1887

Abstract

During a screening study to determine the presence of species of the genus in reptiles, three putative strains (RC7, RC11 and RC20) were isolated from different individuals of the western Hermann’s tortoise (). Initially, these isolates were characterized as representing subsp. by multiplex PCR and partial 16S rRNA gene sequence analysis. Further whole- genome characterization revealed considerable differences compared to other species. A polyphasic study was then undertaken to determine the exact taxonomic position of the isolates. The three strains were characterized by conventional phenotypic tests and whole genome sequencing. We generated robust phylogenies that showed a distinct clade containing only these strains using the 16S rRNA and genes and a set of 40 universal proteins. Our phylogenetic analysis demonstrates their designation as representing a novel species and this was further confirmed using whole- genome average nucleotide identity within the genus (~80 %). Compared to most species, these strains hydrolysed hippurate, and grew well at 25 °C but not at 42 °C. Phenotypic and genetic analyses demonstrate that the three strains isolated from the western Hermann’s tortoise represent a novel species within the genus , for which the name sp. nov. is proposed, with RC20 (=DSM 102159=LMG 29375) as the type strain.

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2016-09-01
2024-04-24
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References

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410 [View Article][PubMed]
    [Google Scholar]
  2. Charif D., Thioulouse J., Lobry J. R., Perrière G. 2005; Online synonymous codon usage analyses with the ade4 and seqinR packages. Bioinformatics 21:545–547 [View Article][PubMed]
    [Google Scholar]
  3. Debruyne L., Broman T., Bergstrom S., Olsen B., On S. L. W., Vandamme P. 2010a; Campylobacter subantarcticus sp. nov., isolated from birds in the sub-Antarctic region. Int J Syst Evol Microbiol 60:815–819 [View Article]
    [Google Scholar]
  4. Debruyne L., Broman T., Bergstrom S., Olsen B., On S. L. W., Vandamme P. 2010b; Campylobacter volucris sp. nov., isolated from black-headed gulls (Larus ridibundus) . Int J Syst Evol Microbiol 60:1870–1875 [View Article]
    [Google Scholar]
  5. Debruyne L., Gevers D., Vandamme P. 2008; Taxonomy of the family of Campylobacteraceae . In Campylobacter , pp. 3–25 Edited by Nachamkin I., Szymanski C. M., Blaser M. J. Washington D.C: ASM press; [CrossRef]
    [Google Scholar]
  6. Debruyne L., On S. L. W., De Brandt E., Vandamme P. 2009; Novel Campylobacter lari-like bacteria from humans and molluscs: description of Campylobacter peloridis sp. nov., Campylobacter lari subsp. concheus subsp. nov. and Campylobacter lari subsp. lari subsp. nov. J Syst Evol Microbiol 59:1126–1132 [View Article]
    [Google Scholar]
  7. Fitzgerald C., Tu Z. C., Patrick M., Stiles T., Lawson A. J., Santovenia M., Gilbert M. J., van Bergen M., Joyce K. et al. 2014; Campylobacter fetus subsp. testudinum subsp. nov., isolated from humans and reptiles. Int J Syst Evol Microbiol 64:2944–2948 [View Article][PubMed]
    [Google Scholar]
  8. Giacomelli M., Piccirillo A. 2014; Pet reptiles as potential reservoir of Campylobacter species with zoonotic potential. Vet Rec 174:479 [View Article][PubMed]
    [Google Scholar]
  9. Giacomelli M., Andrighetto C., Lombardi A., Martini M., Piccirillo A. 2012; A longitudinal study on thermophilic Campylobacter spp. in commercial turkey flocks in northern Italy: occurrence and genetic diversity. Avian Dis 56:693–700 [View Article][PubMed]
    [Google Scholar]
  10. Gilbert M. J., Kik M., Miller W. G., Duim B., Wagenaar J. A. 2015; Campylobacter iguaniorum sp. nov., isolated from reptiles. Int J Syst Evol Microbiol 65:975–982 [View Article][PubMed]
    [Google Scholar]
  11. Goris J., Konstantinidis K. T., Klappenbach J. A., Coenye T., Vandamme P., Tiedje J. M. 2007; DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91 [View Article][PubMed]
    [Google Scholar]
