1887

Abstract

Verotoxigenic (VTEC) are food- and water-borne pathogens associated with both sporadic illness and outbreaks of enteric disease. While it is known that cattle are reservoirs of VTEC, little is known about the genomic variation of VTEC in cattle, and whether the variation in genomes reported for human outbreak strains is consistent with individual animal or group/herd sources of infection. A previous study of VTEC prevalence identified serotypes carried persistently by three consecutive cohorts of heifers within a closed herd of cattle. This present study aimed to: (i) determine whether the genomic relatedness of bovine isolates is similar to that reported for human strains associated with single source outbreaks, (ii) estimate the rates of genome change among dominant serotypes over time within a cattle herd, and (iii) identify genomic features of serotypes associated with persistence in cattle. Illumina MiSeq genome sequencing and genotyping based on allelic and single nucleotide variations were completed, while genome change over time was measured using Bayesian evolutionary analysis sampling trees. The accessory genome, including the non-protein-encoding intergenic regions (IGRs), virulence factors, antimicrobial-resistance genes and plasmid gene content of representative persistent and sporadic cattle strains were compared using Fisher’s exact test corrected for multiple comparisons. Herd strains from serotypes O6:H34 (=22), O22:H8 (=30), O108:H8 (=39), O139:H19 (=44) and O157:H7 (=106) were readily distinguishable from epidemiologically unrelated strains of the same serotype using a similarity threshold of 10 or fewer allele differences between adjacent nodes. Temporal-cohort clustering within each serotype was supported by date randomization analysis. Substitutions per site per year were consistent with previously reported values for ; however, there was low branch support for these values. Acquisition of the phage-encoded Shiga toxin 2 gene in serotype O22:H8 was observed. Pan-genome analyses identified accessory regions that were more prevalent in persistent serotypes (≤0.05) than in sporadic serotypes. These results suggest that VTEC serotypes from a specific cattle population are highly clonal with a similar level of relatedness as human single-source outbreak-associated strains, but changes in the genome occur gradually over time. Additionally, elements in the accessory genomes may provide a selective advantage for persistence of VTEC within cattle herds.

Funding
This study was supported by the:
  • Government of Canada Genomics and Research Development Initiative
    • Principle Award Recipient: Not Applicable
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
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2020-06-04
2021-10-24
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References

  1. Bettelheim KA. The non-O157 Shiga-toxigenic (verocytotoxigenic) Escherichia coli; under-rated pathogens. Crit Rev Microbiol 2007; 33:67–87
    [Google Scholar]
  2. 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
    [Google Scholar]
  3. Chattaway MA, Dallman TJ, Gentle A, Wright MJ, Long SE et al. Whole genome sequencing for public health surveillance of Shiga toxin-producing Escherichia coli other than serogroup O157. Front Microbiol 2016; 7:258
    [Google Scholar]
  4. 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; 7:766
    [Google Scholar]
  5. Holmes A, Dallman TJ, Shabaan S, Hanson M, Allison L. Validation of whole-genome sequencing for identification and characterization of Shiga toxin-producing Escherichia coli to produce standardized data to enable data sharing. J Clin Microbiol 2018; 56:e01388-17 [View Article][PubMed]
    [Google Scholar]
  6. Lüth S, Kleta S, Al Dahouk S. Whole genome sequencing as a typing tool for foodborne pathogens like Listeria monocytogenes – the way towards global harmonisation and data exchange. Trends Food Sci Technol 2018; 73:67–75
    [Google Scholar]
