1887

Abstract

The class is currently divided into one order and two families on the basis of 16S rRNA gene sequence phylogenies. We report here comprehensive comparative genomic analyses of the sequenced members of the class to demarcate its different evolutionary groups in molecular terms, independently of phylogenetic trees. Our comparative genomic analyses have identified 14 conserved signature indels (CSIs) and 48 conserved signature proteins (CSPs) that either are specific for the entire class or differentiate four main groups within the class. Two CSIs and nine CSPs are shared uniquely by all or most members of the class , distinguishing this class from all other sequenced members of the phylum . Four other CSIs and six CSPs were specific characteristics of the family , two CSIs and four CSPs were uniquely present in the family , six CSIs and eight CSPs were found only in and related genera, and 17 CSPs were identified uniquely in and related genera. Four additional CSPs support a pairing of the groups containing the genera and . We also report detailed phylogenetic analyses for the based on core protein sequences and 16S rRNA gene sequences, which strongly support the four main groups identified by CSIs and by CSPs. Based on the results from different lines of investigation, we propose a division of the class into an emended order containing the new families fam. nov. and fam. nov. and two new orders, ord. nov. and ord. nov., respectively containing the families and .

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2015-09-01
2019-12-05
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References

  1. Ahmod N.Z. , Gupta R.S. , Shah H.N. . ( 2011;). Identification of a Bacillus anthracis specific indel in the yeaC gene and development of a rapid pyrosequencing assay for distinguishing B. anthracis from the B. cereus group. J Microbiol Methods 87: 278–285 [CrossRef] [PubMed].
    [Google Scholar]
  2. Altschul S.F. , Madden T.L. , Schäffer A.A. , Zhang J. , Zhang Z. , Miller W. , Lipman D.J. . ( 1997;). Gapped blast psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402 [CrossRef] [PubMed].
    [Google Scholar]
  3. Campbell C. , Sutcliffe I.C. , Gupta R.S. . ( 2014;). Comparative proteome analysis of Acidaminococcus intestini supports a relationship between outer membrane biogenesis in Negativicutes and Proteobacteria . Arch Microbiol 196: 307–310 [CrossRef] [PubMed].
    [Google Scholar]
  4. Castresana J. . ( 2000;). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540–552 [CrossRef] [PubMed].
    [Google Scholar]
  5. Cole J.R. , Wang Q. , Fish J.A. , Chai B. , McGarrell D.M. , Sun Y. , Brown C.T. , Porras-Alfaro A. , Kuske C.R. , Tiedje J.M. . ( 2014;). Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42: (D1), D633–D642 [CrossRef] [PubMed].
    [Google Scholar]
  6. D'Auria G. , Galán J.C. , Rodríguez-Alcayna M. , Moya A. , Baquero F. , Latorre A. . ( 2011;). Complete genome sequence of Acidaminococcus intestini RYC-MR95, a Gram-negative bacterium from the phylum Firmicutes. J Bacteriol 193: 7008–7009 [CrossRef] [PubMed].
    [Google Scholar]
  7. Edgar R.C. . ( 2010;). Search and clustering orders of magnitude faster than blast . Bioinformatics 26: 2460–2461 [CrossRef] [PubMed].
    [Google Scholar]
  8. Fang G. , Rocha E. , Danchin A. . ( 2005;). How essential are nonessential genes?. Mol Biol Evol 22: 2147–2156 [CrossRef] [PubMed].
    [Google Scholar]
  9. Galperin M.Y. , Koonin E.V. . ( 2004;). ‘Conserved hypothetical’ proteins: prioritization of targets for experimental study. Nucleic Acids Res 32: 5452–5463 [CrossRef] [PubMed].
    [Google Scholar]
  10. Gao B. , Gupta R.S. . ( 2007;). Phylogenomic analysis of proteins that are distinctive of Archaea and its main subgroups and the origin of methanogenesis. BMC Genomics 8: 86 [CrossRef] [PubMed].
    [Google Scholar]
  11. Gao B. , Gupta R.S. . ( 2012;). Microbial systematics in the post-genomics era. Antonie van Leeuwenhoek 101: 45–54 [CrossRef] [PubMed].
