1887

Abstract

To clarify the taxonomic position of Eubacterium combesii , the whole genome of its type strain, DSM 20696, was sequenced. Comparison of this sequence with known sequences of other bacteria confirmed that E. combesii represented a member of the Clostridium sporogenes / Clostridium botulinum Group I clade. However, the results of phylogenetic analysis also demonstrated that the latter two species did not form the same genetic entity and that E. combesii was in the C. botulinum Group I subclade. Meanwhile, we showed that E. combesii DSM 20696 did not produce botulinum neurotoxins (BoNTs) and thus should be identified as a strain of C. sporogenes in accordance with the current nomenclature of BoNT-producing clostridia, which is based, in particular, on Opinion 69 issued by the Judicial Commission of the ICSB. However, review of the corresponding Request for an Opinion revealed that it had been based on an erroneous statement. Therefore, we request reconsideration of Opinion 69 and propose to reclassify Eubacterium combesii as a later synonym of Clostridium botulinum . The results of phylogenetic analysis of the other five groups of BoNT-producing clostridia indicated that all the groups were far distant from each other. However, the members of Groups IV–VI are classified as strains of different species, while all members of Groups I–III are designated C. botulinum . Meanwhile, similarly to Group I, Groups II and III are also polyphyletic and appear to consist of two and four species, respectively. These results demonstrate, once again, discrepancies in the nomenclature of BoNT-producing bacteria and corroborate our request for reconsideration of Opinion 69.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.002942
2018-07-30
2019-12-15
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/68/9/3068.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.002942&mimeType=html&fmt=ahah

