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Volume 5, Issue 5

Emergence and divergence of major lineages of Shiga-toxin-producing Escherichia coli in Australia Open Access

Abstract

Shiga-toxin-producing Escherichia coli (STEC) infection is an important global cause of foodborne disease. To date however, genomics-based studies of STEC have been predominately focused upon STEC collected in the Northern Hemisphere. Here, we demonstrate the population structure of 485 STEC isolates in Australia, and show that several clonal groups (CGs) common to Australia were infrequently detected in a representative selection of contemporary STEC genomes from around the globe. Further, phylogenetic analysis demonstrated that lineage II of the global O157:H7 STEC was most prevalent in Australia, and was characterized by a frameshift mutation in flgF, resulting in the H-non-motile phenotype. Strong concordance between in silico and phenotypic serotyping was observed, along with concordance between in silico and conventional detection of stx genes. These data represent the most comprehensive STEC analysis from the Southern Hemisphere, and provide a framework for future national genomics-based surveillance of STEC in Australia.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): enteric pathogens , epidemiology , evolution , genomic epidemiology and STEC
© 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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2019-05-20
2024-04-26
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References

  1. Kirk MD, Pires SM, Black RE, Caipo M, Crump JA et al. World health organization estimates of the global and regional disease burden of 22 foodborne bacterial, protozoal, and viral diseases, 2010: a data synthesis. PLoS Med 2015; 12:e1001921–1
     [Google Scholar]
  2. 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]
     [Google Scholar]
  3. Ford L, Kirk M, Glass K, Hall G. Sequelae of foodborne illness caused by 5 pathogens, Australia, circa 2010. Emerg Infect Dis 2014; 20:1865–1871 [View Article]
     [Google Scholar]
  4. Lynn RM, O'Brien SJ, Taylor CM, Adak GK, Chart H et al. Childhood hemolytic uremic syndrome, United Kingdom and ireland. Emerg Infect Dis 2005; 11:590–596 [View Article]
     [Google Scholar]
  5. Butcher H, Elson R, Chattaway MA, Featherstone CA, Willis C et al. Whole genome sequencing improved case ascertainment in an outbreak of shiga toxin-producing Escherichia coli O157 associated with raw drinking milk. Epidemiol Infect 2016; 144:2812–2823 [View Article]
     [Google Scholar]
  6. Michino H, Araki K, Minami S, Takaya S, Sakai N et al. Massive outbreak of Escherichia coli O157:H7 infection in schoolchildren in Sakai City, Japan, associated with consumption of white radish sprouts. Am J Epidemiol 1999; 150:787–796 [View Article]
     [Google Scholar]
  7. Karmali MA. Infection by Shiga toxin-producing Escherichia coli: an overview. Mol Biotechnol 2004; 26:117–122 [View Article]
     [Google Scholar]
  8. Frank C, Faber MS, Askar M, Bernard H, Fruth A et al. Large and ongoing outbreak of haemolytic uraemic syndrome, Germany, may 2011. Euro Surveill 2011; 16:
     [Google Scholar]
  9. Rasko DA, Webster DR, Sahl JW, Bashir A, Boisen N et al. Origins of the E. coli strain causing an outbreak of hemolytic-uremic syndrome in Germany. N Engl J Med 2011; 365:709–717 [View Article]
     [Google Scholar]
  10. Dallman TJ, Byrne L, Ashton PM, Cowley LA, Perry NT et al. Whole-genome sequencing for national surveillance of Shiga toxin-producing Escherichia coli O157. Clin Infect Dis 2015; 61:305–312 [View Article]
     [Google Scholar]
  11. Holmes A, Allison L, Ward M, Dallman TJ, Clark R et al. Utility of whole-genome sequencing of Escherichia coli O157 for outbreak detection and epidemiological surveillance. J Clin Microbiol 2015; 53:3565–3573 [View Article]
     [Google Scholar]
  12. Ingle DJ, Holt KE, Levine MM, Kuzevski A, Valcanis M et al. In silico serotyping of E. coli from short read data identifies limited novel O-loci but extensive diversity of O:H serotype combinations within and between pathogenic lineages. Microb Genom 2016; 2:1–14 [View Article]
