrate treatment. Appl Environ Microbiol 2009;75:7086–7096 [CrossRef][PubMed]
    [Google Scholar]
  5. Sundberg C, Al-Soud WA, Larsson M, Alm E, Yekta SS et al. 454 pyrosequencing analyses of bacterial and archaeal richness in 21 full-scale biogas digesters. FEMS Microbiol Ecol 2013;85:612–626 [CrossRef][PubMed]
    [Google Scholar]
  6. Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ et al. Metagenomic analysis of the human distal gut microbiome. Science 2006;312:1355–1359 [CrossRef][PubMed]
    [Google Scholar]
  7. Wrighton KC, Agbo P, Warnecke F, Weber KA, Brodie EL et al. A novel ecological role of the Firmicutes identified in thermophilic microbial fuel cells. Isme J 2008;2:1146–1156 [CrossRef][PubMed]
    [Google Scholar]
  8. Zhang W, Lu Z. Phylogenomic evaluation of members above the species level within the phylum Firmicutes based on conserved proteins. Environ Microbiol Rep 2015;7:273–281 [CrossRef][PubMed]
    [Google Scholar]
  9. Yutin N, Galperin MY. A genomic update on clostridial phylogeny: Gram-negative spore formers and other misplaced clostridia. Environ Microbiol 2013;15:2631–2641 [CrossRef][PubMed]
    [Google Scholar]
  10. Pavan ME, Pavan EE, Glaeser SP, Etchebehere C, Kämpfer P et al. Proposal for a new classification of a deep branching bacterial phylogenetic lineage: transfer of Coprothermobacter proteolyticus and Coprothermobacter platensis to Coprothermobacteraceae fam. nov., within Coprothermobacterales ord. nov., Coprothermobacteria classis nov. and Coprothermobacterota phyl. nov. and emended description of the family Thermodesulfobiaceae. Int J Syst Evol Microbiol 2018;68:1627–1632 [CrossRef][PubMed]
    [Google Scholar]
  11. Watanabe M, Kojima H, Fukui M. Limnochorda pilosa gen. nov., sp. nov., a moderately thermophilic, facultatively anaerobic, pleomorphic bacterium and proposal of Limnochordaceae fam. nov., Limnochordales ord. nov. and Limnochordia classis nov. in the phylum Firmicutes. Int J Syst Evol Microbiol 2015;65:2378–2384 [CrossRef][PubMed]
    [Google Scholar]
  12. Marchandin H, Teyssier C, Campos J, Jean-Pierre H, Roger F et al. Negativicoccus succinicivorans gen. nov., sp. nov., isolated from human clinical samples, emended description of the family Veillonellaceae and description of Negativicutes classis nov., Selenomonadales ord. nov. and Acidaminococcaceae fam. nov. in the bacterial phylum Firmicutes. Int J Syst Evol Microbiol 2010;60:1271–1279 [CrossRef][PubMed]
    [Google Scholar]
  13. Sokolova T, Hanel J, Onyenwoke RU, Reysenbach AL, Banta A et al. Novel chemolithotrophic, thermophilic, anaerobic bacteria Thermolithobacter ferrireducens gen. nov., sp. nov. and Thermolithobacter carboxydivorans sp. nov. Extremophiles 2007;11:145–157 [CrossRef][PubMed]
    [Google Scholar]
  14. Alauzet C, Marchandin H, Courtin P, Mory F, Lemée L et al. Multilocus analysis reveals diversity in the genus Tissierella: description of Tissierella carlieri sp. nov. in the new class Tissierellia classis nov. Syst Appl Microbiol 2014;37:23–34 [CrossRef][PubMed]
    [Google Scholar]
  15. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 2018;36:996–1004 [CrossRef][PubMed]
    [Google Scholar]
  16. Cheng L, He Q, Ding C, Dai LR, Li Q et al. Novel bacterial groups dominate in a thermophilic methanogenic hexadecane-degrading consortium. FEMS Microbiol Ecol 2013;85:568–577 [CrossRef][PubMed]
    [Google Scholar]
  17. Widdel F, Boetius A, Rabus R. Anaerobic biodegradation of hydrocarbons including methane. In Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E et al. The Prokaryotes: Ecophysiology and Biochemistry New York: Springer; 2006; pp.1028–1049
    [Google Scholar]
  18. Cheng L, Dai L, Li X, Zhang H, Lu Y. Isolation and characterization of Methanothermobacter crinale sp. nov., a novel hydrogenotrophic methanogen from the Shengli oil field. Appl Environ Microbiol 2011;77:5212–5219 [CrossRef][PubMed]
    [Google Scholar]
  19. Lane D. 16S/23S rRNA Sequencing. In Stackebrandt E, Goodfellow M. (editors) Development and Application of Nucleic Acid Probes New York: John Wiley & Son Ltd; 1991; pp.115–175