  7. Grad YH, Lipsitch M, Feldgarden M, Arachchi HM, Cerqueira GC et al. Genomic epidemiology of the Escherichia coli O104:H4 outbreaks in Europe, 2011. Proc Natl Acad Sci USA 2012; 109:3065–3070
    [Google Scholar]
  8. Rumore J, Tschetter L, Kearney A, Kandar R, McCormick R et al. Evaluation of whole-genome sequencing for outbreak detection of verotoxigenic Escherichia coli O157:H7 from the Canadian perspective. BMC Genomics 2018; 19:870
    [Google Scholar]
  9. Jenkins C, Dallman TJ, Grant KA. Impact of whole genome sequencing on the investigation of food-borne outbreaks of Shiga toxin-producing Escherichia coli serogroup O157:H7, England, 2013 to 2017. Euro Surveill 2019; 24:1800346 [View Article]
    [Google Scholar]
  10. Joensen KG, Scheutz F, Lund O, Hasman H, Kaas RS et al. Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J Clin Microbiol 2014; 52:1501–1510
    [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
    [Google Scholar]
  12. Mikhail AFW, Jenkins C, Dallman TJ, Inns T, Douglas A et al. An outbreak of Shiga toxin-producing Escherichia coli O157:H7 associated with contaminated salad leaves: epidemiological, genomic and food trace back investigations. Epidemiol Infect 2018; 146:187–196
    [Google Scholar]
  13. Orsi RH, Borowsky ML, Lauer P, Young SK, Nusbaum C et al. Short-term genome evolution of Listeria monocytogenes in a non-controlled environment. BMC Genomics 2008; 9:539
    [Google Scholar]
  14. Haugum K, Johansen J, Gabrielsen C, Brandal LT, Bergh K et al. Comparative genomics to delineate pathogenic potential in non-O157 Shiga toxin-producing Escherichia coli (STEC) from patients with and without haemolytic uremic syndrome (HUS) in Norway. PLoS One 2014; 9:e111788
    [Google Scholar]
  15. 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]
  16. Dekker JP, Frank KM. Next-generation epidemiology: using real-time core genome multilocus sequence typing to support infection control policy. J Clin Microbiol 2016; 54:2850–2853
    [Google Scholar]
  17. Roer L, Hansen F, Thomsen MCF, Knudsen JD, Hansen DS et al. WGS-based surveillance of third-generation cephalosporin-resistant Escherichia coli from bloodstream infections in Denmark. J Antimicrob Chemother 2017; 72:1922–1929
    [Google Scholar]
  18. Underwood AP, Dallman T, Thomson NR, Williams M, Harker K et al. Public health value of next-generation DNA sequencing of enterohemorrhagic Escherichia coli isolates from an outbreak. J Clin Microbiol 2013; 51:232–237
    [Google Scholar]
  19. Schürch AC, Arredondo-Alonso S, Willems RJL, Goering RV. Whole genome sequencing options for bacterial strain typing and epidemiologic analysis based on single nucleotide polymorphism versus gene-by-gene–based approaches. Clin Microbiol Infect 2018; 24:350–354
    [Google Scholar]
  20. 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
    [Google Scholar]
  21. 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
    [Google Scholar]
  22. Bettelheim KA, Goldwater PN. Serotypes of non-O157 shigatoxigenic Escherichia coli (STEC). Adv Microbiol 2014; 4:377–389
    [Google Scholar]
  23. Duchêne S, Holt KE, Weill F, Le Hello S, Hawkey J et al. Genome-scale rates of evolutionary change in bacteria. Microb Genom. 2016; 2:e000094
    [Google Scholar]
  24. Casali N, Broda A, Harris SR, Parkhill J, Brown T et al. Whole genome sequence analysis of a large isoniazid-resistant tuberculosis outbreak in London: a retrospective observational study. PLoS Med 2016; 13:e1002137
    [Google Scholar]
  25. Kennemann L, Didelot X, Aebischer T, Kuhn S, Drescher B et al. Helicobacter pylori genome evolution during human infection. Proc Natl Acad Sci USA 2011; 108:5033–5038
    [Google Scholar]
  26. 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
    [Google Scholar]
  27. Holt KE, Thieu Nga TV, Pham Thanh D, Vinh H, Kim DW et al. Tracking the establishment of local endemic populations of an emergent enteric pathogen. Proc Natl Acad Sci USA 2013; 110:17522–17527
    [Google Scholar]
