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Volume 18, Number 4—April 2012

Identification of Intermediate in Evolutionary Model of Enterohemorrhagic Escherichia coli O157

Christian Jenke, Shana R. Leopold, Thomas Weniger, Jörg Rothgänger, Dag Harmsen, Helge Karch, and Alexander MellmannComments to Author 
Author affiliations: Institute for Hygiene and National Consulting Laboratory on Hemolytic Uremic Syndrome, Münster, Germany (C. Jenke, S.R. Leopold, H. Karch, A. Mellmann); University Hospital Münster Periodontology, Münster (T. Weniger, D. Harmsen); Ridom GmbH, Münster (J. Rothgänger)

Main Article


Fifty strains used for SNP typing of enterohemorrhagic Escherichia coli O157*

Strain ID Year of isolation Illness SF status and serotype Subgroup/cluster† Reference and/or GenBank accession no.
TB182A‡ 1991 D SF O55:H7 A (12)
CB9615‡ 2003 D SF O55:H7 A NC_013941
493/89‡ 1989 HUS SF O157:H B (16)
87–14‡ 1987 HUS NSF O157:H7 C1 (12)
EC4115‡ 2006 BD NSF O157:H7 C1 NC_011353
TW14359‡ 2006 BD NSF O157:H7 C1 NC_013008 (12,17)
TW14588‡ 2006 BD NSF O157:H7 C3 NZ_ABKY00000000.2
86–24‡ 1986 HUS NSF O157:H7 C2 (12)
Sakai‡ 1996 D NSF O157:H7 C3 NC_002695 (18)
EDL933‡ 1983 NA NSF O157:H7 C3 (14)
LSU-61 2001 NA SF O157:H7 Unknown intermediate (10,13)
SNPO157_01 1987 HUS NSF O157:H7 C1 This study
SNPO157_02 1988 D NSF O157:H7 C1 This study
SNPO157_03 1988 HUS SF O157:H B This study
SNPO157_04 1990 HUS NSF O157:H7 C1 This study
SNPO157_05 1991 HUS NSF O157:H C3 This study
SNPO157_06 1992 HUS NSF O157:H7 C3 This study
SNPO157_07 1993 HUS NSF O157:H7 C1 This study
SNPO157_08 1995 HUS NSF O157:H7 C1 This study
SNPO157_09 1995 HUS SF O157:H B This study
SNPO157_10 1996 HUS NSF O157:H C1 This study
SNPO157_11 1996 HUS SF O157:H B This study
SNPO157_12 1996 HUS SF O157:H B This study
SNPO157_13 1996 HUS NSF O157:H7 C1 This study
SNPO157_14 1997 HUS NSF O157:H7 C1 This study
SNPO157_15 1997 HUS NSF O157:H7 C1 This study
SNPO157_16 1998 HUS NSF O157:H7 C1 This study
SNPO157_17 1999 HUS NSF O157:H7 C1 This study
SNPO157_18 1999 HUS NSF O157:H7 C3 This study
SNPO157_19 2000 HUS NSF O157:H7 C1 This study
SNPO157_20 2000 D NSF O157:H7 C3 This study
SNPO157_21 2001 HUS SF O157:H B This study
SNPO157_22 2001 HUS NSF O157:H C3 This study
SNPO157_23 2002 D NSF O157:H7 C3 This study
SNPO157_24 2002 A NSF O157:H7 C1 This study
SNPO157_25 2003 HUS NSF O157:H7 C3 This study
SNPO157_26 2004 HUS NSF O157:H7 C1 This study
SNPO157_27 2005 HUS NSF O157:H7 C3 This study
SNPO157_28 2005 BD NSF O157:H7 C3 This study
SNPO157_29 2005 HUS NSF O157:H7 C1 This study
SNPO157_30 2006 HUS NSF O157:H7 C3 This study
SNPO157_31 2007 HUS NSF O157:H7 C3 This study
SNPO157_32 2007 HUS NSF O157:H7 C3 This study
SNPO157_33 2008 HUS NSF O157:H7 C3 This study
SNPO157_34 2008 D SF O157:H B This study
SNPO157_35 2008 HUS SF O157:H B This study
SNPO157_36 2009 D NSF O157:H7 § This study
SNPO157_37 2009 HUS SF O157:H B This study
SNPO157_38 2010 HUS NSF O157:H7 C3 This study
SNPO157_39 2010 HUS SF O157:H B This study

