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Abstract

A key virulence factor of enterohaemorrhagic Escherichia coli (EHEC) is the bacteriophage-encoded Shiga toxin (Stx). Stxs are classified into two types, Stx1 and Stx2, and Stx2-producing strains are thought to cause more severe infections than strains producing only Stx1. Although O26 : H11 is the second most prevalent EHEC following O157 : H7, the majority of O26 : H11 strains produce Stx1 alone. However, Stx2-producing O26 strains have increasingly been detected worldwide. Through a large-scale genome analysis, we present a global phylogenetic overview and evolutionary timescale for E. coli O26 : H11. The origin of O26 has been estimated to be 415 years ago. Sequence type 21C1 (ST21C1), one of the two sublineages of ST21, the most predominant O26 : H11 lineage worldwide, emerged 213 years ago from one of the three ST29 sublineages (ST29C2). The other ST21 lineage (ST21C2) emerged 95 years ago from ST21C1. Increases in population size occurred in the late 20th century for all of the O26 lineages, but most remarkably for ST21C2. Analysis of the distribution of stx2-positive strains revealed the recent and repeated acquisition of the stx2 gene in multiple lineages of O26, both in ST21 and ST29. Other major EHEC virulence genes, such as type III secretion system effector genes and plasmid-encoded virulence genes, were well conserved in ST21 compared to ST29. In addition, more antimicrobial-resistance genes have accumulated in the ST21C1 lineage. Although current attention is focused on several highly virulent ST29 clones that have acquired the stx2 gene, there is also a considerable risk that the ST21 lineage could yield highly virulent clones.

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2017-11-21
2024-12-09
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References

  1. Tarr PI, Gordon CA, Chandler WL. Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet 2005; 365:1073–1086 [View Article][PubMed]
    [Google Scholar]
  2. Caprioli A, Morabito S, Brugère H, Oswald E. Enterohaemorrhagic Escherichia coli: emerging issues on virulence and modes of transmission. Vet Res 2005; 36:289–311 [View Article][PubMed]
    [Google Scholar]
  3. Croxen MA, Law RJ, Scholz R, Keeney KM, Wlodarska M et al. Recent advances in understanding enteric pathogenic Escherichia coli . Clin Microbiol Rev 2013; 26:822–880 [View Article][PubMed]
    [Google Scholar]
  4. Boerlin P, Mcewen SA, Boerlin-Petzold F, Wilson JB, Johnson RP et al. Associations between virulence factors of Shiga toxin-producing Escherichia coli and disease in humans. J Clin Microbiol 1999; 37:497–503[PubMed]
    [Google Scholar]
  5. Tobe T, Beatson SA, Taniguchi H, Abe H, Bailey CM et al. An extensive repertoire of type III secretion effectors in Escherichia coli O157 and the role of lambdoid phages in their dissemination. Proc Natl Acad Sci USA 2006; 103:14941–14946 [View Article][PubMed]
    [Google Scholar]
  6. Ogura Y, Ooka T, Iguchi A, Toh H, Asadulghani M et al. Comparative genomics reveal the mechanism of the parallel evolution of O157 and non-O157 enterohemorrhagic Escherichia coli . Proc Natl Acad Sci USA 2009; 106:17939–17944 [View Article][PubMed]
    [Google Scholar]
  7. Abu-Ali GS, Lacher DW, Wick LM, Qi W, Whittam TS. Genomic diversity of pathogenic Escherichia coli of the EHEC 2 clonal complex. BMC Genomics 2009; 10:296 [View Article][PubMed]
    [Google Scholar]
  8. Reid SD, Herbelin CJ, Bumbaugh AC, Selander RK, Whittam TS. Parallel evolution of virulence in pathogenic Escherichia coli . Nature 2000; 406:64–67 [View Article][PubMed]
    [Google Scholar]
  9. Elliott EJ, Robins-Browne RM, O'Loughlin EV, Bennett-Wood V, Bourke J et al. Nationwide study of haemolytic uraemic syndrome: clinical, microbiological, and epidemiological features. Arch Dis Child 2001; 85:125–131 [View Article][PubMed]
    [Google Scholar]
  10. European Food Safety Authority and European Centre for Disease Prevention and Control The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2015. EFSA Journal 2016; 14:4634
    [Google Scholar]