  28. Stoesser N, Sheppard AE, Pankhurst L, De Maio N, Moore CE et al. Evolutionary history of the global emergence of the Escherichia coli epidemic clone ST131. mBio 2016; 7:e02162
    [Google Scholar]
  29. Larsen MH, Dalmasso M, Ingmer H, Langsrud S, Malakauskas M et al. Persistence of foodborne pathogens and their control in primary and secondary food production chains. Food Control 2014; 44:92–109
    [Google Scholar]
  30. Stasiewicz MJ, Oliver HF, Wiedmann M, den Bakker HC. Whole-genome sequencing allows for improved identification of persistent Listeria monocytogenes in food-associated environments. Appl Environ Microbiol 2015; 81:6024–6037
    [Google Scholar]
  31. Malley TJV, Butts J, Wiedmann M. Seek and destroy process: Listeria monocytogenes process controls in the ready-to-eat meat and poultry industry. J Food Prot 2015; 78:436–445 [View Article][PubMed]
    [Google Scholar]
  32. Beutin L, Geier D, Zimmermann S, Aleksic S, Gillespie HA et al. Epidemiological relatedness and clonal types of natural populations of Escherichia coli strains producing Shiga toxins in separate populations of cattle and sheep. Appl Environ Microbiol 1997; 63:2175–2180
    [Google Scholar]
  33. Shere JA, Bartlett KJ, Kaspar CW. Longitudinal study of Escherichia coli O157:H7 dissemination on four dairy farms in Wisconsin. Appl Environ Microbiol 1998; 64:1390–1399 [View Article][PubMed]
    [Google Scholar]
  34. Gannon VPJ, Graham TA, King R, Michel P, Read S et al. Escherichia coli O157:H7 infection in cows and calves in a beef cattle herd in Alberta, Canada. Epidemiol Infect 2002; 129:163–172 [View Article][PubMed]
    [Google Scholar]
  35. Carlson BA, Nightingale KK, Mason GL, Ruby JR, Choat WT et al. Escherichia coli O157:H7 strains that persist in feedlot cattle are genetically related and demonstrate an enhanced ability to adhere to intestinal epithelial cells. Appl Environ Microbiol 2009; 75:5927–5937 [View Article][PubMed]
    [Google Scholar]
  36. Barth SA, Menge C, Eichhorn I, Semmler T, Wieler LH et al. The accessory genome of Shiga toxin-producing Escherichia coli defines a persistent colonization type in cattle. Appl Environ Microbiol 2016; 82:5455–5464 [View Article][PubMed]
    [Google Scholar]
  37. Buchanan CJ, Webb AL, Mutschall SK, Kruczkiewicz P, Barker DOR et al. A genome-wide association study to identify diagnostic markers for human pathogenic Campylobacter jejuni strains. Front Microbiol 2017; 8:1224 [View Article][PubMed]
    [Google Scholar]
  38. Lewis BB, Carter RA, Ling L, Leiner I, Taur Y et al. Pathogenicity locus, core genome, and accessory gene contributions to Clostridium difficile virulence. mBio 2017; 8:e00885-17 [View Article][PubMed]
    [Google Scholar]
  39. Wang LYR, Jokinen CC, Laing CR, Johnson RP, Ziebell K et al. Multi-year persistence of verotoxigenic Escherichia coli (VTEC) in a closed Canadian beef herd: a cohort study. Front Microbiol 2018; 9:2040
    [Google Scholar]
  40. Matthews TC, Bristow FR, Griffiths EJ, Petkau A, Adam J et al. The integrated rapid infectious disease analysis (IRIDA) platform. bioRxiv 2018381830 [View Article]
    [Google Scholar]
  41. Seemann T, Kwong J, Gladman S, da Silva AG. Shovill, version 1.0.1 2018 https://github.com/tseemann/shovill
  42. 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
    [Google Scholar]
  43. Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH et al. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol 2016; 17:132
    [Google Scholar]
  44. Li H. Seqtk: toolkit for processing sequences in FASTA/Q formats 2012
  45. Deorowicz S, Kokot M, Grabowski S, Debudaj-Grabysz A. KMC 2: fast and resource-frugal k-mer counting. Bioinformatics 2015; 31:1569–1576
    [Google Scholar]
  46. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120
    [Google Scholar]
  47. Song L, Florea L, Langmead B. Lighter: fast and memory-efficient sequencing error correction without counting. Genome Biol 2014; 15:509
    [Google Scholar]
  48. Magoč T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 2011; 27:2957–2963
    [Google Scholar]