    [Google Scholar]
  12. Gogarten J.P. , Doolittle W.F. , Lawrence J.G. . ( 2002;). Prokaryotic evolution in light of gene transfer. Mol Biol Evol 19: 2226–2238 [CrossRef] [PubMed].
    [Google Scholar]
  13. Gupta R.S. . ( 1998;). Protein phylogenies and signature sequences: a reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol Mol Biol Rev 62: 1435–1491 [PubMed].
    [Google Scholar]
  14. Gupta R.S. . ( 2010;). Applications of conserved indels for understanding microbial phylogeny. . In Molecular Phylogeny of Microorganisms, pp. 135–150. Edited by Oren A. , Papke R. T. . Wymondham, UK: Caister Academic Press;.
    [Google Scholar]
  15. Gupta R.S. . ( 2014;). Identification of conserved indels that are useful for classification and evolutionary studies. Methods Microbiol 41: 153–182.[CrossRef]
    [Google Scholar]
  16. Gupta R.S. , Griffiths E. . ( 2002;). Critical issues in bacterial phylogeny. Theor Popul Biol 61: 423–434 [CrossRef] [PubMed].
    [Google Scholar]
  17. Gupta R.S. , Griffiths E. . ( 2006;). Chlamydiae-specific proteins and indels: novel tools for studies. Trends Microbiol 14: 527–535 [CrossRef] [PubMed].
    [Google Scholar]
  18. Gupta R.S. , Mok A. . ( 2007;). Phylogenomics and signature proteins for the alpha Proteobacteria and its main groups. BMC Microbiol 7: 106 [CrossRef] [PubMed].
    [Google Scholar]
  19. Gupta R.S. , Mahmood S. , Adeolu M. . ( 2013;). 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 4: 217 [PubMed].
    [Google Scholar]
  20. Gupta R.S. , Naushad S. , Baker S. . ( 2015;). Phylogenomic analyses and molecular signatures for the class Halobacteria and its two major clades: a proposal for division of the class Halobacteria into an emended order Halobacteriales and two new orders, Haloferacales ord. nov. and Natrialbales ord. nov., containing the novel families Haloferacaceae fam. nov. and Natrialbaceae fam. nov.. Int J Syst Evol Microbiol 65: 1050–1069 [CrossRef] [PubMed].
    [Google Scholar]
  21. Jeanmougin F. , Thompson J.D. , Gouy M. , Higgins D.G. , Gibson T.J. . ( 1998;). Multiple sequence alignment with Clustal X. Trends Biochem Sci 23: 403–405 [CrossRef] [PubMed].
    [Google Scholar]
  22. Jones A.L. . ( 2012;). The future of taxonomy. Adv Appl Microbiol 80: 23–35 [PubMed].[CrossRef]
    [Google Scholar]
  23. Katoh K. , Standley D.M. . ( 2013;). mafft multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30: 772–780 [CrossRef] [PubMed].
    [Google Scholar]
  24. Ludwig W. , Schleifer K.-H. , Whitman W.B. . ( 2009;). Revised road map to the phylum Firmicutes . . In Bergey's Manual of Systematic Bacteriology, 2nd edn., vol. 3, pp. 1–13. Edited by De Vos P. , Garrity G. M. , Jones D. , Krieg N. R. , Ludwig W. , Rainey F. A. , Schleifer K. H. , Whitman W. B. . New York: Springer; [CrossRef].
    [Google Scholar]
  25. Marchandin H. , Jumas-Bilak E. . ( 2014;). The family Veillonellaceae . . In The Prokaryotes, 4th edn., vol. 7, pp. 433–453. Edited by Rosenberg E. , DeLong E. , Lory S. , Stackebrandt E. , Thompson F. . Berlin, Heidelberg: Springer; [CrossRef].
    [Google Scholar]
  26. Marchandin H. , Teyssier C. , Campos J. , Jean-Pierre H. , Roger F. , Gay B. , Carlier J.P. , Jumas-Bilak E. . ( 2010;). 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 60: 1271–1279 [CrossRef] [PubMed].
    [Google Scholar]
  27. Mardis E.R. . ( 2008;). The impact of next-generation sequencing technology on genetics. Trends Genet 24: 133–141 [CrossRef] [PubMed].