References

  1. Prévot AR, Laplanche J. Étude d'une bactérie anaérobie nouvelle de Guinée Française Cillobacterium combesi n. sp. Annales de l'Institut Pasteur 1947;73:687–688
    [Google Scholar]
  2. Holdeman LV, Moore WEC. Eubacterium. In Cato EP, Cummins CS, Holdeman LV, Johnson JL, Moore WEC et al. (editors) Outline of Clinical Methods in Anaerobic Bacteriology, 2nd ed. Blacksburg, VA: Virginia Polytechnic Institute, Anaerobe Laboratory; 1970; pp.23–30
    [Google Scholar]
  3. Romanov MN, Bato RV, Yokoyama MT, Rust SR. PCR detection and 16S rRNA sequence-based phylogeny of a novel Propionibacterium acidipropionici applicable for enhanced fermentation of high moisture corn. J Appl Microbiol 2004;97:38–47 [CrossRef][PubMed]
    [Google Scholar]
  4. Dobritsa AP, Kutumbaka KK, Werner K, Wiedmann M, Asmus A et al. Clostridium tepidum sp. nov., a close relative of Clostridium sporogenes and Clostridium botulinum group I. Int J Syst Evol Microbiol 2017;67:2317–2322 [CrossRef][PubMed]
    [Google Scholar]
  5. Moore WEC, Moore LVH. Genus Eubacterium Prevot 1938, 294AL. In Sneath PHA, Mair NS, Sharpe ME, Holt JG. (editors) Bergey’s Manual of Systematic Bacteriologyvol. 2 Baltimore, MD: Williams & Wilkins; 1986; pp.1353–1373
    [Google Scholar]
  6. Euzéby JP. List of Prokaryotic Names with Standing in Nomenclature. www.bacterio.net/eubacterium.html [accessed 21 August 2017]
  7. Dobritsa AP, Kutumbaka KK, Samadpour M. Reclassification of Paraburkholderia panaciterrae (Farh et al. 2015) Dobritsa & Samadpour 2016 as a later synonym of Paraburkholderia ginsengiterrae (Farh et al. 2015) Dobritsa & Samadpour 2016. Int J Syst Evol Microbiol 2016;66:4085–4087 [CrossRef][PubMed]
    [Google Scholar]
  8. Dobritsa AP, Linardopoulou EV, Samadpour M. Transfer of 13 species of the genus Burkholderia to the genus Caballeronia and reclassification of Burkholderia jirisanensis as Paraburkholderia jirisanensis comb. nov. Int J Syst Evol Microbiol 2017;67:3846–3853 [CrossRef][PubMed]
    [Google Scholar]
  9. Nakano K, Terabayashi Y, Shiroma A, Shimoji M, Tamotsu H et al. First complete genome sequence of Clostridium sporogenes DSM 795T, a nontoxigenic surrogate for Clostridium botulinum, determined using pacbio single-molecule real-time technology. Genome Announc 2015;3:e00832-15 [CrossRef][PubMed]
    [Google Scholar]
  10. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013;29:1072–1075 [CrossRef][PubMed]
    [Google Scholar]
  11. Allen B, Drake M, Harris N, Sullivan T. Using KBase to assemble and annotate prokaryotic genomes. Curr Protoc Microbiol 2017;46:1E.13.1–1E.13.18 [CrossRef][PubMed]
    [Google Scholar]
  12. Maslanka SE, Solomon HM, Sharma S, Johnson EA. Clostridium botulinum and its toxins. In Doores S, Salfinger Y, Tortorello ML, Wilcke BW. (editors) Compendium of Methods for the Microbiological Examination of Foods, 5th ed. Washington, DC: American Public Health Association; 2015; pp.391–401
    [Google Scholar]
  13. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007;57:81–91 [CrossRef][PubMed]
    [Google Scholar]
  14. Kim M, Oh HS, Park SC, 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 [CrossRef][PubMed]
    [Google Scholar]
  15. Auch AF, von Jan M, Klenk HP, Göker M. Digital DNA–DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2010;2:117–134 [CrossRef][PubMed]
    [Google Scholar]
  16. Weigand MR, Pena-Gonzalez A, Shirey TB, Broeker RG, Ishaq MK et al. Implications of genome-based discrimination between Clostridium botulinum group I and Clostridium sporogenes strains for bacterial taxonomy. Appl Environ Microbiol 2015;81:5420–5429 [CrossRef][PubMed]
    [Google Scholar]
  17. Williamson CH, Sahl JW, Smith TJ, Xie G, Foley BT et al. Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia. BMC Genomics 2016;17:180 [CrossRef][PubMed]
    [Google Scholar]
  18. Olsen I, Johnson JL, Moore LVH, Moore WEC. Rejection of Clostridium putrificum and conservation of Clostridium botulinum and Clostridium sporogenes. Request for an opinion. Int J Syst Bacteriol 1995;45:414
    [Google Scholar]
  19. Judicial Commission of the International Committee on Systematic Bacteriology Rejection of Clostridium putrificum and conservation of Clostridium botulinum and Clostridium sporogenes - Opinion 69. Int J Syst Bacteriol 1999;49:339
    [Google Scholar]