  49. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence alignment MAP format and SAMtools. Bioinformatics 2009; 25:2078–2079
    [Google Scholar]
  50. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM 2013 https://arxiv.org/abs/1303.3997
  51. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963
    [Google Scholar]
  52. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595
    [Google Scholar]
  53. Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH et al. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res 2017; 27:722–736
    [Google Scholar]
  54. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359
    [Google Scholar]
  55. Hunt M, Silva ND, Otto TD, Parkhill J, Keane JA et al. Circlator: automated circularization of genome assemblies using long sequencing reads. Genome Biol 2015; 16:294
    [Google Scholar]
  56. Le KK, Whiteside MD, Hopkins JE, Gannon VPJ, Laing CR. Spfy: an integrated graph database for real-time prediction of bacterial phenotypes and downstream comparative analyses. Database 2018; 2018:bay086 [View Article][PubMed]
    [Google Scholar]
  57. Rambaut A. FigTree, version 1.4.3 2016
  58. Letunic I, Bork P. Interactive tree of life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 2007; 23:127–128
    [Google Scholar]
  59. Laing C, Buchanan C, Taboada EN, Zhang Y, Kropinski A et al. Pan-genome sequence analysis using Panseq: an online tool for the rapid analysis of core and accessory genomic regions. BMC Bioinformatics 2010; 11:461
    [Google Scholar]
  60. Franz E, Rotariu O, Lopes BS, MacRae M, Bono JL et al. Phylogeographic analysis reveals multiple international transmission events have driven the global emergence of Escherichia coli O157:H7. Clin Infect Dis 2018; 69:428–437
    [Google Scholar]
  61. Guindon S, Lethiec F, Duroux P, Gascuel O. PHYML online – a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 2005; 33:W557–559
    [Google Scholar]
  62. Petkau A, Mabon P, Sieffert C, Knox NC, Cabral J et al. SNVPhyl: a single nucleotide variant phylogenomics pipeline for microbial genomic epidemiology. Microb Genom 2017; 3:e000116
    [Google Scholar]
  63. 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
    [Google Scholar]
  64. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012; 29:1969–1973
    [Google Scholar]
  65. Rambaut A, Drummond AJ. LogCombiner, version 1.8.2 2015 http://beast.bio.ed.ac.uk
  66. Rambaut A, Suchard MA, Xie W, Drummond AJ. Tracer: MCMC trace analysis tool, version 1.7.0 2013 http://beast.bio.ed.ac.uk
  67. Rambaut A, Drummond AJ. TreeAnnotator: MCMC output analysis, version 1.8.4 2015 http://beast.bio.ed.ac.uk
  68. Seemann T. ABRicate: mass screening of contigs for antimicrobial resistance or virulence genes, version 0.7 2017 https://github.com/tseemann/abricate
  69. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069
    [Google Scholar]
  70. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693
    [Google Scholar]
  71. Brynildsrud O, Bohlin J, Scheffer L, Eldholm V. Rapid scoring of genes in microbial pan-genome-wide association studies with Scoary. Genome Biol 2016; 17:238
    [Google Scholar]
  72. Stothard P, Grant JR, Van Domselaar G. Visualizing and comparing circular genomes using the CGView family of tools. Brief Bioinform 2019; 20:1576–1582 [View Article]
    [Google Scholar]
  73. Thorpe HA, Bayliss SC, Sheppard SK, Feil EJ. Piggy: a rapid, large-scale pan-genome analysis tool for intergenic regions in bacteria. Gigascience 2018; 7:giy015 [View Article]
    [Google Scholar]
  74. Kruczkiewicz P. Genome Fisher 2013 https://bitbucket.org/peterk87/genomefisher
  75. Soon JM, Chadd SA, Baines RN. Escherichia coli O157:H7 in beef cattle: on farm contamination and pre-slaughter control methods. Anim Health Res Rev 2011; 12:197–211
    [Google Scholar]
  76. CDC Multistate outbreak of listeriosis linked to soft cheeses distributed by Karoun Dairies, Inc. (final update). Atlanta, GA: CDC; 2015. https://www.cdc.gov/listeria/outbreaks/soft-cheeses-09-15/.