  11. Terajima J, Iyoda S, Ohnishi M, Watanabe H. Shiga toxin (verotoxin)-producing Escherichia coli in Japan. Microbiol Spectr 2014; 2: [View Article][PubMed]
    [Google Scholar]
  12. Brooks JT, Sowers EG, Wells JG, Greene KD, Griffin PM et al. Non-O157 Shiga toxin-producing Escherichia coli infections in the United States, 1983–2002. J Infect Dis 2005; 192:1422–1429 [View Article][PubMed]
    [Google Scholar]
  13. Gerber A, Karch H, Allerberger F, Verweyen HM, Zimmerhackl LB. Clinical course and the role of shiga toxin-producing Escherichia coli infection in the hemolytic-uremic syndrome in pediatric patients, 1997–2000, in Germany and Austria: a prospective study. J Infect Dis 2002; 186:493–500 [View Article][PubMed]
    [Google Scholar]
  14. Pollock KG, Bhojani S, Beattie TJ, Allison L, Hanson M et al. Highly virulent Escherichia coli O26, Scotland. Emerg Infect Dis 2011; 17:1777–1779 [View Article][PubMed]
    [Google Scholar]
  15. Buvens G, Piérard D. Virulence profiling and disease association of verocytotoxin-producing Escherichia coli O157 and non-O157 isolates in Belgium. Foodborne Pathog Dis 2012; 9:530–535 [View Article][PubMed]
    [Google Scholar]
  16. Jelacic JK, Damrow T, Chen GS, Jelacic S, Bielaszewska M et al. Shiga toxin-producing Escherichia coli in Montana: bacterial genotypes and clinical profiles. J Infect Dis 2003; 188:719–729 [View Article][PubMed]
    [Google Scholar]
  17. Allerberger F, Friedrich AW, Grif K, Dierich MP, Dornbusch HJ et al. Hemolytic-uremic syndrome associated with enterohemorrhagic Escherichia coli O26:H infection and consumption of unpasteurized cow's milk. Int J Infect Dis 2003; 7:42–45 [View Article][PubMed]
    [Google Scholar]
  18. Ishijima N, Lee KI, Kuwahara T, Nakayama-Imaohji H, Yoneda S et al. Identification of a new virulent clade in enterohemorrhagic Escherichia coli O26:H11/H- sequence type 29. Sci Rep 2017; 7:43136 [View Article][PubMed]
    [Google Scholar]
  19. Käppeli U, Hächler H, Giezendanner N, Beutin L, Stephan R. Human infections with non-O157 Shiga toxin-producing Escherichia coli, Switzerland, 2000–2009. Emerg Infect Dis 2011; 17:180–185 [View Article][PubMed]
    [Google Scholar]
  20. Misselwitz J, Karch H, Bielazewska M, John U, Ringelmann F et al. Cluster of hemolytic-uremic syndrome caused by Shiga toxin-producing Escherichia coli O26:H11. Pediatr Infect Dis J 2003; 22:349–354 [View Article][PubMed]
    [Google Scholar]
  21. Bielaszewska M, Mellmann A, Bletz S, Zhang W, Köck R et al. Enterohemorrhagic Escherichia coli O26:H11/H-: a new virulent clone emerges in Europe. Clin Infect Dis 2013; 56:1373–1381 [View Article][PubMed]
    [Google Scholar]
  22. Ison SA, Delannoy S, Bugarel M, Nagaraja TG, Renter DG et al. Targeted amplicon sequencing for single-nucleotide-polymorphism genotyping of attaching and effacing Escherichia coli O26:H11 cattle strains via a high-throughput library preparation technique. Appl Environ Microbiol 2015; 82:640–649 [View Article][PubMed]
    [Google Scholar]
  23. Zhang WL, Bielaszewska M, Liesegang A, Tschäpe H, Schmidt H et al. Molecular characteristics and epidemiological significance of Shiga toxin-producing Escherichia coli O26 strains. J Clin Microbiol 2000; 38:2134–2140[PubMed]
    [Google Scholar]
  24. Eichhorn I, Heidemanns K, Semmler T, Kinnemann B, Mellmann A et al. Highly virulent non-O157 enterohemorrhagic Escherichia coli (EHEC) serotypes reflect similar phylogenetic lineages, providing new insights into the evolution of EHEC. Appl Environ Microbiol 2015; 81:7041–7047 [View Article][PubMed]
    [Google Scholar]
  25. Ferdous M, Friedrich AW, Grundmann H, de Boer RF, Croughs PD et al. Molecular characterization and phylogeny of Shiga toxin-producing Escherichia coli isolates obtained from two Dutch regions using whole genome sequencing. Clin Microbiol Infect 2016; 22:642.e1–642.e9 [View Article][PubMed]
    [Google Scholar]
  26. Januszkiewicz A, Wołkowicz T, Chróst A, Szych J. Characterization of the Shiga toxin-producing Escherichia coli O26 isolated from human in Poland between 1996 and 2014. Lett Appl Microbiol 2015; 60:605–608 [View Article][PubMed]
    [Google Scholar]
