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ARS Home » Plains Area » Clay Center, Nebraska » U.S. Meat Animal Research Center » Meat Safety and Quality » Research » Publications at this Location » Publication #272024
Title: Phylogeny of Shiga toxin-producing Escherichia coli O157 isolated from cattle and clinically ill humans

Author
item Bono, James - Jim
item Smith, Timothy - Tim
item KEEN, JAMES - University Of Nebraska
item Harhay, Gregory
item McDaneld, Tara
item Mandrell, Robert
item JUNG, WOO KYUNG - Washington State University
item BESSER, THOMAS - Washington State University
item GERNER-SMIDT, PETER - Centers For Disease Control And Prevention (CDC) - United States
item BIELASZEWSKA, MARTINA - University Of Munster
item KARCH, HELGE - University Of Munster
item Clawson, Michael - Mike

Submitted to: Molecular Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/14/2012
Publication Date: 2/21/2012
Citation: Bono, J.L., Smith, T.P., Keen, J.E., Harhay, G.P., McDaneld, T.G., Mandrell, R.E., Jung, W., Besser, T.E., Gerner-Smidt, P., Bielaszewska, M., Karch, H., Clawson, M.L. 2012. Phylogeny of Shiga toxin-producing Escherichia coli O157 isolated from cattle and clinically ill humans. Molecular Biology and Evolution. 29(8):2047-2062. doi: 10.1093/molbev/mss072.

Interpretive Summary: Shiga toxin-producing Escherichia coli O157:H7 (STEC O157) recently emerged as a significant cause of diarrhea, hemorrhagic colitis, and hemolytic uremic syndrome throughout much of the world. Cattle are a reservoir for STEC O157, and many human outbreaks have been linked to the consumption of beef products contaminated with the bacteria. However, cattle are known to maintain genetically diverse STEC O157, of which not all are typically found in clinically ill humans. To identify genetic subtypes associated with either cattle or human disease, and to understand STEC O157 evolution, we genotyped 762 nucleotide polymorphisms in a large collection of strains isolated from humans and cattle. Evolutionary analyses revealed eight major lineages of STEC O157. How cattle originally acquired STEC O157 is unknown, however, they are a reservoir for seven of the eight lineages. One lineage harbored by cattle is rarely found in clinically ill humans. Two other lineages harbored by cattle accounted for the majority of human disease in this study. A marker set was developed that efficiently detects STEC O157 subtypes, including those associated with the cattle reservoir and human disease.

Technical 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 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.