*All strains were isolated from humans except strain LSU-61, which was isolated from a deer (10), and EDL933, which was isolated from food (14). Strains isolated from humans were categorized into 3 subgroups (11,12); subgroup A represents isolates of serotype O55:H7, subgroup B SF O157:H– isolates, and subgroup C NSF O157:H7. Subgroup C is subdivided into clusters 1–3. SNP, single-nucleotide polymorphism; ID, identification; SF, sorbitol fermenting; D, diarrhea; HUS, hemolytic uremic syndrome; NSF, non-SF; BD, bloody diarrhea; NA, not applicable; A, asymptomatic.
†Subgroup and, if applicable, cluster designation based on 4 SNP loci (Sakai genome positions 337933, 1460599, 2370797, and 5404166) and the occupancy of potential stx integration sites in accordance with (11,12,15). Boldface indicates cluster designation of prototype strains.
‡Strains were analyzed in silico.
§SNP pattern for NSF O157:H7 grouping resulted in an unknown combination.

Main Article

  1. Holtz  LR, Neill  MA, Tarr  PI. Acute bloody diarrhea: a medical emergency for patients of all ages. Gastroenterology. 2009;136:188798. DOIPubMedGoogle Scholar
  2. Levine  MM. Escherichia coli that cause diarrhea: enterotoxigenic, enteropathogenic, enteroinvasive, enterohemorrhagic, and enteroadherent. J Infect Dis. 1987;155:37789. DOIPubMedGoogle Scholar
  3. Tarr  PI, Gordon  CA, Chandler  WL. Shiga toxin–producing Escherichia coli and haemolytic uraemic syndrome. Lancet. 2005;365:107386. DOIPubMedGoogle Scholar
  4. Karch  H, Tarr  PI, Bielaszewska  M. Enterohaemorrhagic Escherichia coli in human medicine. Int J Med Microbiol. 2005;295:40518. DOIPubMedGoogle Scholar
  5. Karch  H, Bielaszewska  M. Sorbitol-fermenting Shiga toxin–producing Escherichia coli O157:H– strains: epidemiology, phenotypic and molecular characteristics, and microbiological diagnosis. J Clin Microbiol. 2001;39:20439. DOIPubMedGoogle Scholar
  6. Karch  H, Mellmann  A, Bielaszewska  M. Epidemiology and pathogenesis of enterohaemorrhagic Escherichia coli. Berl Munch Tierarztl Wochenschr. 2009;122:41724.PubMedGoogle Scholar
  7. Pennington  H. Escherichia coli O157. Lancet. 2010;376:142835. DOIPubMedGoogle Scholar
  8. Werber  D, Bielaszewska  M, Frank  C, Stark  K, Karch  H. Watch out for the even eviler cousin—sorbitol-fermenting E coli O157. Lancet. 2011;377:2989. DOIPubMedGoogle Scholar
  9. Feng  P, Lampel  KA, Karch  H, Whittam  TS. Genotypic and phenotypic changes in the emergence of Escherichia coli O157:H7. J Infect Dis. 1998;177:17503. DOIPubMedGoogle Scholar
  10. Feng  PCH, Monday  SR, Lacher  DW, Allison  L, Siitonen  A, Keys  C, Genetic diversity among clonal lineages within Escherichia coli O157:H7 stepwise evolutionary model. Emerg Infect Dis. 2007;13:17016.PubMedGoogle Scholar
  11. Shaikh  N, Tarr  PI. Escherichia coli O157:H7 Shiga toxin–encoding bacteriophages: integrations, excisions, truncations, and evolutionary implications. J Bacteriol. 2003;185:3596605. DOIPubMedGoogle Scholar