  77. Schmid D, Allerberger F, Huhulescu S, Pietzka A, Amar C et al. Whole genome sequencing as a tool to investigate a cluster of seven cases of listeriosis in Austria and Germany, 2011–2013. Clin Microbiol Infect 2014; 20:431–436
    [Google Scholar]
  78. Jackson BR, Tarr C, Strain E, Jackson KA, Conrad A et al. Implementation of nationwide real-time whole-genome sequencing to enhance listeriosis outbreak detection and investigation. Clin Infect Dis 2016; 63:380–386
    [Google Scholar]
  79. Kleta S, Hammerl JA, Dieckmann R, Malorny B, Borowiak M et al. Molecular tracing to find source of protracted invasive listeriosis outbreak, southern Germany, 2012–2016. Emerg Infect Dis 2017; 23:1680–1683
    [Google Scholar]
  80. Goering RV, Köck R, Grundmann H, Werner G, Friedrich AW et al. From theory to practice: molecular strain typing for the clinical and public health setting. Euro Surveill 2013; 18:20383 [View Article][PubMed]
    [Google Scholar]
  81. 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][PubMed]
    [Google Scholar]
  82. Akiba M, Sameshima T, Nakazawa M. Clonal turnover of enterohemorrhagic Escherichia coli O157:H7 in experimentally infected cattle. FEMS Microbiol Lett 2000; 184:79–83 [View Article][PubMed]
    [Google Scholar]
  83. Cobbold R, Desmarchelier P. Characterisation and clonal relationships of Shiga-toxigenic Escherichia coli (STEC) isolated from Australian dairy cattle. Vet Microbiol 2001; 79:323–335 [View Article][PubMed]
    [Google Scholar]
  84. Schouten JM, Graat EAM, Frankena K, van de Giessen AW, van der Zwaluw WK et al. A longitudinal study of Escherichia coli O157 in cattle of a Dutch dairy farm and in the farm environment. Vet Microbiol 2005; 107:193–204 [View Article][PubMed]
    [Google Scholar]
  85. Cobbaut K, Houf K, Boyen F, Haesebrouck F, De Zutter L. Genotyping and antimicrobial resistance patterns of Escherichia coli O157 originating from cattle farms. Foodborne Pathog Dis 2011; 8:719–724 [View Article][PubMed]
    [Google Scholar]
  86. Joris M-A, Verstraete K, De Reu K, De Zutter L. Longitudinal follow-up of the persistence and dissemination of EHEC on cattle farms in Belgium. Foodborne Pathog Dis 2013; 10:295–301 [View Article][PubMed]
    [Google Scholar]
  87. Yoshii N, Ogura Y, Hayashi T, Ajiro T, Sameshima T et al. Pulsed-field gel electrophoresis profile changes resulting from spontaneous chromosomal deletions in enterohemorrhagic Escherichia coli O157:H7 during passage in cattle. Appl Environ Microbiol 2009; 75:5719–5726
    [Google Scholar]
  88. Faith NG, Shere JA, Brosch R, Arnold KW, Ansay SE et al. Prevalence and clonal nature of Escherichia coli O157:H7 on dairy farms in Wisconsin. Appl Environ Microbiol 1996; 62:1519–1525
    [Google Scholar]
  89. Geue L, Klare S, Schnick C, Mintel B, Meyer K et al. Analysis of the clonal relationship of serotype O26:H11 enterohemorrhagic Escherichia coli Isolates from Cattle. Appl Environ Microbiol 2009; 75:6947–6953
    [Google Scholar]
  90. Geue L, Schares S, Mintel B, Conraths FJ, Müller E et al. Rapid microarray-based genotyping of enterohemorrhagic Escherichia coli serotype O156:H25/H-/Hnt isolates from cattle and clonal relationship analysis. Appl Environ Microbiol 2010; 76:55105519 [View Article][PubMed]
    [Google Scholar]
  91. Cadona JS, Bustamante AV, González J, Sanso AM. Genetic relatedness and novel sequence types of non-O157 Shiga toxin-producing Escherichia coli strains isolated in Argentina. Front Cell Infect Microbiol 2016; 6:93
    [Google Scholar]
  92. Bentancor A, Rumi MV, Gentilini MV, Sardoy C, Irino K et al. Shiga toxin-producing and attaching and effacing Escherichia coli in cats and dogs in a high hemolytic uremic syndrome incidence region in Argentina. FEMS Microbiol Lett 2007; 267:251–256
    [Google Scholar]
  93. Menrath A, Wieler LH, Heidemanns K, Semmler T, Fruth A et al. Shiga toxin producing Escherichia coli: identification of non-O157:H7-super-shedding cows and related risk factors. Gut Pathog 2010; 2:7 [View Article][PubMed]
