Phylogenetic comparison of enteroinvasive isolated from cases of diarrhoeal disease in England, 2005–2016 Free

Abstract

We compared the genomes of 60 isolates of enteroinvasive (EIEC) in order to better understand the step-wise evolutionary process from non-pathogenic to host-adapted pathogenic . All isolates belonged to either sequence type (ST) 6, ST99 or ST270. Each ST was located on different branches of the phylogeny and had invasion plasmids (pINVs) belonging to FII-21 (ST99, ST270), FII-27 (ST270) or FII-28 (ST6, ST270) incompatibility groups. A higher number of insertion sequence (IS) elements were identified in ST6 and ST270 than in ST99, and appeared to be driving the loss of functional genes. Comparison of the pINV from each ST revealed different degrees of gene loss, with pINV from ST270 being most similar to that found in species. We captured three EIEC STs at different stages of patho-adaptation, with ST270 being the most ‘shigella-like’ and the most divergent from non-pathogenic , and ST99 being the least divergent.

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2018-06-01
2024-03-29
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References

  1. Ewing WH. The genus Escherichia and the genus Shigella. In Edwards and Ewing’s Identification of Enterobacteriaceae, 4th ed. New York: Elsevier Science Publishing Co., Inc; 1986 pp. 93–172
    [Google Scholar]
  2. van den Beld MJ, Reubsaet FA. Differentiation between Shigella, enteroinvasive Escherichia coli (EIEC) and noninvasive Escherichia coli. Eur J Clin Microbiol Infect Dis 2012; 31:899–904 [View Article][PubMed]
    [Google Scholar]
  3. Pupo GM, Lan R, Reeves PR. Multiple independent origins of Shigella clones of Escherichia coli and convergent evolution of many of their characteristics. Proc Natl Acad Sci USA 2000; 97:10567–10572 [View Article][PubMed]
    [Google Scholar]
  4. Lan R, Alles MC, Donohoe K, Martinez MB, Reeves PR. Molecular evolutionary relationships of enteroinvasive Escherichia coli and Shigella spp. Infect Immun 2004; 72:5080–5088 [View Article][PubMed]
    [Google Scholar]
  5. Pasqua M, Michelacci V, di Martino ML, Tozzoli R, Grossi M et al. The intriguing evolutionary journey of enteroinvasive E. coli (EIEC) toward pathogenicity. Front Microbiol 2017; 8:2390 [View Article][PubMed]
    [Google Scholar]
  6. Peng J, Yang J, Jin Q. The molecular evolutionary history of Shigella spp. and enteroinvasive Escherichia coli. Infect Genet Evol 2009; 9:147–152 [View Article][PubMed]
    [Google Scholar]
  7. Lan R, Lumb B, Ryan D, Reeves PR. Molecular evolution of large virulence plasmid in Shigella clones and enteroinvasive Escherichia coli. Infect Immun 2001; 69:6303–6309 [View Article][PubMed]
    [Google Scholar]
  8. Bliven KA, Maurelli AT. Antivirulence genes: insights into pathogen evolution through gene loss. Infect Immun 2012; 80:4061–4070 [View Article][PubMed]
    [Google Scholar]
  9. Hazen TH, Leonard SR, Lampel KA, Lacher DW, Maurelli AT et al. Investigating the relatedness of enteroinvasive Escherichia coli to other E. coli and Shigella isolates by using comparative genomics. Infect Immun 2016; 84:2362–2371 [View Article][PubMed]
    [Google Scholar]
  10. Pettengill EA, Pettengill JB, Binet R. Phylogenetic analyses of Shigella and enteroinvasive Escherichia coli for the identification of molecular epidemiological markers: whole-genome comparative analysis does not support distinct genera designation. Front Microbiol 2015; 6:1573 [View Article][PubMed]
    [Google Scholar]
  11. Zuo G, Xu Z, Hao B. Shigella strains are not clones of Escherichia coli but sister species in the genus Escherichia. Genomics Proteomics Bioinformatics 2013; 11:61–65 [View Article][PubMed]
    [Google Scholar]
  12. Chattaway MA, Schaefer U, Tewolde R, Dallman TJ, Jenkins C. Identification of Escherichia coli and Shigella species from whole-genome sequences. J Clin Microbiol 2017; 55:616–623 [View Article][PubMed]
    [Google Scholar]
