Phylogeny of Shiga Toxin-Producing Escherichia coli O157 Isolated from Cattle and Clinically Ill Humans

Authors

James L. Bono, US Meat Animal Research Center, Clay Center, NebraskaFollow
Timothy P. L. Smith, US Meat Animal Research CenterFollow
James E. Keen, Great Plains Veterinary Educational Center, University of NebraskaFollow
Gregory P. Harhay, US Meat Animal Research Center, Clay Center, NebraskaFollow
Tara G. McDaneld, US Meat Animal Research Center, Clay Center, NebraskaFollow
Robert E. Mandrell, USDA-ARS Western Regional Research Center, Albany, CaliforniaFollow
Woo Kyung Jung, Washington State University
Thomas E. Besser, Washington State UniversityFollow
Peter Gerner-Smidt, Centers for Disease Control and Prevention
Martina Bielaszewska, University of Münster, Germany
Helge Karch, University of Münster, GermanyFollow
Michael L. Clawson, US Meat Animal Research Center, Clay Center, NebraskaFollow

Date of this Version

2012

Document Type

Article

Citation

Mol. Biol. Evol. 29(8):2047–2062. 2012 doi:10.1093/molbev/mss072

Comments

This article is a U.S. government work, and is not subject to copyright in the United States.

Abstract

Cattle are a major reservoir for Shiga toxin-producing Escherichia coli O157 (STEC O157) and harbor multiple genetic subtypes that do not all associate with human disease. STEC O157 evolved from an E. coli O55:H7 progenitor; however, a lack of genome sequence has hindered investigations on the divergence of human- and/or cattle-associated subtypes. Our goals were to 1) identify nucleotide polymorphisms for STEC O157 genetic subtype detection, 2) determine the phylogeny of STEC O157 genetic subtypes using polymorphism-derived genotypes and a phage insertion typing system, and 3) compare polymorphism-derived genotypes identified in this study with pulsed field gel electrophoresis (PFGE), the current gold standard for evaluating STEC O157 diversity. Using 762 nucleotide polymorphisms that were originally identified through whole-genome sequencing of 189 STEC O157 human- and cattle-isolated strains, we genotyped a collection of 426 STEC O157 strains. Concatenated polymorphism alleles defined 175 genotypes that were tagged by a minimal set of 138 polymorphisms. Eight major lineages of STEC O157 were identified, of which cattle are a reservoir for seven. Two lineages regularly harbored by cattle accounted for the majority of human disease in this study, whereas another was rarely represented in humans and may have evolved toward reduced human virulence. Notably, cattle are not a known reservoir for E. coli O55:H7 or STEC O157:H¯ (the first lineage to diverge within the STEC O157 serogroup), which both cause human disease. This result calls into question how cattle may have originally acquired STEC O157. The polymorphism-derived genotypes identified in this study did not surpass PFGE diversity assessed by BlnI and XbaI digestions in a subset of 93 strains. However, our results show that they are highly effective in assessing the evolutionary relatedness of epidemiologically unrelated STEC O157 genetic subtypes, including those associated with the cattle reservoir and human disease.

Supplementary tables 1–5 are attached (below) as .xlsx files