    [Google Scholar]
  94. Blanco J, Blanco M, Blanco JE, Mora A, González EA et al. Verotoxin-producing Escherichia coli in Spain: prevalence, serotypes, and virulence genes of O157:H7 and non-O157 VTEC in ruminants, raw beef products, and humans. Exp Biol Med 2003; 228:345–351 [View Article][PubMed]
    [Google Scholar]
  95. Tozzoli R, Grande L, Michelacci V, Ranieri P, Maugliani A et al. Shiga toxin-converting phages and the emergence of new pathogenic Escherichia coli: a world in motion. Front Cell Infect Microbiol 2014; 4:80
    [Google Scholar]
  96. Santiviago CA, Toro CS, Bucarey SA, Mora GC. A chromosomal region surrounding the ompD porin gene marks a genetic difference between Salmonella typhi and the majority of Salmonella serovars. Microbiology 2001; 147:1897–1907 [View Article][PubMed]
    [Google Scholar]
  97. Lee DR, Schnaitman CA. Comparison of outer membrane porin proteins produced by Escherichia coli and Salmonella typhimurium. J Bacteriol 1980; 142:1019–1022 [View Article][PubMed]
    [Google Scholar]
  98. Felczak MM, Kaguni JM. The rcbA gene product reduces spontaneous and induced chromosome breaks in Escherichia coli. J Bacteriol 2012; 194:2152–2164 [View Article]
    [Google Scholar]
  99. Soo VWC, Hanson-Manful P, Patrick WM. Artificial gene amplification reveals an abundance of promiscuous resistance determinants in Escherichia coli. Proc Natl Acad Sci USA 2011; 108:1484–1489 [View Article][PubMed]
    [Google Scholar]
  100. Masuda N, Church GM. Regulatory network of acid resistance genes in Escherichia coli. Mol Microbiol 2003; 48:699–712 [View Article]
    [Google Scholar]
  101. Di Masi DR, White JC, Schnaitman CA, Bradbeer C. Transport of vitamin B12 in Escherichia coli: common receptor sites for vitamin B12 and the E colicins on the outer membrane of the cell envelope. J Bacteriol 1973; 115:506–513 [View Article][PubMed]
    [Google Scholar]
  102. Bradbeer C, Woodrow ML. Transport of vitamin B12 in Escherichia coli: energy dependence. J Bacteriol 1976; 128:99–104 [View Article][PubMed]
    [Google Scholar]
  103. Segura A, Auffret P, Bibbal D, Bertoni M, Durand A et al. Factors involved in the persistence of a Shiga toxin-producing Escherichia coli O157:H7 strain in bovine feces and gastro-intestinal content. Front Microbiol 2018; 9:375 [View Article][PubMed]
    [Google Scholar]
  104. Potter AA, Klashinsky S, Li Y, Frey E, Townsend H et al. Decreased shedding of Escherichia coli O157:H7 by cattle following vaccination with type III secreted proteins. Vaccine 2004; 22:362–369 [View Article]
    [Google Scholar]
  105. Geue L, Segura-Alvarez M, Conraths FJ, Kuczius T, Bockemühl J et al. A long-term study on the prevalence of Shiga toxin-producing Escherichia coli (STEC) on four German cattle farms. Epidemiol Infect 2002; 129:173–185 [View Article]
    [Google Scholar]
  106. Geue L, Selhorst T, Schnick C, Mintel B, Conraths FJ. Analysis of the clonal relationship of Shiga toxin-producing Escherichia coli serogroup O165:H25 isolated from cattle. Appl Environ Microbiol 2006; 72:2254–2259 [View Article]
    [Google Scholar]
  107. Rice DH, McMenamin KM, Pritchett LC, Hancock DD, Besser TE. Genetic subtyping of Escherichia coli O157 isolates from 41 Pacific Northwest USA cattle farms. Epidemiol Infect 1999; 122:479–484 [View Article]
    [Google Scholar]
  108. Ahrenfeldt J, Skaarup C, Hasman H, Pedersen AG, Aarestrup FM et al. Bacterial whole genome-based phylogeny: construction of a new benchmarking dataset and assessment of some existing methods. BMC Genomics 2017; 18:19 [View Article]
    [Google Scholar]
  109. Zhou W, Nielsen JB, Fritsche LG, Dey R, Gabrielsen ME et al. Efficiently controlling for case-control imbalance and sample relatedness in large-scale genetic association studies. Nat Genet 2018; 50:1335–1341 [View Article][PubMed]
    [Google Scholar]
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