  27. Delannoy S, Mariani-Kurkdjian P, Bonacorsi S, Liguori S, Fach P. Characteristics of emerging human-pathogenic Escherichia coli O26:H11 strains isolated in France between 2010 and 2013 and carrying the stx2d gene only. J Clin Microbiol 2015; 53:486–492 [View Article][PubMed]
    [Google Scholar]
  28. Zweifel C, Cernela N, Stephan R. Detection of the emerging Shiga toxin-producing Escherichia coli O26:H11/H- sequence type 29 (ST29) clone in human patients and healthy cattle in Switzerland. Appl Environ Microbiol 2013; 79:5411–5413 [View Article][PubMed]
    [Google Scholar]
  29. Gonzalez-Escalona N, Toro M, Rump LV, Cao G, Nagaraja TG et al. Virulence gene profiles and clonal relationships of Escherichia coli O26:H11 isolates from feedlot cattle as determined by whole-genome sequencing. Appl Environ Microbiol 2016; 82:3900–3912 [View Article][PubMed]
    [Google Scholar]
  30. Ison SA, Delannoy S, Bugarel M, Nightingale KK, Webb HE et al. Genetic diversity and pathogenic potential of attaching and effacing Escherichia coli O26:H11 strains recovered from bovine feces in the United States. Appl Environ Microbiol 2015; 81:3671–3678 [View Article][PubMed]
    [Google Scholar]
  31. Bletz S, Bielaszewska M, Leopold SR, Köck R, Witten A et al. Evolution of enterohemorrhagic Escherichia coli O26 based on single-nucleotide polymorphisms. Genome Biol Evol 2013; 5:1807–1816 [View Article][PubMed]
    [Google Scholar]
  32. Bonanno L, Loukiadis E, Mariani-Kurkdjian P, Oswald E, Garnier L et al. Diversity of Shiga toxin-producing Escherichia coli (STEC) O26:H11 strains examined via stx subtypes and insertion sites of stx and espk bacteriophages. Appl Environ Microbiol 2015; 81:3712–3721 [View Article][PubMed]
    [Google Scholar]
  33. Krüger A, Lucchesi PM, Sanso AM, Etcheverría AI, Bustamante AV et al. Genetic characterization of Shiga toxin-producing Escherichia coli O26:H11 strains isolated from animal, food, and clinical samples. Front Cell Infect Microbiol 2015; 5:74 [View Article][PubMed]
    [Google Scholar]
  34. Leomil L, Pestana de Castro AF, Krause G, Schmidt H, Beutin L. Characterization of two major groups of diarrheagenic Escherichia coli O26 strains which are globally spread in human patients and domestic animals of different species. FEMS Microbiol Lett 2005; 249:335–342 [View Article][PubMed]
    [Google Scholar]
  35. Norman KN, Clawson ML, Strockbine NA, Mandrell RE, Johnson R et al. Comparison of whole genome sequences from human and non-human Escherichia coli O26 strains. Front Cell Infect Microbiol 2015; 5:21 [View Article][PubMed]
    [Google Scholar]
  36. Kajitani R, Toshimoto K, Noguchi H, Toyoda A, Ogura Y et al. Efficient de novo assembly of highly heterozygous genomes from whole-genome shotgun short reads. Genome Res 2014; 24:1384–1395 [View Article][PubMed]
    [Google Scholar]
  37. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M et al. Versatile and open software for comparing large genomes. Genome Biol 2004; 5:R12 [View Article][PubMed]
    [Google Scholar]
  38. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 2015; 43:e15 [View Article][PubMed]
    [Google Scholar]
  39. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006; 22:2688–2690 [View Article][PubMed]
    [Google Scholar]
  40. Letunic I, Bork P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 2007; 23:127–128 [View Article][PubMed]
    [Google Scholar]
  41. Cheng L, Connor TR, Sirén J, Aanensen DM, Corander J. Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Mol Biol Evol 2013; 30:1224–1228 [View Article][PubMed]
    [Google Scholar]
  42. Rambaut A, Lam TT, Max Carvalho L, Pybus OG. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol 2016; 2::vew007 [View Article][PubMed]
    [Google Scholar]
  43. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012; 29:1969–1973 [View Article][PubMed]
    [Google Scholar]
  44. Suchard MA, Rambaut A. Many-core algorithms for statistical phylogenetics. Bioinformatics 2009; 25:1370–1376 [View Article][PubMed]
    [Google Scholar]
  45. Duchêne S, Holt KE, Weill FX, Le Hello S, Hawkey J et al. Genome-scale rates of evolutionary change in bacteria. Microb Genom 2016; 2:e000094 [View Article][PubMed]
    [Google Scholar]
