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Genomic epidemiology and evolution of Escherichia coli in wild animals

Robert Murphy, View ORCID ProfileMartin Palm, Ville Mustonen, Jonas Warringer, View ORCID ProfileAnne Farewell, View ORCID ProfileDanesh Moradigaravand, Leopold Parts
doi: https://doi.org/10.1101/2020.07.23.216937
Robert Murphy
1University of Copenhagen, Department of Biology, Section for Ecology and Evolution, Universitetsparken 15, 2100 Copenhagen East, Denmark
2Center for Computational Biology, Institute of Cancer and Genomic Sciences, University of Birmingham, Birmingham, United Kingdom
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Martin Palm
3Department for Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden, Centre for Antibiotic Resistance Research at the University of Gothenburg, Gothenburg, Sweden
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Ville Mustonen
4Organismal and Evolutionary Biology Research Programme, Department of Computer Science, Institute of Biotechnology, University of Helsinki, Helsinki, Finland
5Helsinki Institute for Information Technology HIIT, Helsinki, Finland
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Jonas Warringer
3Department for Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden, Centre for Antibiotic Resistance Research at the University of Gothenburg, Gothenburg, Sweden
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Anne Farewell
3Department for Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden, Centre for Antibiotic Resistance Research at the University of Gothenburg, Gothenburg, Sweden
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Danesh Moradigaravand
2Center for Computational Biology, Institute of Cancer and Genomic Sciences, University of Birmingham, Birmingham, United Kingdom
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  • For correspondence: d.moradigaravand@bham.ac.uk
Leopold Parts
6Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridgeshire, United Kingdom
7Department of Computer Science, University of Tartu, Tartu, Estonia
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  • For correspondence: d.moradigaravand@bham.ac.uk
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Abstract

Escherichia coli is a common bacterial species in the gastrointestinal tracts of warm-blooded animals and humans. Pathogenic and antimicrobial resistance in E. coli may emerge via host switching from animal reservoirs. Despite its potential clinical importance, knowledge of the population structure of commensal E. coli within wild hosts and the epidemiological links between E. coli in non-human hosts and E. coli in humans is still scarce. In this study, we analysed the whole genome sequencing data of a collection of 119 commensal E. coli recovered from the guts of 68 mammal and bird species in Mexico and Venezuela in the 1990s. We observed low concordance between the population structures of E. coli colonizing wild animals and the phylogeny, taxonomy and ecological and physiological attributes of the host species, with distantly related E. coli often colonizing the same or similar host species and distantly related host species often hosting closely related E. coli. We found no evidence for recent transmission of E. coli genomes from wild animals to either domesticated animals or humans. However, multiple livestock- and human-related virulence factor genes were present in E. coli of wild animals, including virulence factors characteristic for Shiga toxin-producing E. coli (STEC) and atypical enteropathogenic E. coli (aEPEC), where several isolates from wild hosts harboured the locus of enterocyte effacement (LEE) pathogenicity island. Moreover, E. coli in wild animal hosts often harboured known antibiotic resistance determinants, including against ciprofloxacin, aminoglycosides, tetracyclines and beta-lactams, with some determinants present in multiple, distantly related E. coli lineages colonizing very different host animals. We conclude that although the genome pools of E. coli colonizing wild animal and human gut are well separated, they share virulence and antibiotic resistance genes and E. coli underscoring that wild animals could serve as reservoirs for E. coli pathogenicity in human and livestock infections.

Importance Escherichia coli is a clinically importance bacterial species implicated in human and livestock associated infections worldwide. The bacterium is known to reside in the guts of humans, livestock and wild animals. Although wild animals are recognized to serve as potential reservoirs for pathogenic E. coli strains, the knowledge of the population structure of E. coli in wild hosts is still scarce. In this study we used the fine resolution of whole genome sequencing to provide novel insights into the evolution of E. coli genomes within a broad range of wild animal species (including mammals and birds), the co-evolution of E. coli strains with their hosts and the genetics of pathogenicity of E. coli strains in wild hosts. Our results provide evidence for the clinical importance of wild animals as reservoirs for pathogenic strains and necessitate the inclusion of non-human hosts in the surveillance programs for E. coli infections.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
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Posted July 23, 2020.
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Genomic epidemiology and evolution of Escherichia coli in wild animals
Robert Murphy, Martin Palm, Ville Mustonen, Jonas Warringer, Anne Farewell, Danesh Moradigaravand, Leopold Parts
bioRxiv 2020.07.23.216937; doi: https://doi.org/10.1101/2020.07.23.216937
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Genomic epidemiology and evolution of Escherichia coli in wild animals
Robert Murphy, Martin Palm, Ville Mustonen, Jonas Warringer, Anne Farewell, Danesh Moradigaravand, Leopold Parts
bioRxiv 2020.07.23.216937; doi: https://doi.org/10.1101/2020.07.23.216937

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