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Volume 16, Number 4—April 2010
Research

Phylogenetic Analysis of Enterohemorrhagic Escherichia coli O157, Germany, 1987–2008

Christian Jenke, Dag Harmsen, Thomas Weniger, Jörg Rothgänger, Eija Hyytiä-Trees, Martina Bielaszewska, Helge Karch, and Alexander MellmannComments to Author 
Author affiliations: Institute for Hygiene, Münster, Germany (C. Jenke, M. Bielaszewska, H. Karch, A. Mellmann); Department of Periodontology, Münster (D. Harmsen, T. Weniger); Ridom GmbH, Würzburg, Germany (J. Rothgänger); Centers for Disease Control and Prevention, Atlanta, Georgia, USA (E. Hyytiä-Trees)

Main Article

Table 1

VNTR characteristics of enterohemorrhagic Escherichia coli, Germany, 1987–2008*

VNTR locus Alternative name† Repeat length, bp Inside ORF (no.)‡ No. repeats
No. alleles§ Null alleles Null allele frequency, % ID Typeability, %¶
Minimum Maximum
3 Vhec3, TR5 6 + (Z0268) 3 23 22 + 2.0 0.86 98.0
34 Vhec2, TR6 18 + (Z5865) 4 12 8 0.66 100.0
9 Vhec4, TR1 6 + (Z3935/Z3936) 6 23 15 + 31.7 0.90 68.3
25 TR4 6 2 15 6 0.74 100.0
17 TR3 6 + (Z5935) 2 19 10 0.80 100.0
19 TR7 6 + (Z3274) 3 11 9 0.76 100.0
36# Vhec7 7 3 15 13 + 44.1 0.87 55.9
37# 6 + (L7083) 3 17 11 + 2.0 0.82 98.0

*VNTR, variable number tandem repeat; ORF, open reading frame; ID, index of diversity without null alleles.
†Vhec loci as explained by Lindstedt et al. (15). TR loci are from Noller et al. (14).
‡Number is based on current EDL933 genome data. ORF encoding VNTR loci encoded either hypothetical proteins or proteins with unknown function.
§Including null alleles.
¶Typeability determines the proportion of all alleles without null alleles.
#Located on plasmid pO157 of reference strain EDL933.

