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Volume 5, Issue 10

Genus-wide core-genome multilocus sequence typing for species identification and strain characterization Open Access

Abstract

The genus comprises species that differ widely in their pathogenic potential and public-health significance. is responsible for plague, while is a prominent enteropathogen. Strains within some species, including also vary in their pathogenic properties. Phenotypic identification of species is time-consuming, labour-intensive and may lead to incorrect identifications. Here, we developed a method to automatically identify and subtype all isolates from their genomic sequence. A phylogenetic analysis of isolates based on a core subset of 500 shared genes clearly demarcated all existing species and uncovered novel, yet undefined taxa. An automated taxonomic assignment procedure was developed using species-specific thresholds based on core-genome multilocus sequence typing (cgMLST). The performance of this method was assessed on 1843 isolates prospectively collected by the French National Surveillance System and analysed in parallel using phenotypic reference methods, leading to nearly complete (1814; 98.4 %) agreement at species and infra-specific (biotype and serotype) levels. For 29 isolates, incorrect phenotypic assignments resulted from atypical biochemical characteristics or lack of phenotypic resolution. To provide an identification tool, a database of cgMLST profiles and reference taxonomic information has been made publicly accessible (https://bigsdb.pasteur.fr/yersinia). Genomic sequencing-based identification and subtyping of any is a powerful and reliable novel approach to define the pathogenic potential of isolates of this medically important genus.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): core-genome multilocus sequence typing , genotyping , identification , phylogenetics , species and Yersinia
© 2019 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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2019-10-01
2024-04-19
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References

  1. Carniel E, Autenrieth I, Cornelis G, Fukushima H, Guinet F et al. Y. enterocolitica and Y. pseudotuberculosis . In Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E. eds The Prokaryotes New York: Dworkin; 2006 pp 270–398
     [Google Scholar]
  2. EFSA ECDC The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. Efsa J 2018; 16:5500
     [Google Scholar]
  3. Ross AJ, Rucker RR, Ewing WH. Description of a bacterium associated with redmouth disease of rainbow trout (Salmo gairdneri). Can J Microbiol 1966; 12:763–770 [View Article]
     [Google Scholar]
  4. Hurst MRH, Becher SA, Young SD, Nelson TL, Glare TR. Yersinia entomophaga sp. nov., isolated from the New Zealand grass grub Costelytra zealandica . Int J Syst Evol Microbiol 2011; 61:844–849 [View Article]
     [Google Scholar]
  5. Sprague LD, Neubauer H. Yersinia aleksiciae sp. nov. Int J Syst Evol Microbiol 2005; 55:831–835 [View Article]
     [Google Scholar]
  6. Merhej V, Adékambi T, Pagnier I, Raoult D, Drancourt M. Yersinia massiliensis sp. nov., isolated from fresh water. Int J Syst Evol Microbiol 2008; 58:779–784 [View Article]
     [Google Scholar]
  7. Sprague LD, Scholz HC, Amann S, Busse HJ, Neubauer H. Yersinia similis sp. nov. Int J Syst Evol Microbiol 2008; 58:952–958 [View Article]
     [Google Scholar]
  8. Murros-Kontiainen A, Johansson P, Niskanen T, Fredriksson-Ahomaa M, Korkeala H et al. Yersinia pekkanenii sp. nov. Int J Syst Evol Microbiol 2011; 61:2363–2367 [View Article]
     [Google Scholar]
  9. Murros-Kontiainen A, Fredriksson-Ahomaa M, Korkeala H, Johansson P, Rahkila R et al. Yersinia nurmii sp. nov. Int J Syst Evol Microbiol 2011; 61:2368–2372 [View Article]
     [Google Scholar]
  10. Nguyen SV, Muthappa DM, Hurley D, Donoghue O, McCabe E et al. Yersinia hibernica sp. nov., isolated from pig-production environments. Int J Syst Evol Microbiol 2019; 69:2023–2027
     [Google Scholar]
  11. Savin C, Martin L, Bouchier C, Filali S, Chenau J et al. The Yersinia pseudotuberculosis complex: characterization and delineation of a new species, Yersinia wautersii . Int J Med Microbiol 2014; 304:452–463 [View Article]
     [Google Scholar]
  12. Kandolo K, Wauters G. Pyrazinamidase activity in Yersinia enterocolitica and related organisms. J Clin Microbiol 1985; 21:980–982
     [Google Scholar]
  13. Lee WH. Two plating media modified with Tween 80 for isolating Yersinia enterocolitica . Appl Env Microbiol 1977; 33:215–216
     [Google Scholar]
  14. Wauters G, Aleksić S, Charlier J, Schulze G. Somatic and flagellar antigens of Yersinia enterocolitica and related species. Contrib Microbiol Immunol 1991; 12:239–243
     [Google Scholar]