  20. Hill KK, Smith TJ, Helma CH, Ticknor LO, Foley BT et al. Genetic diversity among botulinum neurotoxin-producing clostridial strains. J Bacteriol 2007;189:818–832 [CrossRef][PubMed]
    [Google Scholar]
  21. Smith TJ, Hill KK, Raphael BH. Historical and current perspectives on Clostridium botulinum diversity. Res Microbiol 2015;166:290–302 [CrossRef][PubMed]
    [Google Scholar]
  22. Peck MW, Smith TJ, Anniballi F, Austin JW, Bano L et al. Historical perspectives and guidelines for botulinum neurotoxin subtype nomenclature. Toxins 2017;9:38 [CrossRef][PubMed]
    [Google Scholar]
  23. Collins MD, East AK. Phylogeny and taxonomy of the food-borne pathogen Clostridium botulinum and its neurotoxins. J Appl Microbiol 1998;84:5–17[PubMed]
    [Google Scholar]
  24. 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]
  25. Hall JD, McCroskey LM, Pincomb BJ, Hatheway CL. Isolation of an organism resembling Clostridium barati which produces type F botulinal toxin from an infant with botulism. J Clin Microbiol 1985;21:654–655[PubMed]
    [Google Scholar]
  26. McCroskey LM, Hatheway CL, Fenicia L, Pasolini B, Aureli P. Characterization of an organism that produces type E botulinal toxin but which resembles Clostridium butyricum from the feces of an infant with type E botulism. J Clin Microbiol 1986;23:201–202[PubMed]
    [Google Scholar]
  27. Suen JC, Hatheway CL, Steigerwalt AG, Brenner DJ. Clostridium argentinense sp. nov.: a genetically homogeneous group composed of all strains of Clostridium botulinum toxin type G and some nontoxigenic strains previously identified as Clostridium subterminale or Clostridium hastiforme. Int J Syst Bacteriol 1988;38:375–381
    [Google Scholar]
  28. Lee WH, Riemann H. The genetic relatedness of proteolytic Clostridium botulinum strains. J Gen Microbiol 1970;64:85–90 [CrossRef][PubMed]
    [Google Scholar]
  29. Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O et al. International Committee on Systematic Bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 1987;37:463–464
    [Google Scholar]
  30. Williamson CHD, Vazquez AJ, Hill K, Smith TJ, Nottingham R et al. Differentiating botulinum neurotoxin-producing clostridia with a simple, multiplex PCR assay. Appl Environ Microbiol 2017;83:e00806-17 [CrossRef][PubMed]
    [Google Scholar]
  31. Bengston IA. Studies on organisms concerned as causative factors in botulism. US Public Health Serv, Hyg Lab Bull 1924;136:1–97
    [Google Scholar]
  32. Spray RS, McClung LS, McCoy E. Genus II. Clostridium Prazmowski, 1880. In Breed RS, Murray EGD, Smith NR. (editors) Bergey’s Manual of Determinative Bacteriology, 7th ed. Baltimore, MD: Williams & Wilkins; 1957; pp.634–693
    [Google Scholar]
  33. Prévot AR. Rapport d'introduction du president du sous-comite Clostridium pour l'unification de la nomenclature des types toxinogènes de C. botulinum. Int Bull Bact Nomen Tax 1953;3:120–123
    [Google Scholar]
  34. Stringer SC, Carter AT, Webb MD, Wachnicka E, Crossman LC et al. Genomic and physiological variability within Group II (non-proteolytic) Clostridium botulinum. BMC Genomics 2013;14:333 [CrossRef][PubMed]
    [Google Scholar]
  35. Gunnison JB, Meyer KF. Cultural study of an international collection of Clostridium botulinum and Parabotulinum. XXXVIII. J Infect Dis 1929;45:119–134 [CrossRef]
    [Google Scholar]
  36. Parker CT, Tindall BJ, Garrity GM. International code of nomenclature of prokaryotes. Prokaryotic code (2008 Revision). Int J Syst Evol Microbiol 2015.; [Epub ahead of print]
    [Google Scholar]
  37. Sasaki Y, Takikawa N, Kojima A, Norimatsu M, Suzuki S et al. Phylogenetic positions of Clostridium novyi and Clostridium haemolyticum based on 16S rDNA sequences. Int J Syst Evol Microbiol 2001;51:901–904 [CrossRef][PubMed]
    [Google Scholar]
  38. Skarin H, Segerman B. Plasmidome interchange between Clostridium botulinum, Clostridium novyi and Clostridium haemolyticum converts strains of independent lineages into distinctly different pathogens. PLoS One 2014;9:e107777 [CrossRef][PubMed]
    [Google Scholar]
  39. Institutional Animal Care and Use Committee Guidebook, 2nd ed. Bethesda, MD: ARENA/OLAW; 2002
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.002942
Loading
/content/journal/ijsem/10.1099/ijsem.0.002942
Loading

Data & Media loading...

Most Cited This Month

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