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References
  1. Tarr  PI, Gordon  CA, Chandler  WL. Shiga toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet. 2005;365:107386.PubMedGoogle Scholar
  2. Holtz  LR, Neill  MA, Tarr  PI. Acute bloody diarrhea: a medical emergency for patients of all ages. Gastroenterology. 2009;136:188798. DOIPubMedGoogle Scholar
  3. Levine  MM. Escherichia coli that cause diarrhea: enterotoxigenic, enteropathogenic, enteroinvasive, enterohemorrhagic, and enteroadherent. J Infect Dis. 1987;155:37789.PubMedGoogle Scholar
  4. Williams  DM, Sreedhar  SS, Mickell  JJ, Chan  JCM. Acute kidney failure: a pediatric experience over 20 years. Arch Pediatr Adolesc Med. 2002;156:893900.PubMedGoogle Scholar
  5. Karch  H, Tarr  PI, Bielaszewska  M. Enterohaemorrhagic Escherichia coli in human medicine. Int J Med Microbiol. 2005;295:40518. DOIPubMedGoogle Scholar
  6. Swaminathan  B, Barrett  TJ, Hunter  SB, Tauxe  RV. PulseNet: the molecular subtyping network for foodborne bacterial disease surveillance, United States. Emerg Infect Dis. 2001;7:3829.PubMedGoogle Scholar
  7. Lindstedt  BA. Multiple-locus variable number tandem repeats analysis for genetic fingerprinting of pathogenic bacteria. Electrophoresis. 2005;26:256782. DOIPubMedGoogle Scholar
  8. Hyytiä-Trees  E, Smole  SC, Fields  PA, Swaminathan  B, Ribot  EM. Second generation subtyping: a proposed PulseNet protocol for multiple-locus variable-number tandem repeat analysis of Shiga toxin–producing Escherichia coli O157 (STEC O157). Foodborne Pathog Dis. 2006;3:11831. DOIPubMedGoogle Scholar
  9. Murchan  S, Kaufmann  ME, Deplano  A, de Ryck  R, Struelens  M, Zinn  CE, Harmonization of pulsed-field gel electrophoresis protocols for epidemiological typing of strains of methicillin-resistant Staphylococcus aureus: a single approach developed by consensus in 10 European laboratories and its application for tracing the spread of related strains. J Clin Microbiol. 2003;41:157485. DOIPubMedGoogle Scholar
  10. Tenover  FC, Arbeit  R, Archer  G, Biddle  J, Byrne  S, Goering  R, Comparison of traditional and molecular methods of typing isolates of Staphylococcus aureus. J Clin Microbiol. 1994;32:40715.PubMedGoogle Scholar
  11. Frothingham  R. Differentiation of strains in Mycobacterium tuberculosis complex by DNA sequence polymorphisms, including rapid identification of M. bovis BCG. J Clin Microbiol. 1995;33:8404.PubMedGoogle Scholar
  12. Supply  P, Allix  C, Lesjean  S, Cardoso-Oelemann  M, Rusch-Gerdes  S, Willery  E, Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis. J Clin Microbiol. 2006;44:4498510. DOIPubMedGoogle Scholar
  13. van Belkum  A. Tracing isolates of bacterial species by multilocus variable number of tandem repeat analysis (MLVA). FEMS Immunol Med Microbiol. 2007;49:227. DOIPubMedGoogle Scholar
  14. Noller  AC, McEllistrem  MC, Pacheco  AGF, Boxrud  DJ, Harrison  LH. Multilocus variable-number tandem repeat analysis distinguishes outbreak and sporadic Escherichia coli O157:H7 isolates. J Clin Microbiol. 2003;41:538997. DOIPubMedGoogle Scholar
  15. Lindstedt  BA, Heir  E, Gjernes  E, Vardund  T, Kapperud  G. DNA fingerprinting of Shiga-toxin producing Escherichia coli O157 based on multiple-locus variable-number tandem-repeats analysis (MLVA). Ann Clin Microbiol Antimicrob. 2003;2:12. DOIPubMedGoogle Scholar
  16. Supply  P, Warren  RM, Banuls  A, Lesjean  S, Van Der Spuy  GD, Lewis  L, Linkage disequilibrium between minisatellite loci supports clonal evolution of Mycobacterium tuberculosis in a high tuberculosis incidence area. Mol Microbiol. 2003;47:52938. DOIPubMedGoogle Scholar
  17. Wirth  T, Hildebrand  F, Allix-Beguec  C, Wolbeling  F, Kubica  T, Kremer  K, Origin, spread and demography of the Mycobacterium tuberculosis complex. PLoS Pathog. 2008;4:e1000160. DOIPubMedGoogle Scholar
  18. Helgason  E, Tourasse  NJ, Meisal  R, Caugant  DA, Kolsto  A. Multilocus sequence typing scheme for bacteria of the Bacillus cereus group. Appl Environ Microbiol. 2004;70:191201. DOIPubMedGoogle Scholar
  19. Maiden  MC, Bygraves  JA, Feil  E, Morelli  G, Russell  JE, Urwin  R, Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A. 1998;95:31405. DOIPubMedGoogle Scholar
  20. Feil  EJ. Small change: keeping pace with microevolution. Nat Rev Microbiol. 2004;2:48395. DOIPubMedGoogle Scholar
  21. Noller  AC, McEllistrem  MC, Stine  OC, Morris  JGJ, Boxrud  DJ, Dixon  B, Multilocus sequence typing reveals a lack of diversity among Escherichia coli O157:H7 isolates that are distinct by pulsed-field gel electrophoresis. J Clin Microbiol. 2003;41:6759. DOIPubMedGoogle Scholar
  22. 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
  23. Hyytiä-Trees  E, Lafon  P, Vauterin  P, Ribot  E. Multilaboratory validation study of standardized multiple-locus variable-number tandem repeat analysis protocol for Shiga toxin–producing Escherichia coli O157: a novel approach to normalize fragment size data between capillary electrophoresis platform. Foodborne Pathog Dis. 2009; Sep):28.[Epub ahead of print].
  24. Karch  H, Heesemann  J, Laufs  R, O’Brien  AD, Tacket  CO, Levine  MM. A plasmid of enterohemorrhagic Escherichia coli O157:H7 is required for expression of a new fimbrial antigen and for adhesion to epithelial cells. Infect Immun. 1987;55:45561.PubMedGoogle Scholar
  25. Karch  H, Wiss  R, Gloning  H, Emmrich  P, Aleksic  S, Bockemuhl  J. Hemolytic-uremic syndrome in infants due to verotoxin-producing Escherichia coli [in German]. Dtsch Med Wochenschr. 1990;115:48995. DOIPubMedGoogle Scholar
  26. 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
  27. 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
  28. 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
  29. 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
  30. 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
  31. Riley  LW, Remis  RS, Helgerson  SD, McGee  HB, Wells  JG, Davis  BR, Hemorrhagic colitis associated with a rare Escherichia coli serotype. N Engl J Med. 1983;308:6815.PubMedGoogle Scholar
  32. 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
  33. Benson  G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 1999;27:57380. DOIPubMedGoogle Scholar
  34. Hunter  PR, Gaston  MA. Numerical index of the discriminatory ability of typing systems: an application of Simpson’s index of diversity. J Clin Microbiol. 1988;26:24656.PubMedGoogle Scholar
  35. Smith  JM, Feil  EJ, Smith  NH. Population structure and evolutionary dynamics of pathogenic bacteria. Bioessays. 2000;22:111522. DOIPubMedGoogle Scholar
  36. 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
  37. Holt  KE, Parkhill  J, Mazzoni  CJ, Roumagnac  P, Weill  F, Goodhead  I, High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nat Genet. 2008;40:98793. DOIPubMedGoogle Scholar
  38. Wells  JG, Davis  BR, Wachsmuth  IK, Riley  LW, Remis  RS, Sokolow  R, Laboratory investigation of hemorrhagic colitis outbreaks associated with a rare Escherichia coli serotype. J Clin Microbiol. 1983;18:51220.PubMedGoogle Scholar
  39. Achtman  M. Evolution, population structure, and phylogeography of genetically monomorphic bacterial pathogens. Annu Rev Microbiol. 2008;62:5370. DOIPubMedGoogle Scholar
  40. Kawamori  F, Hiroi  M, Harada  T, Ohata  K, Sugiyama  K, Masuda  T, Molecular typing of Japanese Escherichia coli O157:H7 isolates from clinical specimens by multilocus variable-number tandem repeat analysis and PFGE. J Med Microbiol. 2008;57:5863. DOIPubMedGoogle Scholar

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