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

Bono, James L., Smith, Timothy P.L., Keen, James E., Harhay, Gregory P., McDaneld, Tara G., Mandrell, Robert E., Jung, Woo Kyung, Besser, Thomas E., Gerner-Smidt, Peter, Bielaszewska, Martina, Karch, Helge, Clawson, Michael L.
Molecular Biology and Evolution 2012 v.29 no.8 pp. 2047
Escherichia coli O157, Escherichia infections, alleles, bacteriophages, cattle, disease reservoirs, genetic polymorphism, genotype, human diseases, humans, nucleotide sequences, phylogeny, pulsed-field gel electrophoresis, virulence
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 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 193 STEC O157 human and cattle isolated strains, we genotyped a large collection of 430 STEC O157 strains. Concatenated polymorphism alleles defined 175 polymorphism-derived 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 that are harbored by cattle accounted for the majority of human disease in this study, whereas one other was rarely represented in humans and may have evolved towards reduced human virulence. Notably, cattle are not a reservoir for E. coli O55:H7 or STEC O157H*-, 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 Bln1 and Xba1 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.