  12. Leopold  SR, Magrini  V, Holt  NJ, Shaikh  N, Mardis  ER, Cagno  J, A precise reconstruction of the emergence and constrained radiations of Escherichia coli O157 portrayed by backbone concatenomic analysis. Proc Natl Acad Sci U S A. 2009;106:87138.PubMedGoogle Scholar
  13. Dunn  JR, Keen  JE, Moreland  D, Alex  T. Prevalence of Escherichia coli O157:H7 in white-tailed deer from Louisiana. J Wildl Dis. 2004;40:3615.PubMedGoogle Scholar
  14. Perna  NT, Plunkett  G III, Burland  V, Mau  B, Glasner  JD, Rose  DJ, Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature. 2001;409:52933. DOIPubMedGoogle Scholar
  15. Shaikh  N, Holt  NJ, Johnson  JR, Tarr  PI. Fim operon variation in the emergence of enterohemorrhagic Escherichia coli: an evolutionary and functional analysis. FEMS Microbiol Lett. 2007;273:5863. DOIPubMedGoogle Scholar
  16. Karch  H, Wiss  R, Gloning  H, Emmrich  P, Aleksic  S, Bockemühl  J. Hemolytic-uremic syndrome in infants due to verotoxin-producing Escherichia coli [in German]. Dtsch Med Wochenschr. 1990;115:48995. DOIPubMedGoogle Scholar
  17. Kulasekara  BR, Jacobs  M, Zhou  Y, Wu  Z, Sims  E, Saenphimmachak  C, Analysis of the genome of the Escherichia coli O157:H7 2006 spinach-associated outbreak isolate indicates candidate genes that may enhance virulence. Infect Immun. 2009;77:371321. DOIPubMedGoogle Scholar
  18. Hayashi  T, Makino  K, Ohnishi  M, Kurokawa  K, Ishii  K, Yokoyama  K, Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12. DNA Res. 2001;8:1122. DOIPubMedGoogle Scholar
  19. Jenke  C, Harmsen  D, Weniger  T, Rothgänger  J, Hyytiä-Trees  E, Bielaszewska  M, Phylogenetic analysis of enterohemorrhagic Escherichia coli O157, Germany, 1987–2008. Emerg Infect Dis. 2010;16:6106.PubMedGoogle Scholar
  20. Friedrich  AW, Bielaszewska  M, Zhang  W, Pulz  M, Kuczius  T, Ammon  A, Escherichia coli harboring Shiga toxin 2 gene variants: frequency and association with clinical symptoms. J Infect Dis. 2002;185:7484. DOIPubMedGoogle Scholar
  21. Mellmann  A, Bielaszewska  M, Zimmerhackl  LB, Prager  R, Harmsen  D, Tschäpe  H, Enterohemorrhagic Escherichia coli in human infection: in vivo evolution of a bacterial pathogen. Clin Infect Dis. 2005;41:78592. DOIPubMedGoogle Scholar
  22. Prager  R, Strutz  U, Fruth  A, Tschäpe  H. Subtyping of pathogenic Escherichia coli strains using flagellar (H)-antigens: serotyping versus fliC polymorphisms. Int J Med Microbiol. 2003;292:47786. DOIPubMedGoogle Scholar
  23. Sonntag  AK, Prager  R, Bielaszewska  M, Zhang  W, Fruth  A, Tschäpe  H, Phenotypic and genotypic analyses of enterohemorrhagic Escherichia coli O145 strains from patients in Germany. J Clin Microbiol. 2004;42:95462. DOIPubMedGoogle Scholar
  24. Zhang  Y, Laing  C, Steele  M, Ziebell  K, Johnson  R, Benson  AK, Genome evolution in major Escherichia coli O157:H7 lineages. BMC Genomics. 2007;8:121. DOIPubMedGoogle Scholar
  25. Wilson  K. Preparation of genomic DNA from bacteria. Curr Protoc Mol Biol. 2001;Chapter 2:Unit 2.4.