    [Google Scholar]
  20. Feng Y, Cheng L, Zhang X, Li X, Deng Y et al. Thermococcoides shengliensis gen. nov., sp. nov., a new member of the order Thermotogales isolated from oil-production fluid. Int J Syst Evol Microbiol 2010;60:932–937 [CrossRef][PubMed]
    [Google Scholar]
  21. Ma S, Huang Y, Wang C, Fan H, Dai L et al. Defluviitalea raffinosedens sp. nov., a thermophilic, anaerobic, saccharolytic bacterium isolated from an anaerobic batch digester treating animal manure and rice straw. Int J Syst Evol Microbiol 2017;67:1607–1612 [CrossRef][PubMed]
    [Google Scholar]
  22. 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[PubMed]
    [Google Scholar]
  23. 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 [CrossRef]
    [Google Scholar]
  24. 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 [CrossRef]
    [Google Scholar]
  25. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959;37:911–917 [CrossRef][PubMed]
    [Google Scholar]
  26. Tindall BJ, Sikorski J, Smibert RA, Krieg NR. Phenotypic characterization and the principles of comparative systematics. Methods for General and Molecular Microbiology, 3rd ed. American Society of Microbiology; 2007
    [Google Scholar]
  27. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981;17:368–376 [CrossRef][PubMed]
    [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 [CrossRef][PubMed]
    [Google Scholar]
  29. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 2016;33:1870–1874 [CrossRef][PubMed]
    [Google Scholar]
  30. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985;39:783–791 [CrossRef][PubMed]
    [Google Scholar]
  31. Adeolu M, Alnajar S, Naushad S, S Gupta R. Genome-based phylogeny and taxonomy of the 'Enterobacteriales': proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol 2016;66:5575–5599 [CrossRef][PubMed]
    [Google Scholar]
  32. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010;11:119 [CrossRef][PubMed]
    [Google Scholar]
  33. Eddy SR. Accelerated Profile HMM Searches. PLoS Comput Biol 2011;7:e1002195 [CrossRef][PubMed]
    [Google Scholar]
  34. Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004;5:113 [CrossRef]
    [Google Scholar]
  35. Price MN, Dehal PS, Arkin AP. FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS One 2010;5:e9490 [CrossRef][PubMed]
    [Google Scholar]
  36. Whelan S, Goldman N. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 2001;18:691–699 [CrossRef][PubMed]
    [Google Scholar]
  37. Segata N, Börnigen D, Morgan XC, Huttenhower C. PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat Commun 2013;4:2304 [CrossRef][PubMed]
    [Google Scholar]
  38. Lee I, Ouk Kim Y, Park SC, Chun J. OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 2016;66:1100–1103 [CrossRef]
    [Google Scholar]
  39. Qin QL, Xie BB, Zhang XY, Chen XL, Zhou BC et al. A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 2014;196:2210–2215 [CrossRef][PubMed]
    [Google Scholar]
  40. Sekiguchi Y et al. Tepidanaerobacter syntrophicus gen. nov., sp. nov., an anaerobic, moderately thermophilic, syntrophic alcohol- and lactate-degrading bacterium isolated from thermophilic digested sludges. Int J Syst Evol Microbiol 2006;56:1621–1629 [CrossRef]
    [Google Scholar]
  41. 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 [CrossRef][PubMed]
    [Google Scholar]
  42. Kunisawa T. Evolutionary relationships of completely sequenced Clostridia species and close relatives. Int J Syst Evol Microbiol 2015;65:4276–4283 [CrossRef][PubMed]
    [Google Scholar]
  43. Antunes LC, Poppleton D, Klingl A, Criscuolo A, Dupuy B et al. Phylogenomic analysis supports the ancestral presence of LPS-outer membranes in the Firmicutes. eLife 2016;5: [CrossRef][PubMed]
    [Google Scholar]
  44. Sultanpuram VR, Mothe T, Chintalapati S, Chintalapati VR. Pelagirhabdus alkalitolerans gen. nov., sp. nov., an alkali-tolerant and thermotolerant bacterium isolated from beach sediment, and reclassification of Amphibacillus fermentum as Pelagirhabdus fermentum comb. nov. Int J Syst Evol Microbiol 2016;66:84–90 [CrossRef][PubMed]