  15. Wauters G, Kandolo K, Janssens M. Revised biogrouping scheme of Yersinia enterocolitica . Contrib Microbiol Immunol 1987; 9:14–21
     [Google Scholar]
  16. Martin L, Leclercq A, Savin C, Carniel E. Characterization of atypical isolates of Yersinia intermedia and definition of two new biotypes. J Clin Microbiol 2009; 47:2377–2380 [View Article]
     [Google Scholar]
  17. Gérôme P, Le Flèche P, Blouin Y, Scholz HC, Thibault FM et al. Yersinia pseudotuberculosis ST42 (O:1) strain misidentified as Yersinia pestis by mass spectrometry analysis. Genome Announc 2014; 2:e00435-14
     [Google Scholar]
  18. Ayyadurai S, Flaudrops C, Raoult D, Drancourt M. Rapid identification and typing of Yersinia pestis and other Yersinia species by matrix-assisted laser desorption/ionization time-of-flight (MALDI-TOF) mass spectrometry. BMC Microbiol 2010; 10:285 [View Article]
     [Google Scholar]
  19. Harch SAJ, Jennison AV, Bastian I. Yersinia pseudotuberculosis bacteraemia: a diagnostic dilemma in the era of MALDI-TOF mass spectrometry. Pathology 2019; 51:434–436 [View Article]
     [Google Scholar]
  20. Rizzardi K, Wahab T, Jernberg C. Rapid subtyping of Yersinia enterocolitica by matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) for diagnostics and surveillance. J Clin Microbiol 2013; 51:4200–4203 [View Article]
     [Google Scholar]
  21. Kotetishvili M, Kreger A, Wauters G, Morris JG, Sulakvelidze A et al. Multilocus sequence typing for studying genetic relationships among Yersinia species. J Clin Microbiol 2005; 43:2674–2684 [View Article]
     [Google Scholar]
  22. Duan R, Liang J, Shi G, Cui Z, Hai R et al. Homology analysis of pathogenic Yersinia species Yersinia enterocolitica, Yersinia pseudotuberculosis, and Yersinia pestis based on multilocus sequence typing. J Clin Microbiol 2014; 52:20–29 [View Article]
     [Google Scholar]
  23. Hall M, Chattaway MA, Reuter S, Savin C, Strauch E et al. Use of whole-genus genome sequence data to develop a multilocus sequence typing tool that accurately identifies Yersinia isolates to the species and subspecies levels. J Clin Microbiol 2015; 53:35–42 [View Article]
     [Google Scholar]
  24. Maiden MCJ, Jansen van Rensburg MJ, Bray JE, Earle SG, Ford SA et al. MLST revisited: the gene-by-gene approach to bacterial genomics. Nat Rev Microbiol 2013; 11:728–736 [View Article]
     [Google Scholar]
  25. Bialek-Davenet S, Criscuolo A, Ailloud F, Passet V, Jones L et al. Genomic definition of hypervirulent and multidrug-resistant Klebsiella pneumoniae clonal groups. Emerg Infect Dis 2014; 20:1812–1820 [View Article]
     [Google Scholar]
  26. Moura A, Criscuolo A, Pouseele H, Maury MM, Leclercq A et al. Whole genome-based population biology and epidemiological surveillance of Listeria monocytogenes . Nat Microbiol 2016; 2:16185 [View Article]
     [Google Scholar]
  27. Jolley KA, Hill DMC, Bratcher HB, Harrison OB, Feavers IM et al. Resolution of a meningococcal disease outbreak from whole-genome sequence data with rapid web-based analysis methods. J Clin Microbiol 2012; 50:3046–3053 [View Article]
     [Google Scholar]
  28. Cody AJ, Bray JE, Jolley KA, McCarthy ND, Maiden MCJ. Core genome multilocus sequence typing scheme for stable, comparative analyses of Campylobacter jejuni and C. coli human disease isolates. J Clin Microbiol 2017; 55:2086–2097 [View Article]
     [Google Scholar]
  29. Jolley KA, Maiden MCJ. BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 2010; 11:595 [View Article]
     [Google Scholar]
  30. Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res 2018; 3:124 [View Article]
     [Google Scholar]
  31. Le Guern A-S, Martin L, Savin C, Carniel E. Yersiniosis in France: overview and potential sources of infection. Int J Infect Dis 2016; 46:1–7 [View Article]
     [Google Scholar]
  32. CDC WHO Laboratory Manual of Plague Diagnostic Tests Atlanta, GA; Geneva: Centers for Disease Control and Prevention; World Health Organization; 2000
     [Google Scholar]
  33. Criscuolo A, Brisse S. AlienTrimmer: a tool to quickly and accurately TRIM off multiple short contaminant sequences from high-throughput sequencing reads. Genomics 2013; 102:500–506 [View Article]
     [Google Scholar]
  34. Crusoe MR, Alameldin HF, Awad S, Boucher E, Caldwell A et al. The khmer software package: enabling efficient nucleotide sequence analysis. F1000Res 2015; 4:900 [View Article]
     [Google Scholar]
  35. Liu Y, Schröder J, Schmidt B. Musket: a multistage k-mer spectrum-based error corrector for Illumina sequence data. Bioinformatics 2013; 29:308–315 [View Article]
     [Google Scholar]
  36. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article]
     [Google Scholar]
  37. Haubold B, Klötzl F, Pfaffelhuber P. andi: fast and accurate estimation of evolutionary distances between closely related genomes. Bioinformatics 2015; 31:1169–1175 [View Article]
