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A prospective role for the rumen in generating antibiotic resistance

View ORCID ProfileCameron R. Strachan, Anna J. Mueller, Mahdi Ghanbari, Viktoria Neubauer, Benjamin Zwirzitz, Sarah Thalguter, Monika Dziecol, Stefanie U. Wetzels, View ORCID ProfileJürgen Zanghellini, Martin Wagner, Stephan Schmitz-Esser, View ORCID ProfileEvelyne Mann
doi: https://doi.org/10.1101/729681
Cameron R. Strachan
FFoQSI GmbH, Technopark 1C, 3430 Tulln, AustriaInstitute of Food Safety, Food Technology and Veterinary Public Health, Department for Farm Animals and Public Health, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 Vienna, Austria
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  • For correspondence: cameron.strachan@vetmeduni.ac.at
Anna J. Mueller
University of Vienna, Centre for Microbiology and Environmental Systems Science, Division of Microbial Ecology, Althanstrasse 14, 1090 Vienna, Austria
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Mahdi Ghanbari
BIOMIN Research Center, Technopark 1, 3430, Tulln, Austria
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Viktoria Neubauer
Institute of Food Safety, Food Technology and Veterinary Public Health, Department for Farm Animals and Public Health, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 Vienna, Austria
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Benjamin Zwirzitz
FFoQSI GmbH, Technopark 1C, 3430 Tulln, AustriaInstitute of Food Safety, Food Technology and Veterinary Public Health, Department for Farm Animals and Public Health, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 Vienna, Austria
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Sarah Thalguter
FFoQSI GmbH, Technopark 1C, 3430 Tulln, AustriaInstitute of Food Safety, Food Technology and Veterinary Public Health, Department for Farm Animals and Public Health, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 Vienna, Austria
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Monika Dziecol
Institute of Food Safety, Food Technology and Veterinary Public Health, Department for Farm Animals and Public Health, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 Vienna, Austria
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Stefanie U. Wetzels
Institute of Food Safety, Food Technology and Veterinary Public Health, Department for Farm Animals and Public Health, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 Vienna, Austria
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Jürgen Zanghellini
Austrian Centre of Industrial Biotechnology, 1190 Vienna, AustriaDepartment of Biotechnology, University of Natural Resources and Life Sciences, Vienna, 1190 Vienna, AustriaAustrian Biotech University of Applied Sciences, 3430 Tulln, Austria
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Martin Wagner
FFoQSI GmbH, Technopark 1C, 3430 Tulln, AustriaInstitute of Food Safety, Food Technology and Veterinary Public Health, Department for Farm Animals and Public Health, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 Vienna, Austria
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Stephan Schmitz-Esser
Department of Animal Science, Iowa State University, 3222 National Swine Research and Information Center, 1029 North University Blvd, Ames, IA 50011-3611, USA.
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Evelyne Mann
Institute of Food Safety, Food Technology and Veterinary Public Health, Department for Farm Animals and Public Health, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 Vienna, Austria
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ABSTRACT

Antibiotics were a revolutionary discovery of the 20th century, but the ability of bacteria to spread the genetic determinants of resistance via horizontal gene transfer (HGT) has quickly endangered their use1. Indeed, there is a global network of microbial gene exchange, the analysis of which has revealed particularly frequent transfer of resistance determinants between farm animals and human-associated bacteria2. Here, we leverage the recent release of a rumen microbial genome reference set and show that the wide-spread resistance gene cluster aadE-sat4-aphA-3 is harboured in ruminal Bacteroidetes. While this cluster appears to have been recently transferred between commensal bacteria in the rumen and many diverse animal and human pathogens, comparative analysis suggests that the cluster stabilized in the pathogens. Then, focusing on streptomycin resistance, it was found that homologues from the rumen span much of the known diversity of aminoglycoside O-nucleotidyltransferases (AadEs) and that distinct variants of the enzyme are present in a single rumen bacterial genome. Notably, a second variant of AadE has also been recently transferred, albeit more often as a single gene, throughout a different set of animal and human associated bacteria. By examining the synteny of AadE orthologues in various bacterial genomes and analyzing corresponding gene trees in an environmental context, we speculate that the ruminant associated microbiome has a salient role in the emergence of specific resistance variants and clusters. In light of the recent literature on the evolutionary origin of antibiotic resistance, we further suggest that the rumen provides a possible route of dissemination of resistance genes from soil resistomes, throughout the farm, and to human pathogens3.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted August 12, 2019.
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A prospective role for the rumen in generating antibiotic resistance
Cameron R. Strachan, Anna J. Mueller, Mahdi Ghanbari, Viktoria Neubauer, Benjamin Zwirzitz, Sarah Thalguter, Monika Dziecol, Stefanie U. Wetzels, Jürgen Zanghellini, Martin Wagner, Stephan Schmitz-Esser, Evelyne Mann
bioRxiv 729681; doi: https://doi.org/10.1101/729681
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A prospective role for the rumen in generating antibiotic resistance
Cameron R. Strachan, Anna J. Mueller, Mahdi Ghanbari, Viktoria Neubauer, Benjamin Zwirzitz, Sarah Thalguter, Monika Dziecol, Stefanie U. Wetzels, Jürgen Zanghellini, Martin Wagner, Stephan Schmitz-Esser, Evelyne Mann
bioRxiv 729681; doi: https://doi.org/10.1101/729681

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