  12. Hum S., Quinn K., Brunner J., On S. L. 1997; Evaluation of a PCR assay for identification and differentiation of Campylobacter fetus subspecies. Aust Vet J 75:827–831 [View Article][PubMed]
    [Google Scholar]
  13. Inglis G. D., Hoar B. M., Whiteside D. P., Morck D. W. 2007; Campylobacter canadensis sp. nov., from captive whooping cranes in Canada. Int J Syst Evol Microbiol 57:2636–2644 [View Article][PubMed]
    [Google Scholar]
  14. Iraola G., Hernández M., Calleros L., Paolicchi F., Silveyra S., Velilla A., Carretto L., Rodríguez E., Pérez R. 2012; Application of a multiplex PCR assay for Campylobacter fetus detection and subspecies differentiation in uncultured samples of aborted bovine fetuses. J Vet Sci 13:371–376 [View Article][PubMed]
    [Google Scholar]
  15. Iraola G., Pérez R., Naya H., Paolicchi F., Pastor E., Valenzuela S., Morsella C., Velilla A., Hernández M. et al. 2014; Genomic evidence for the emergence and evolution of pathogenicity and niche preferences in the genus Campylobacter . Genome Biol Evol 6:2392–2405 [View Article][PubMed]
    [Google Scholar]
  16. Kaakoush N. O., Castaño-Rodríguez N., Mitchell H. M., Man S. M. 2015; Global epidemiology of Campylobacter infection. Clin Microbiol Rev 28:687–720 [View Article][PubMed]
    [Google Scholar]
  17. Konstantinidis K. T., Tiedje J. M. 2005; Genomic insights that advance the species definition for prokaryotes. PNAS 102:2567–2572 [View Article][PubMed]
    [Google Scholar]
  18. Koziel M., O'Doherty P., Vandamme P., Corcoran G. D., Sleator R. D., Lucey B. 2014; Campylobacter corcagiensis sp. nov., isolated from faeces of captive lion-tailed macaques (Macaca silenus) . Int J Syst Evol Microbiol 64:2878–2883 [View Article][PubMed]
    [Google Scholar]
  19. Lawson A. J., On S. L., Logan J. M., Stanley J. 2001; Campylobacter hominis sp. nov., from the human gastrointestinal tract. Int J Syst Evol Microbiol 51:651–660 [View Article][PubMed]
    [Google Scholar]
  20. Linton D., Owen R. J., Stanley J. 1996; Rapid identification by PCR of the genus Campylobacter and of five Campylobacter species enteropathogenic for man and animals. Res Microbiol 147:707–718 [View Article][PubMed]
    [Google Scholar]
  21. Maiwald M. 2004; Broad-Range PCR for Detection and Identification of Bacteria. In Molecular Microbiology: Diagnostics Principles and Practice , pp. 379–390 Edited by Persing D. H., Tenover F. C., Versalovic J., Tang Y. W., Relman D., White T. J. Washington D.C: ASM press;
    [Google Scholar]
  22. Man S. M. 2011; The clinical importance of emerging Campylobacter species. NatRev Gastroenterol Hepatol 8:669–685 [View Article]
    [Google Scholar]
  23. Mende D. R., Sunagawa S., Zeller G., Bork P. 2013; Accurate and universal delineation of prokaryotic species. Nat Methods 10:881–884 [View Article][PubMed]
    [Google Scholar]
  24. Miller W. G., Yee E., Jolley K. A., Chapman M. H. 2014; Use of an improved atpA amplification and sequencing method to identify members of the Campylobacteraceae and Helicobacteraceae. Lett Appl Microbiol 58:582–590 [View Article][PubMed]
    [Google Scholar]
  25. On S. L., Holmes B. 1991a; Effect of inoculum size on the phenotypic characterization of Campylobacter species. J Clin Microbiol 29:923–926[PubMed]
    [Google Scholar]
  26. On S. L., Holmes B. 1991b; Reproducibility of tolerance tests that are useful in the identification of campylobacteria. J Clin Microbiol 29:1785–1788[PubMed]
    [Google Scholar]
  27. On S. L., Holmes B. 1992; Assessment of enzyme detection tests useful in identification of campylobacteria. J Clin Microbiol 30:746–749[PubMed]
    [Google Scholar]
  28. On S. L., Atabay H. I., Corry J. E., Harrington C. S., Vandamme P. 1998; Emended description of Campylobacter sputorum and revision of its infrasubspecific (biovar) divisions, including C . sputorum biovar paraureolyticus, a urease-producing variant from cattle and humans. Int J Syst Bacteriol 48:195–206 [View Article][PubMed]
    [Google Scholar]