     [Google Scholar]
  38. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article]
     [Google Scholar]
  39. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article]
     [Google Scholar]
  40. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 2017; 14:587–589 [View Article]
     [Google Scholar]
  41. 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
     [Google Scholar]
  42. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389–3402 [View Article]
     [Google Scholar]
  43. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009; 10:421 [View Article]
     [Google Scholar]
  44. Konstantinidis KT, Tiedje JM. Towards a genome-based taxonomy for prokaryotes. J Bacteriol 2005; 187:6258–6264 [View Article]
     [Google Scholar]
  45. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 2016; 32:929–931 [View Article]
     [Google Scholar]
  46. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article]
     [Google Scholar]
  47. Reuter S, Connor TR, Barquist L, Walker D, Feltwell T et al. Parallel independent evolution of pathogenicity within the genus Yersinia . Proc Natl Acad Sci USA 2014; 111:6768–6773 [View Article]
     [Google Scholar]
  48. Laukkanen-Ninios R, Didelot X, Jolley KA, Morelli G, Sangal V et al. Population structure of the Yersinia pseudotuberculosis complex according to multilocus sequence typing. Environ Microbiol 2011; 13:3114–3127 [View Article]
     [Google Scholar]
  49. Achtman M, Zurth K, Morelli G, Torrea G, Guiyoule A et al. Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis . Proc Natl Acad Sci USA 1999; 96:14043–14048 [View Article]
     [Google Scholar]
  50. Bercovier H, Mollaret HH, Alonso JM, Brault J, Fanning GR et al. Intra- and interspecies relatedness of Yersinia pestis by DNA hybridization and its relationship to Yersinia pseudotuberculosis . Curr Microbiol 1980; 4:225–229 [View Article]
     [Google Scholar]
  51. Souza RA, Falcão DP, Falcão JP. Emended description of Yersinia massiliensis . Int J Syst Evol Microbiol 2011; 61:1094–1097 [View Article]
     [Google Scholar]
  52. Linde HJ, Neubauer H, Meyer H, Aleksic S, Lehn N. Identification of Yersinia species by the Vitek GNI card. J Clin Microbiol 1999; 37:211–214
     [Google Scholar]
  53. Morka K, Bystroń J, Bania J, Korzeniowska-Kowal A, Korzekwa K et al. Identification of Yersinia enterocolitica isolates from humans, pigs and wild boars by MALDI TOF MS. BMC Microbiol 2018; 18:86 [View Article]
     [Google Scholar]
  54. Bouchez V, Guglielmini J, Dazas M, Landier A, Toubiana J et al. Genomic sequencing of Bordetella pertussis for epidemiology and global surveillance of whooping cough. Emerg Infect Dis 2018; 24:988–994 [View Article]
     [Google Scholar]
  55. Martin L, Cabanel N, Lesoille C, Ménard T, Carniel E. Investigation of an unusual increase in human yersinioses in Creuse, France. Int J Infect Dis 2015; 34:76–78 [View Article]
     [Google Scholar]
  56. Saraka D, Savin C, Kouassi S, Cissé B, Koffi E et al. Yersinia enterocolitica, a neglected cause of human enteric infections in Côte d'Ivoire. PLoS Negl Trop Dis 2017; 11:e0005216 [View Article]
     [Google Scholar]
  57. Virtanen S, Laukkanen-Ninios R, Ortiz Martínez P, Siitonen A, Fredriksson-Ahomaa M et al. Multiple-locus variable-number tandem-repeat analysis in genotyping Yersinia enterocolitica strains from human and porcine origins. J Clin Microbiol 2013; 51:2154–2159 [View Article]
     [Google Scholar]
  58. Rossen JWA, Friedrich AW, Moran-Gilad J, Genomic ESG, Molecular D. Practical issues in implementing whole-genome-sequencing in routine diagnostic microbiology. Clin Microbiol Infect 2018; 24:355–360 [View Article]
     [Google Scholar]
  59. Bletz S, Mellmann A, Rothgänger J, Harmsen D. Ensuring backwards compatibility: traditional genotyping efforts in the era of whole genome sequencing. Clin Microbiol Infect 2015; 21::347.e1–347.e4 [View Article]
     [Google Scholar]
  60. van Belkum A, Tassios PT, Dijkshoorn L, Haeggman S, Cookson B et al. Guidelines for the validation and application of typing methods for use in bacterial epidemiology. Clin Microbiol Infect 2007; 13 (Suppl. 3):1–46 [View Article]
     [Google Scholar]
  61. Revez J, Espinosa L, Albiger B, Leitmeyer KC, Struelens MJ et al. Survey on the use of whole-genome sequencing for infectious diseases surveillance: rapid expansion of European national capacities, 2015–2016. Front Public Health 2017; 5:347 [View Article]
     [Google Scholar]
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Genus-wide Yersinia core-genome multilocus sequence typing for species identification and strain characterization
M Gen 5, e000301 (2019); https://doi.org/10.1099/mgen.0.000301
/content/journal/mgen/10.1099/mgen.0.000301
/content/journal/mgen/10.1099/mgen.0.000301
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