    [Google Scholar]
  28. Marx H. , Graf A.B. , Tatto N.E. , Thallinger G.G. , Mattanovich D. , Sauer M. . ( 2011;). Genome sequence of the ruminal bacterium Megasphaera elsdenii . J Bacteriol 193: 5578–5579 [CrossRef] [PubMed].
    [Google Scholar]
  29. Moore L.V.H. , Moore W.E.C. . ( 1994;). Oribaculum catoniae gen. nov., sp. nov., Catonella morbi gen. nov., sp. nov., Hallella seregens gen. nov., sp. nov., Johnsonella ignava gen. nov., sp. nov., and Dialister pneumosintes gen. nov., comb. nov., nom. rev., anaerobic gram-negative bacilli from the human gingival crevice. Int J Syst Bacteriol 44: 187–192 [CrossRef] [PubMed].
    [Google Scholar]
  30. Naushad H.S. , Lee B. , Gupta R.S. . ( 2014;). Conserved signature indels and signature proteins as novel tools for understanding microbial phylogeny and systematics: identification of molecular signatures that are specific for the phytopathogenic genera Dickeya, Pectobacterium and Brenneria . Int J Syst Evol Microbiol 64: 366–383 [CrossRef] [PubMed].
    [Google Scholar]
  31. Naushad S. , Adeolu M. , Wong S. , Sohail M. , Schellhorn H.E. , Gupta R.S. . ( 2015;). A phylogenomic and molecular marker based taxonomic framework for the order Xanthomonadales: proposal to transfer the families Algiphilaceae and Solimonadaceae to the order Nevskiales ord. nov. and to create a new family within the order Xanthomonadales, the family Rhodanobacteraceae fam. nov., containing the genus Rhodanobacter and its closest relatives. Antonie van Leeuwenhoek 107: 467–485 [CrossRef] [PubMed].
    [Google Scholar]
  32. NCBI Resource Coordinators ( 2015;). Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 43: (D1), D6–D17 [CrossRef] [PubMed].
    [Google Scholar]
  33. Parte A.C. . ( 2014;). LPSN – list of prokaryotic names with standing in nomenclature. Nucleic Acids Res 42: (D1), D613–D616 [CrossRef] [PubMed].
    [Google Scholar]
  34. Price M.N. , Dehal P.S. , Arkin A.P. . ( 2010;). FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS One 5: e9490 [CrossRef] [PubMed].
    [Google Scholar]
  35. Quast C. , Pruesse E. , Yilmaz P. , Gerken J. , Schweer T. , Yarza P. , Peplies J. , Glöckner F.O. . ( 2013;). The silva ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41: (D1), D590–D596 [CrossRef] [PubMed].
    [Google Scholar]
  36. Rainey F. . ( 2009;). Family X. Veillonellaceae Rogosa 1971b, 232AL . . In Bergey's Manual of Systematic Bacteriology, 2nd edn., vol. 3, pp. 1059–1129. Edited by De Vos P. , Garrity G. M. , Jones D. , Krieg N. R. , Ludwig W. , Rainey F. A. , Schleifer K. H. , Whitman W. B. . New York: Springer;.
    [Google Scholar]
  37. Rogosa M. . ( 1969;). Acidaminococcus gen. n., Acidaminococcus fermentans sp. n., anaerobic gram-negative diplococci using amino acids as the sole energy source for growth. J Bacteriol 98: 756–766 [PubMed].
    [Google Scholar]
  38. Rogosa M. . ( 1971;). Transfer of Veillonella Prévot and Acidaminococcus Rogosa from Neisseriaceae to Veillonellaceae fam. nov., and the inclusion of Megasphaera Rogosa in Veillonellaceae . Int J Syst Bacteriol 21: 231–233 [CrossRef].
    [Google Scholar]
  39. Rokas A. , Holland P.W.H. . ( 2000;). Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15: 454–459 [CrossRef] [PubMed].
    [Google Scholar]
  40. Rokas A. , Williams B.L. , King N. , Carroll S.B. . ( 2003;). Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425: 798–804 [CrossRef] [PubMed].
    [Google Scholar]
  41. Sawana A. , Adeolu M. , Gupta R.S. . ( 2014;). Molecular signatures and phylogenomic analysis of the genus Burkholderia: proposal for division of this genus into the emended genus Burkholderia containing pathogenic organisms and a new genus Paraburkholderia gen. nov. harboring environmental species. Front Genet 5: 429 [CrossRef] [PubMed].