     [Google Scholar]
  13. Jenkins C, Joensen KG, Tetzschner AMM, Iguchi A, Aarestrup FM, Scheutz F. Whole-genome sequencing data for serotyping Escherichia coli-It's time for a change!. J Clin Microbiol 2015; 53:2402–2403 [View Article]
     [Google Scholar]
  14. Lindsey RL, Pouseele H, Chen JC, Strockbine NA, Carleton HA. Implementation of whole genome sequencing (WGS) for identification and characterization of Shiga toxin-producing Escherichia coli (STEC) in the United States. Front Microbiol 2016; 7:457–459 [View Article]
     [Google Scholar]
  15. Mellor GE, Fegan N, Gobius KS, Smith HV, Jennison AV et al. Geographically distinct Escherichia coli O157 isolates differ by lineage, Shiga toxin genotype, and total shiga toxin production. J Clin Microbiol 2015; 53:579–586 [View Article]
     [Google Scholar]
  16. National notifiable disease surveillance system. Available at http://www9.health.gov.au/cda/source/cda-index.cfm 1st November, 2018
    [Google Scholar]
  17. Motarjemi Y, Moy G, Todd ECD. Encyclopedia of Food Safety Elsevier, Academic Press; 2014
     [Google Scholar]
  18. Vasant BR, Stafford RJ, Jennison AV, Bennett SM, Bell RJ et al. Mild illness during outbreak of Shiga toxin-producing Escherichia coli O157 infections associated with agricultural show, Australia. Emerg Infect Dis 2017; 23:1686–1689 [View Article]
     [Google Scholar]
  19. Dallman TJ, Ashton PM, Byrne L, Perry NT, Petrovska L, Allison L, Gally DL, Wain J 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; 1:1–13 [View Article]
     [Google Scholar]
  20. Manning SD, Motiwala AS, Springman AC, Qi W, Lacher DW et al. Variation in virulence among clades of Escherichia coli O157:H7 associated with disease outbreaks. Proc Natl Acad Sci U S A 2008; 105:4868–4873 [View Article]
     [Google Scholar]
  21. 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]
     [Google Scholar]
  22. Chandler ME, Bettelheim KA. A rapid method of identifying Escherichia coli H antigens. Zentralbl Bakteriol Orig A 1974; 229:74–79
     [Google Scholar]
  23. Paton AW, Paton JC. Detection and characterization of Shiga toxigenic Escherichia coli by using multiplex PCR assays for stx1, stx2, eaeA, enterohemorrhagic E. coli hlyA, rfbO111, and rfbO157. J Clin Microbiol 1998; 36:598–602
     [Google Scholar]
  24. 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]
  25. Wirth T, Falush D, Lan R, Colles F, Mensa P et al. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 2006; 60:1136–1151 [View Article]
     [Google Scholar]
  26. Wickham H. ggplot2: Elegant Graphics for Data Analysis Cham: Springer International Publishing; 2016
     [Google Scholar]
  27. Eaves DJ, Randall L, Gray DT, Buckley A, Woodward MJ et al. Prevalence of mutations within the quinolone resistance-determining region of gyrA, gyrB, parC, and parE and association with antibiotic resistance in quinolone-resistant Salmonella enterica. Antimicrob Agents Chemother 2004; 48:4012–4015 [View Article]
     [Google Scholar]
  28. Inouye M, Dashnow H, Raven L-A, Schultz MB, Pope BJ et al. SRST2: rapid genomic surveillance for public health and hospital microbiology Labs. Genome Med 2014; 6:1–16 [View Article]
     [Google Scholar]
  29. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin Minchin PR, OHara RB et al. 2015; vegan: community ecology package [Internet]. Available from http://CRAN.R-project.org/package=vegan
     [Google Scholar]
  30. Ashton PM, Perry N, Ellis R, Petrovska L, Wain J et al. Insight into shiga toxin genes encoded by Escherichia coli O157 from whole genome sequencing. PeerJ 2015; 3:e739–16 [View Article]
     [Google Scholar]
  31. Hunt M, Mather AE, Sánchez-Busó L, Page AJ, Parkhill J et al. ARIBA: rapid antimicrobial resistance genotyping directly from sequencing reads. Microb Genom 2017; 3:1–21 [View Article]
     [Google Scholar]
  32. Iguchi A, Iyoda S, Kikuchi T, Ogura Y, Katsura K et al. A complete view of the genetic diversity of the Escherichia coli O-antigen biosynthesis gene cluster. DNA Res 2015; 22:101–107 [View Article]
     [Google Scholar]
  33. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article]
