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Environmental Microbiology

Genetic and Phenotypic Factors Associated with Persistent Shedding of Shiga Toxin-Producing Escherichia coli by Beef Cattle

Heather M. Blankenship, Samantha Carbonell, Rebekah E. Mosci, Karen McWilliams, Karen Pietrzen, Scott Benko, Ted Gatesy, Daniel Grooms, Shannon D. Manning
Edward G. Dudley, Editor
Heather M. Blankenship
aDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan, USA
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Samantha Carbonell
aDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan, USA
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Rebekah E. Mosci
aDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan, USA
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Karen McWilliams
cMichigan Department of Agriculture and Rural Development, State of Michigan, East Lansing, Michigan, USA
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Karen Pietrzen
cMichigan Department of Agriculture and Rural Development, State of Michigan, East Lansing, Michigan, USA
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Scott Benko
cMichigan Department of Agriculture and Rural Development, State of Michigan, East Lansing, Michigan, USA
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Ted Gatesy
cMichigan Department of Agriculture and Rural Development, State of Michigan, East Lansing, Michigan, USA
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Daniel Grooms
bCollege of Veterinary Medicine, Iowa State University, Ames, Iowa, USA
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Shannon D. Manning
aDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan, USA
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Edward G. Dudley
The Pennsylvania State University
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DOI: 10.1128/AEM.01292-20
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ABSTRACT

Shiga toxin-producing Escherichia coli (STEC) is a leading cause of foodborne infections. Cattle are an important STEC reservoir, although little is known about specific pathogen traits that impact persistence in the farm environment. Hence, we sought to evaluate STEC isolates recovered from beef cattle in a single herd in Michigan. To do this, we collected fecal grabs from 26 cattle and resampled 13 of these animals at 3 additional visits over a 3-month period. In all, 66 STEC isolates were recovered for genomics and biofilm quantification using crystal violet assays. The STEC population was diverse, representing seven serotypes, including O157:H7, O26:H11, and O103:H2, which are commonly associated with human infections. Although a core genome analysis of 2,933 genes grouped isolates into clusters based on serogroups, some isolates within each cluster had variable biofilm levels and virulence gene profiles. Most (77.8%; n = 49) isolates harbored stx2a, while 38 (57.5%) isolates formed strong biofilms. Isolates belonging to the predominant serogroup O6 (n = 36; 54.5%) were more likely to form strong biofilms, persistently colonize multiple cattle, and be acquired over time. A high-quality single nucleotide polymorphism (SNP) analysis of 33 O6 isolates detected between 0 and 13 single nucleotide polymorphism (SNP) differences between strains, indicating that highly similar strain types were persisting in this herd. Similar findings were observed for other persistent serogroups, although key genes were found to differ among strong and weak biofilm producers. Together, these data highlight the diversity and persistent nature of some STEC types in this important food animal reservoir.

IMPORTANCE Food animal reservoirs contribute to Shiga toxin-producing Escherichia coli (STEC) evolution via the acquisition of horizontally acquired elements like Shiga toxin bacteriophages that enhance pathogenicity. In cattle, persistent fecal shedding of STEC contributes to contamination of beef and dairy products and to crops being exposed to contaminated water systems. Hence, identifying factors important for STEC persistence is critical. This longitudinal study enhances our understanding of the genetic diversity of STEC types circulating in a cattle herd and identifies genotypic and phenotypic traits associated with persistence. Key findings demonstrate that multiple STEC types readily persist in and are transmitted across cattle in a shared environment. These dynamics also enhance the persistence of virulence genes that can be transferred between bacterial hosts, resulting in the emergence of novel STEC strain types. Understanding how pathogens persist and diversify in reservoirs is important for guiding new preharvest prevention strategies aimed at reducing foodborne transmission to humans.

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Genetic and Phenotypic Factors Associated with Persistent Shedding of Shiga Toxin-Producing Escherichia coli by Beef Cattle
Heather M. Blankenship, Samantha Carbonell, Rebekah E. Mosci, Karen McWilliams, Karen Pietrzen, Scott Benko, Ted Gatesy, Daniel Grooms, Shannon D. Manning
Applied and Environmental Microbiology Oct 2020, 86 (20) e01292-20; DOI: 10.1128/AEM.01292-20

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Genetic and Phenotypic Factors Associated with Persistent Shedding of Shiga Toxin-Producing Escherichia coli by Beef Cattle
Heather M. Blankenship, Samantha Carbonell, Rebekah E. Mosci, Karen McWilliams, Karen Pietrzen, Scott Benko, Ted Gatesy, Daniel Grooms, Shannon D. Manning
Applied and Environmental Microbiology Oct 2020, 86 (20) e01292-20; DOI: 10.1128/AEM.01292-20
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KEYWORDS

Escherichia coli
Shiga Toxins
biofilms
cattle
genomics

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