  46. Murray GG, Wang F, Harrison EM, Paterson GK, Mather AE et al. The effect of genetic structure on molecular dating and tests for temporal signal. Methods Ecol Evol 2016; 7:80–89 [View Article][PubMed]
    [Google Scholar]
  47. Ooka T, Seto K, Kawano K, Kobayashi H, Etoh Y et al. Clinical significance of Escherichia albertii . Emerg Infect Dis 2012; 18:488–492 [View Article][PubMed]
    [Google Scholar]
  48. Scheutz F, Teel LD, Beutin L, Piérard D, Buvens G et al. Multicenter evaluation of a sequence-based protocol for subtyping Shiga toxins and standardizing Stx nomenclature. J Clin Microbiol 2012; 50:2951–2963 [View Article][PubMed]
    [Google Scholar]
  49. Schmidt H, Beutin L, Karch H. Molecular analysis of the plasmid-encoded hemolysin of Escherichia coli O157:H7 strain EDL 933. Infect Immun 1995; 63:1055–1061[PubMed]
    [Google Scholar]
  50. Brunder W, Schmidt H, Karch H. KatP, a novel catalase-peroxidase encoded by the large plasmid of enterohaemorrhagic Escherichia coli O157:H7. Microbiology 1996; 142:3305–3315 [View Article][PubMed]
    [Google Scholar]
  51. Brunder W, Schmidt H, Frosch M, Karch H. The large plasmids of Shiga-toxin-producing Escherichia coli (STEC) are highly variable genetic elements. Microbiology 1999; 145:1005–1014 [View Article][PubMed]
    [Google Scholar]
  52. Schmidt H, Henkel B, Karch H. A gene cluster closely related to type II secretion pathway operons of Gram-negative bacteria is located on the large plasmid of enterohemorrhagic Escherichia coli O157 strains. FEMS Microbiol Lett 1997; 148:265–272 [View Article][PubMed]
    [Google Scholar]
  53. Inouye M, Dashnow H, Raven LA, Schultz MB, Pope BJ et al. SRST2: rapid genomic surveillance for public health and hospital microbiology labs. Genome Med 2014; 6:90 [View Article][PubMed]
    [Google Scholar]
  54. Kim J, Nietfeldt J, Benson AK. Octamer-based genome scanning distinguishes a unique subpopulation of Escherichia coli O157:H7 strains in cattle. Proc Natl Acad Sci USA 1999; 96:13288–13293 [View Article][PubMed]
    [Google Scholar]
  55. Zhang Y, Laing C, Steele M, Ziebell K, Johnson R et al. Genome evolution in major Escherichia coli O157:H7 lineages. BMC Genomics 2007; 8:121 [View Article][PubMed]
    [Google Scholar]
  56. Lupolova N, Dallman TJ, Matthews L, Bono JL, Gally DL. Support vector machine applied to predict the zoonotic potential of E. coli O157 cattle isolates. Proc Natl Acad Sci USA 2016; 113:11312–11317 [View Article][PubMed]
    [Google Scholar]
  57. Ben Zakour NL, Alsheikh-Hussain AS, Ashcroft MM, Khanh Nhu NT, Roberts LW et al. Sequential acquisition of virulence and fluoroquinolone resistance has shaped the evolution of Escherichia coli ST131. MBio 2016; 7:e0034700316 [View Article][PubMed]
    [Google Scholar]
  58. Dallman TJ, Ashton PM, Byrne L, Perry NT, Petrovska L et al. Applying phylogenomics to understand the emergence of Shiga-toxin-producing Escherichia coli O157:H7 strains causing severe human disease in the UK. Microb Genom 2015; 1:e000029 [View Article][PubMed]
    [Google Scholar]
  59. Lenski RE, Winkworth CL, Riley MA. Rates of DNA sequence evolution in experimental populations of Escherichia coli during 20,000 generations. J Mol Evol 2003; 56:498–508 [View Article][PubMed]
    [Google Scholar]
  60. Guttman DS, Dykhuizen DE. Clonal divergence in Escherichia coli as a result of recombination, not mutation. Science 1994; 266:1380–1383 [View Article][PubMed]
    [Google Scholar]
  61. Ogura Y, Mondal SI, Islam MR, Mako T, Arisawa K et al. The Shiga toxin 2 production level in enterohemorrhagic Escherichia coli O157:H7 is correlated with the subtypes of toxin-encoding phage. Sci Rep 2015; 5:16663 [View Article][PubMed]
    [Google Scholar]
  62. Arenas-Hernández MM, Martínez-Laguna Y, Torres AG. Clinical implications of enteroadherent Escherichia coli . Curr Gastroenterol Rep 2012; 14:386–394 [View Article][PubMed]
    [Google Scholar]
  63. Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R et al. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis 2016; 16:161–168 [View Article][PubMed]
    [Google Scholar]
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