    [Google Scholar]
  42. Shah H.N. , Collins M.D. . ( 1982;). Reclassification of Bacteroides hypermegas (Harrison and Hansen) in a new genus Megamonas, as Megamonas hypermegas comb. nov. Zentralbl Bakteriol Mikrobiol Hyg Abt I Orig C3: 394–398.
    [Google Scholar]
  43. Stackebrandt E. , Pohla H. , Kroppenstedt R. , Hippe H. , Woese C.R. . ( 1985;). 16S rRNA analysis of Sporomusa, Selenomonas, and Megasphaera: on the phylogenetic origin of Gram-positive eubacteria. Arch Microbiol 143: 270–276 [CrossRef].
    [Google Scholar]
  44. Sutcliffe I.C. . ( 2010;). A phylum level perspective on bacterial cell envelope architecture. Trends Microbiol 18: 464–470 [CrossRef] [PubMed].
    [Google Scholar]
  45. Tamura K. , Peterson D. , Peterson N. , Stecher G. , Nei M. , Kumar S. . ( 2011;). mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739 [CrossRef] [PubMed].
    [Google Scholar]
  46. Tavaré S. . ( 1986;). Some probabilistic and statistical problems in the analysis of DNA sequences. . In Lectures on Mathematics in the Life Sciences, vol. 17, pp. 57–86. Edited by Miura R. M. . Providence, RI: American Mathematical Society;.
    [Google Scholar]
  47. Vesth T. , Ozen A. , Andersen S.C. , Kaas R.S. , Lukjancenko O. , Bohlin J. , Nookaew I. , Wassenaar T.M. , Ussery D.W. . ( 2013;). Veillonella, Firmicutes: microbes disguised as Gram negatives. Stand Genomic Sci 9: 431–448 [CrossRef] [PubMed].
    [Google Scholar]
  48. Wendel J.F. , Doyle J.J. . ( 1998;). Phylogenetic incongruence: window into genome history and molecular evolution. . In Molecular Systematics of Plants II, pp. 265–296. Edited by Soltis D. , Soltis P. , Doyle J. . New York: Springer; [CrossRef].
    [Google Scholar]
  49. Whelan S. , Goldman N. . ( 2001;). A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18: 691–699 [CrossRef] [PubMed].
    [Google Scholar]
  50. Willems A. , Collins M.D. . ( 1995;). Evidence for the placement of the gram-negative Catonella morbi (Moore and Moore) and Johnsonella ignava (Moore and Moore) within the Clostridium subphylum of the gram-positive bacteria on the basis of 16S rRNA sequences. Int J Syst Bacteriol 45: 855–857 [CrossRef] [PubMed].
    [Google Scholar]
  51. Wong S.Y. , Paschos A. , Gupta R.S. , Schellhorn H.E. . ( 2014;). Insertion/deletion-based approach for the detection of Escherichia coli O157: H7 in freshwater environments. Environ Sci Technol 48: 11462–11470 [CrossRef] [PubMed].
    [Google Scholar]
  52. Wu D. , Hugenholtz P. , Mavromatis K. , Pukall R. , Dalin E. , Ivanova N.N. , Kunin V. , Goodwin L. , Wu M. , other authors . ( 2009;). A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462: 1056–1060 [CrossRef] [PubMed].
    [Google Scholar]
  53. Yarza P. , Yilmaz P. , Pruesse E. , Glöckner F.O. , Ludwig W. , Schleifer K.H. , Whitman W.B. , Euzéby J. , Amann R. , Rosselló-Móra R. . ( 2014;). Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12: 635–645 [CrossRef] [PubMed].
    [Google Scholar]
  54. Yilmaz P. , Parfrey L.W. , Yarza P. , Gerken J. , Pruesse E. , Quast C. , Schweer T. , Peplies J. , Ludwig W. , Glöckner F.O. . ( 2014;). The silva and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Res 42: D643–D648 [PubMed].[CrossRef]
    [Google Scholar]
  55. Yutin N. , Galperin M.Y. . ( 2013;). A genomic update on clostridial phylogeny: Gram-negative spore formers and other misplaced clostridia. Environ Microbiol 15: 2631–2641 [PubMed].
    [Google Scholar]
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