1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 65, Issue Pt_9

Genome-based taxonomic framework for the class : division of the class into the orders emend., ord. nov. and ord. nov. Free

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 .

  • Published Online:
© 2015 IUMS
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.000347
2015-09-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/65/9/3203.html?itemId=/content/journal/ijsem/10.1099/ijs.0.000347&mimeType=html&fmt=ahah

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 [View Article] [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 [View Article] [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 [View Article] [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 [View Article] [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 [View Article] [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 [View Article] [PubMed] .
     [Google Scholar]
  7. Edgar R.C. ( 2010;). Search and clustering orders of magnitude faster than blast . Bioinformatics 26 2460–2461 [View Article] [PubMed] .
     [Google Scholar]
  8. Fang G., Rocha E., Danchin A. ( 2005;). How essential are nonessential genes?. Mol Biol Evol 22 2147–2156 [View Article] [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 [View Article] [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 [View Article] [PubMed] .
     [Google Scholar]
  11. Gao B., Gupta R.S. ( 2012;). Microbial systematics in the post-genomics era. Antonie van Leeuwenhoek 101 45–54 [View Article] [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 [View Article] [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 [View Article] [PubMed] .
     [Google Scholar]
  17. Gupta R.S., Griffiths E. ( 2006;). Chlamydiae-specific proteins and indels: novel tools for studies. Trends Microbiol 14 527–535 [View Article] [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 [View Article] [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 [View Article] [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 [View Article] [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 [View Article] [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; [View Article].
     [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; [View Article].
     [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 [View Article] [PubMed] .
     [Google Scholar]
  27. Mardis E.R. ( 2008;). The impact of next-generation sequencing technology on genetics. Trends Genet 24 133–141 [View Article] [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 [View Article] [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 [View Article] [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 [View Article] [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 [View Article] [PubMed] .
     [Google Scholar]
  32. NCBI Resource Coordinators ( 2015;). Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 43 (D1), D6–D17 [View Article] [PubMed] .
     [Google Scholar]
  33. Parte A.C. ( 2014;). LPSN – list of prokaryotic names with standing in nomenclature. Nucleic Acids Res 42 (D1), D613–D616 [View Article] [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 [View Article] [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 [View Article] [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 [View Article].
     [Google Scholar]
  39. Rokas A., Holland P.W.H. ( 2000;). Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15 454–459 [View Article] [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 [View Article] [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 [View Article] [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 [View Article].
     [Google Scholar]
  44. Sutcliffe I.C. ( 2010;). A phylum level perspective on bacterial cell envelope architecture. Trends Microbiol 18 464–470 [View Article] [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 [View Article] [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 [View Article] [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; [View Article].
     [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 [View Article] [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 [View Article] [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 [View Article] [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 [View Article] [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 [View Article] [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]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijs.0.000347
Loading
Genome-based taxonomic framework for the class Negativicutes: division of the class Negativicutes into the orders Selenomonadales emend., Acidaminococcales ord. nov. and Veillonellales ord. nov.
Int J Syst Evol Microbiol 65, 3203 (2015); https://doi.org/10.1099/ijs.0.000347
/content/journal/ijsem/10.1099/ijs.0.000347
/content/journal/ijsem/10.1099/ijs.0.000347
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF

Most cited 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