  26. Wirth  T, Falush  D, Lan  R, Colles  F, Mensa  P, Wieler  LH, Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol. 2006;60:113651. DOIPubMedGoogle Scholar
  27. Dugan  KA, Lawrence  HS, Hares  DR, Fisher  CL, Budowle  B. An improved method for post-PCR purification for mtDNA sequence analysis. J Forensic Sci. 2002;47:8118.PubMedGoogle Scholar
  28. Rump  LV, Strain  EA, Cao  G, Allard  MW, Fischer  M, Brown  EW, Draft genome sequences of six Escherichia coli isolates from the stepwise model emergence of Escherichia coli O157:H7. J Bacteriol. 2011;193:20589. DOIPubMedGoogle Scholar
  29. Besser  TE, Shaikh  N, Holt  NJ, Tarr  PI, Konkel  ME, Malik-Kale  P, Greater diversity of Shiga toxin–encoding bacteriophage insertion sites among Escherichia coli O157:H7 isolates from cattle than in those from humans. Appl Environ Microbiol. 2007;73:6719. DOIPubMedGoogle Scholar
  30. Bielaszewska  M, Prager  R, Zhang  W, Friedrich  AW, Mellmann  A, Tschäpe  H, Chromosomal dynamism in progeny of outbreak-related sorbitol-fermenting enterohemorrhagic Escherichia coli O157:NM. Appl Environ Microbiol. 2006;72:19009. DOIPubMedGoogle Scholar
  31. García-Sánchez  A, Sanchez  S, Rubio  R, Pereira  G, Alonso  JM, Hermoso de Mendoza  J, Presence of Shiga toxin–producing E. coli O157:H7 in a survey of wild artiodactyls. Vet Microbiol. 2007;121:3737. DOIPubMedGoogle Scholar
  32. Díaz  S, Vidal  D, Herrera-Leon  S, Sanchez  S. Sorbitol-fermenting, β-glucuronidase–positive, Shiga toxin–negative Escherichia coli O157:H7 in free-ranging red deer in south-central Spain. Foodborne Pathog Dis. 2011;8:13135. DOIPubMedGoogle Scholar
  33. Lacher  DW, Steinsland  H, Blank  TE, Donnenberg  MS, Whittam  TS. Molecular evolution of typical enteropathogenic Escherichia coli: clonal analysis by multilocus sequence typing and virulence gene allelic profiling. J Bacteriol. 2007;189:34250. DOIPubMedGoogle Scholar
  34. Bielaszewska  M, Köck  R, Friedrich  AW, von Eiff  C, Zimmerhackl  LB, Karch  H, Shiga toxin–mediated hemolytic uremic syndrome: time to change the diagnostic paradigm? PLoS ONE. 2007;2:e1024. DOIPubMedGoogle Scholar
  35. Mellmann  A, Lu  S, Karch  H, Xu  J, Harmsen  D, Schmidt  MA, Recycling of Shiga toxin 2 genes in sorbitol-fermenting enterohemorrhagic Escherichia coli O157:NM. Appl Environ Microbiol. 2008;74:6772. DOIPubMedGoogle Scholar
  36. Manning  SD, Motiwala  AS, Springman  AC, Qi  W, Lacher  DW, Ouellette  LM, Variation in virulence among clades of Escherichia coli O157:H7 associated with disease outbreaks. Proc Natl Acad Sci U S A. 2008;105:486873. DOIPubMedGoogle Scholar
  37. Zhang  W, Qi  W, Albert  TJ, Motiwala  AS, Alland  D, Hyytiä-Trees  EK, Probing genomic diversity and evolution of Escherichia coli O157 by single nucleotide polymorphisms. Genome Res. 2006;16:75767. DOIPubMedGoogle Scholar

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Page updated: March 19, 2012
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