  13. Escher M, Scavia G, Morabito S, Tozzoli R, Maugliani A et al. A severe foodborne outbreak of diarrhoea linked to a canteen in Italy caused by enteroinvasive Escherichia coli, an uncommon agent. Epidemiol Infect 2014; 142:2559–2566 [View Article][PubMed]
    [Google Scholar]
  14. Pettengill EA, Hoffmann M, Binet R, Roberts RJ, Payne J et al. Complete genome sequence of enteroinvasive Escherichia coli O96:H19 associated with a severe foodborne outbreak. Genome Announc 2015; 3:e00883-15 [View Article][PubMed]
    [Google Scholar]
  15. Tewolde R, Dallman T, Schaefer U, Sheppard CL, Ashton P et al. MOST: a modified MLST typing tool based on short read sequencing. PeerJ 2016; 4:e2308 [View Article][PubMed]
    [Google Scholar]
  16. Joensen KG, Tetzschner AM, Iguchi A, Aarestrup FM, Scheutz F et al. Rapid and easy in silico serotyping of Escherichia coli isolates by use of whole-genome sequencing data. J Clin Microbiol 2015; 53:2410–2426 [View Article][PubMed]
    [Google Scholar]
  17. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article][PubMed]
    [Google Scholar]
  18. 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][PubMed]
    [Google Scholar]
  19. Treangen TJ, Ondov BD, Koren S, Phillippy AM. The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol 2014; 15:524 [View Article][PubMed]
    [Google Scholar]
  20. Carattoli A, Bertini A, Villa L, Falbo V, Hopkins KL et al. Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 2005; 63:219–228 [View Article][PubMed]
    [Google Scholar]
  21. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010; 5:e11147 [View Article][PubMed]
    [Google Scholar]
  22. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article][PubMed]
    [Google Scholar]
  23. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 2011; 12:402 [View Article][PubMed]
    [Google Scholar]
  24. Hawkey J, Hamidian M, Wick RR, Edwards DJ, Billman-Jacobe H et al. ISMapper: identifying transposase insertion sites in bacterial genomes from short read sequence data. BMC Genomics 2015; 16:667 [View Article][PubMed]
    [Google Scholar]
  25. Yang F, Yang J, Zhang X, Chen L, Jiang Y et al. Genome dynamics and diversity of Shigella species, the etiologic agents of bacillary dysentery. Nucleic Acids Res 2005; 33:6445–6458 [View Article][PubMed]
    [Google Scholar]
  26. Newitt S, MacGregor V, Robbins V, Bayliss L, Chattaway MA et al. Two linked enteroinvasive Escherichia coli outbreaks, Nottingham, UK, June 2014. Emerg Infect Dis 2016:1178–1184
    [Google Scholar]
  27. Yang J, Nie H, Chen L, Zhang X, Yang F et al. Revisiting the molecular evolutionary history of Shigella spp. J Mol Evol 2007; 64:71–79 [View Article][PubMed]
    [Google Scholar]
  28. Jin Q, Yuan Z, Xu J, Wang Y, Shen Y et al. Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K12 and O157. Nucleic Acids Res 2002; 30:4432–4441 [View Article][PubMed]
    [Google Scholar]
  29. Rolland K, Lambert-Zechovsky N, Picard B, Denamur E. Shigella and enteroinvasive Escherichia coli strains are derived from distinct ancestral strains of E. coli. Microbiology 1998; 144:2667–2672 [View Article][PubMed]
    [Google Scholar]
  30. Venkatesan MM, Goldberg MB, Rose DJ, Grotbeck EJ, Burland V et al. Complete DNA sequence and analysis of the large virulence plasmid of Shigella flexneri. Infect Immun 2001; 69:3271–3285 [View Article]
    [Google Scholar]
  31. Maurelli AT. Black holes, antivirulence genes, and gene inactivation in the evolution of bacterial pathogens. FEMS Microbiol Lett 2007; 267:1–8 [View Article][PubMed]
    [Google Scholar]
  32. Casalino M, Latella MC, Prosseda G, Colonna B. CadC is the preferential target of a convergent evolution driving enteroinvasive Escherichia coli toward a lysine decarboxylase-defective phenotype. Infect Immun 2003; 71:5472–5479 [View Article][PubMed]
    [Google Scholar]
  33. Michelacci V, Prosseda G, Maugliani A, Tozzoli R, Sanchez S et al. Characterization of an emergent clone of enteroinvasive Escherichia coli circulating in Europe. Clin Microbiol Infect 2016; 22:287.e11–287287 [View Article][PubMed]
    [Google Scholar]
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