     [Google Scholar]
  34. Li H, Durbin R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 2010; 26:589–595 [View Article]
     [Google Scholar]
  35. Garrison E, Marth G. Haplotype-based variant detection from short-read sequencing. arXiv 20121–9
     [Google Scholar]
  36. Arndt D, Grant JR, Marcu A, Sajed T, Pon A et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 2016; 44:W16–W21 [View Article]
     [Google Scholar]
  37. Nguyen L-T, 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]
  38. Minh BQ, Nguyen MAT, von Haeseler A, Haeseler von A. Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 2013; 30:1188–1195 [View Article]
     [Google Scholar]
  39. Pommier T, Canbäck B, Lundberg P, Hagström Åke, Tunlid A. RAMI: a tool for identification and characterization of phylogenetic clusters in microbial communities. Bioinformatics 2009; 25:736–742 [View Article]
     [Google Scholar]
  40. 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:e15–5 [View Article]
     [Google Scholar]
  41. 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:vew007–7vew007 [View Article]
     [Google Scholar]
  42. Yu G, Smith DK, Zhu H, Guan Y, TT-Y L. ggtree: an rpackage for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 2016; 8(1:28–36
     [Google Scholar]
  43. Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H et al. Beast 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 2014; 10:e1003537–6 [View Article]
     [Google Scholar]
  44. Duchêne S, Holt KE, Weill F-X, Le Hello S, Hawkey J et al. Genome-scale rates of evolutionary change in bacteria. Microb Genom 2016; 2:1–12 [View Article]
     [Google Scholar]
  45. Yokoyama E, Hirai S, Hashimoto R, Uchimura M. Clade analysis of enterohemorrhagic Escherichia coli serotype O157:H7/H- strains and hierarchy of their phylogenetic relationships. Infection, Genetics and Evolution 2012; 12:1724–1728 [View Article]
     [Google Scholar]
  46. Iyoda S, Manning SD, Seto K, Kimata K, Isobe J et al. Phylogenetic clades 6 and 8 of enterohemorrhagic Escherichia coli O157:H7 with particular stx subtypes are more frequently found in isolates from hemolytic uremic syndrome patients than from asymptomatic carriers. Open Forum Infect Dis 2014; 1:ofu061 [View Article]
     [Google Scholar]
  47. Carver T, Berriman M, Tivey A, Patel C, Böhme U et al. Artemis and act: viewing, annotating and comparing sequences stored in a relational database. Bioinformatics 2008; 24:2672–2676 [View Article]
     [Google Scholar]
  48. 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; 16:1–11 [View Article]
     [Google Scholar]
  49. Pintara AP, Guglielmino CJD, Rathnayake IU, Huygens F, Jennison AV. Molecular prediction of the O157:H-negative phenotype prevalent in Australian shiga toxin-producing Escherichia coli cases improves concordance of InSilico serotyping with phenotypic motility. J Clin Microbiol 2018; 56:e01906–17–8 [View Article]
     [Google Scholar]
  50. Schimmer B, Nygard K, Eriksen H-M, Lassen J, Lindstedt B-A et al. Outbreak of haemolytic uraemic syndrome in Norway caused by stx 2-positive Escherichia coli O103:H25 traced to cured mutton sausages. BMC Infect Dis 2008; 8:1073–10 [View Article]
     [Google Scholar]
  51. von Mentzer A, Connor TR, Wieler LH, Semmler T, Iguchi A et al. Identification of enterotoxigenic Escherichia coli (ETEC) clades with long-term global distribution. Nat Genet 2014; 46:1321–1326 [View Article]
     [Google Scholar]
  52. Wick RR, Schultz MB, Zobel J, Holt KE. Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 2015; 31:3350–3352 [View Article]
     [Google Scholar]
  53. Vally H, Hall G, Dyda A, Raupach J, Knope K et al. Epidemiology of shiga toxin producing Escherichia coli in Australia, 2000-2010. BMC Public Health 2012; 12:63 [View Article]
     [Google Scholar]
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Emergence and divergence of major lineages of Shiga-toxin-producing Escherichia coli in Australia
M Gen 5, e000268 (2019); https://doi.org/10.1099/mgen.0.000268
/content/journal/mgen/10.1099/mgen.0.000268
/content/journal/mgen/10.1099/mgen.0.000268
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