    [Google Scholar]
  45. Zavarzina DG, Tourova TP, Kuznetsov BB, Bonch-Osmolovskaya EA, Slobodkin AI. Thermovenabulum ferriorganovorum gen. nov., sp. nov., a novel thermophilic, anaerobic, endospore-forming bacterium. Int J Syst Evol Microbiol 2002;52:1737–1743 [CrossRef][PubMed]
    [Google Scholar]
  46. Luo C, Rodriguez-R LM, Konstantinidis KT. MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences. Nucleic Acids Res 2014;42:e73 [CrossRef][PubMed]
    [Google Scholar]
  47. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 2018;9:5114 [CrossRef][PubMed]
    [Google Scholar]
  48. Ogg CD, Patel BK. Fervidicola ferrireducens gen. nov., sp. nov., a thermophilic anaerobic bacterium from geothermal waters of the Great Artesian Basin, Australia. Int J Syst Evol Microbiol 2009;59:1100–1107 [CrossRef][PubMed]
    [Google Scholar]
  49. Mäkinen AE, Kaksonen AH, Puhakka JA. Thermovorax subterraneus, gen. nov., sp. nov., a thermophilic hydrogen-producing bacterium isolated from geothermally active underground mine. Extremophiles 2009;13:505–510 [CrossRef][PubMed]
    [Google Scholar]
  50. Wagner ID, Ahmed S, Zhao W, Zhang CL, Romanek CS et al. Caldanaerovirga acetigignens gen. nov., sp. nov., an anaerobic xylanolytic, alkalithermophilic bacterium isolated from Trego Hot Spring, Nevada, USA. Int J Syst Evol Microbiol 2009;59:2685–2691 [CrossRef][PubMed]
    [Google Scholar]
  51. Aliyu H, Lebre P, Blom J, Cowan D, de Maayer P. Phylogenomic re-assessment of the thermophilic genus Geobacillus. Syst Appl Microbiol 2016;39:527–533 [CrossRef][PubMed]
    [Google Scholar]
  52. Li Y, Xue H, Sang SQ, Lin CL, Wang XZ. Phylogenetic analysis of family Neisseriaceae based on genome sequences and description of Populibacter corticis gen. nov., sp. nov., a member of the family Neisseriaceae, isolated from symptomatic bark of Populus × euramericana canker. PLoS One 2017;12:e0174506 [CrossRef][PubMed]
    [Google Scholar]
  53. Lopes-Santos L, Castro DBA, Ferreira-Tonin M, Corrêa DBA, Weir BS et al. Reassessment of the taxonomic position of Burkholderia andropogonis and description of Robbsia andropogonis gen. nov., comb. nov. Antonie van Leeuwenhoek 2017;110:727–736 [CrossRef][PubMed]
    [Google Scholar]
  54. Wirth JS, Whitman WB. Phylogenomic analyses of a clade within the roseobacter group suggest taxonomic reassignments of species of the genera Aestuariivita, Citreicella, Loktanella, Nautella, Pelagibaca, Ruegeria, Thalassobius, Thiobacimonas and Tropicibacter, and the proposal of six novel genera. Int J Syst Evol Microbiol 2018;68:2393–2411 [CrossRef]
    [Google Scholar]
  55. Zhao H, Yang D, Woese CR, Bryant MP. Assignment of fatty acid-beta-oxidizing syntrophic bacteria to Syntrophomonadaceae fam. nov. on the basis of 16S rRNA sequence analyses. Int J Syst Bacteriol 1993;43:278–286 [CrossRef][PubMed]
    [Google Scholar]
  56. Westerholm M, Roos S, Schnürer A. Tepidanaerobacter acetatoxydans sp. nov., an anaerobic, syntrophic acetate-oxidizing bacterium isolated from two ammonium-enriched mesophilic methanogenic processes. Syst Appl Microbiol 2011;34:260–266 [CrossRef][PubMed]
    [Google Scholar]
  57. Ogg CD, Greene AC, Patel BK. Thermovenabulum gondwanense sp. nov., a thermophilic anaerobic Fe(III)-reducing bacterium isolated from microbial mats thriving in a Great Artesian Basin bore runoff channel. Int J Syst Evol Microbiol 2010;60:1079–1084 [CrossRef][PubMed]
    [Google Scholar]
  58. Lee Y-J, Wagner ID, Brice ME, Kevbrin VV, Mills GL et al. Thermosediminibacter oceani gen. nov., sp. nov. and Thermosediminibacter litoriperuensis sp. nov., new anaerobic thermophilic bacteria isolated from Peru Margin. Extremophiles 2005;9:375–383 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.003701
Loading
/content/journal/ijsem/10.1099/ijsem.0.003701
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most cited this month 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