  29. On S. L., Holmes B., Sackin M. J. 1996; A probability matrix for the identification of campylobacters, helicobacters and allied taxa. J Appl Bacteriol 81:425–432[PubMed]
    [Google Scholar]
  30. Roop II R. M., Smibert R. M., Johnson J. L., Krieg N. R. 1985; Campylobacter mucosalis (Lawson, Leaver, Pettigrew, and Rowland 1981) comb. nov.: emended description. Int J Syst Bacteriol 35:189–192 [View Article]
    [Google Scholar]
  31. Rossi M., Debruyne L., Zanoni R. G., Manfreda G., Revez J., Vandamme P. 2009; Campylobacter avium sp. nov., a hippurate-positive species isolated from poultry. Int J Syst Evol Microbiol 59:2364–2369 [View Article][PubMed]
    [Google Scholar]
  32. Sebald M., Véron M. 1963; Teneur en bases de l’AND et classification des vibrions. Ann Inst Pasteur 105:897–910
    [Google Scholar]
  33. Seemann T. 2014; Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069 [View Article][PubMed]
    [Google Scholar]
  34. Stamatakis A. 2014; RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313 [View Article][PubMed]
    [Google Scholar]
  35. Sunagawa S., Mende D. R., Zeller G., Izquierdo-Carrasco F., Berger S. A., Kultima J. R., Coelho L. P., Arumugam M., Tap J. et al. 2013; Metagenomic species profiling using universal phylogenetic marker genes. Nat Methods 10:1196–1199 [View Article][PubMed]
    [Google Scholar]
  36. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013; mega6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729 [View Article][PubMed]
    [Google Scholar]
  37. Tanner A. C. R., Badger S., Lai C. H., Listgarten M. A., Visconti R. A., Socransky S. S. 1981; Wolinella gen. nov., Wolinella succinogenes (Vibrio succinogenes Wolin et al.) comb. nov., and description of Bacteroides gracilis sp. nov., Wolinella recta sp. nov., Campylobacter concisus sp. nov., and Eikenella corrodens from humans with periodontal disease. Int J Syst Bacteriol 31:432–445 [View Article]
    [Google Scholar]
  38. Ursing J. B., Lior H., Owen R. J. 1994; Proposal of minimal standards for describing new species of the family Campylobacteraceae . Int J Syst Bacteriol 44:842–845 [View Article][PubMed]
    [Google Scholar]
  39. Vandamme P., Daneshvar M. I., Dewhirst F. E., Paster B. J., Kersters K., Goossens H., Moss C. W. 1995; Chemotaxonomic analyses of Bacteroides gracilis and Bacteroides ureolyticus and reclassification of B . gracilis as Campylobacter gracilis comb. nov. Int J Syst Bacteriol 45:145–152 [View Article][PubMed]
    [Google Scholar]
  40. Vandamme P., Debruyne L., De Brandt E., Falsen E. 2010; Reclassification of Bacteroides ureolyticus as Campylobacter ureolyticus comb. nov., and emended description of the genus Campylobacter . Int J Syst Evol Microbiol 60:2016–2022 [View Article][PubMed]
    [Google Scholar]
  41. Vandamme P., Dewhirst F. E., Paster B. J., On. S. L. W. 2005; Genus I. Campylobacter . In Bergey’s Manual of Systematic Bacteriology, 2nd edn. vol. 2 pp 1147–1160 Edited by Garrity G. M., Brenner D. J., Krieg N. R., Staley J. T. New York: Springer-Verlag; [CrossRef]
    [Google Scholar]
  42. Willoughby K., Nettleton P. F., Quirie M., Maley M. A., Foster G., Toszeghy M., Newell D. G. 2005; A multiplex polymerase chain reaction to detect and differentiate Campylobacter fetus subspecies fetus and Campylobacter fetus -species venerealis: use on UK isolates of C . fetus and other Campylobacter spp. J Appl Microbiol 99:758–766 [View Article][PubMed]
    [Google Scholar]
  43. Yamazaki-Matsune W., Taguchi M., Seto K., Kawahara R., Kawatsu K., Kumeda Y., Kitazato M., Nukina M., Misawa N. et al. 2007; Development of a multiplex PCR assay for identification of Campylobacter coli, Campylobacter fetus, Campylobacter hyointestinalis subsp. hyointestinalis, Campylobacter jejuni, Campylobacter lari and Campylobacter upsaliensis . J Med Microbiol 56:1467–1473 [View Article][PubMed]
    [Google Scholar]
  44. Zerbino D. R., Birney E. 2008; Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829 [View Article][PubMed]
    [Google Scholar]
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