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Gut Colonization by ESBL-Producing Escherichia coli in Dogs Is Associated with a Distinct Microbiome and Resistome Composition

The gut microbiome of humans and animals acts as a reservoir of extended-spectrum beta-lactamase-producing Escherichia coli (ESBL-EC). Dogs are known for having a high prevalence of ESBL-EC in their gut microbiota, although their ESBL-EC carrier status often shifts over time. We hypothesized that th...

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Autores principales: Stege, Paul B., Hordijk, Joost, Sandholt, Arnar K. S., Zomer, Aldert L., Viveen, Marco C., Rogers, Malbert R. C., Salomons, Moniek, Wagenaar, Jaap A., Mughini-Gras, Lapo, Willems, Rob J. L., Paganelli, Fernanda L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10434115/
https://www.ncbi.nlm.nih.gov/pubmed/37404183
http://dx.doi.org/10.1128/spectrum.00063-23
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author Stege, Paul B.
Hordijk, Joost
Sandholt, Arnar K. S.
Zomer, Aldert L.
Viveen, Marco C.
Rogers, Malbert R. C.
Salomons, Moniek
Wagenaar, Jaap A.
Mughini-Gras, Lapo
Willems, Rob J. L.
Paganelli, Fernanda L.
author_facet Stege, Paul B.
Hordijk, Joost
Sandholt, Arnar K. S.
Zomer, Aldert L.
Viveen, Marco C.
Rogers, Malbert R. C.
Salomons, Moniek
Wagenaar, Jaap A.
Mughini-Gras, Lapo
Willems, Rob J. L.
Paganelli, Fernanda L.
author_sort Stege, Paul B.
collection PubMed
description The gut microbiome of humans and animals acts as a reservoir of extended-spectrum beta-lactamase-producing Escherichia coli (ESBL-EC). Dogs are known for having a high prevalence of ESBL-EC in their gut microbiota, although their ESBL-EC carrier status often shifts over time. We hypothesized that the gut microbiome composition of dogs is implicated in ESBL-EC colonization status. Therefore, we assessed whether ESBL-EC carriage in dogs is associated with changes in the gut microbiome and resistome. Fecal samples were collected longitudinally from 57 companion dogs in the Netherlands every 2 weeks for a total of 6 weeks (n = 4 samples/dog). Carriage of ESBL-EC was determined through selective culturing and PCR and in line with previous studies, we observed a high prevalence of ESBL-EC carriage in dogs. Using 16s rRNA gene profiling we found significant associations between detected ESBL-EC carriage and an increased abundance of Clostridium sensu stricto 1, Enterococcus, Lactococcus, and the shared genera of Escherichia-Shigella in the dog microbiome. A resistome capture sequencing approach (ResCap) furthermore, revealed associations between detected ESBL-EC carriage and the increased abundance of the antimicrobial resistance genes: cmlA, dfrA, dhfR, floR, and sul3. In summary, our study showed that ESBL-EC carriage is associated with a distinct microbiome and resistome composition. IMPORTANCE The gut microbiome of humans and animals is an important source of multidrug resistant pathogens, including beta-lactamase-producing Escherichia coli (ESBL-EC). In this study, we assessed if the carriage of ESBL-EC in dogs was associated with changes in gut composition of bacteria and antimicrobial resistant genes (ARGs). Therefore, stool samples from 57 dogs were collected every 2 weeks for a total of 6 weeks. Sixty eight percent of the dogs carried ESBL-EC during at least one of the time points analyzed. By investigating the gut microbiome and resistome composition, we observed specific changes at time points when dogs were colonized with ESBL-EC compared to time points whenESBL-EC were not detected. In conclusion, our study highlights the importance to study the microbial diversity in companion animals, as gut colonization of particular antimicrobial resistant bacteria might be an indication of a changed microbial composition that is associated with the selection of particular ARGs.
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spelling pubmed-104341152023-08-18 Gut Colonization by ESBL-Producing Escherichia coli in Dogs Is Associated with a Distinct Microbiome and Resistome Composition Stege, Paul B. Hordijk, Joost Sandholt, Arnar K. S. Zomer, Aldert L. Viveen, Marco C. Rogers, Malbert R. C. Salomons, Moniek Wagenaar, Jaap A. Mughini-Gras, Lapo Willems, Rob J. L. Paganelli, Fernanda L. Microbiol Spectr Research Article The gut microbiome of humans and animals acts as a reservoir of extended-spectrum beta-lactamase-producing Escherichia coli (ESBL-EC). Dogs are known for having a high prevalence of ESBL-EC in their gut microbiota, although their ESBL-EC carrier status often shifts over time. We hypothesized that the gut microbiome composition of dogs is implicated in ESBL-EC colonization status. Therefore, we assessed whether ESBL-EC carriage in dogs is associated with changes in the gut microbiome and resistome. Fecal samples were collected longitudinally from 57 companion dogs in the Netherlands every 2 weeks for a total of 6 weeks (n = 4 samples/dog). Carriage of ESBL-EC was determined through selective culturing and PCR and in line with previous studies, we observed a high prevalence of ESBL-EC carriage in dogs. Using 16s rRNA gene profiling we found significant associations between detected ESBL-EC carriage and an increased abundance of Clostridium sensu stricto 1, Enterococcus, Lactococcus, and the shared genera of Escherichia-Shigella in the dog microbiome. A resistome capture sequencing approach (ResCap) furthermore, revealed associations between detected ESBL-EC carriage and the increased abundance of the antimicrobial resistance genes: cmlA, dfrA, dhfR, floR, and sul3. In summary, our study showed that ESBL-EC carriage is associated with a distinct microbiome and resistome composition. IMPORTANCE The gut microbiome of humans and animals is an important source of multidrug resistant pathogens, including beta-lactamase-producing Escherichia coli (ESBL-EC). In this study, we assessed if the carriage of ESBL-EC in dogs was associated with changes in gut composition of bacteria and antimicrobial resistant genes (ARGs). Therefore, stool samples from 57 dogs were collected every 2 weeks for a total of 6 weeks. Sixty eight percent of the dogs carried ESBL-EC during at least one of the time points analyzed. By investigating the gut microbiome and resistome composition, we observed specific changes at time points when dogs were colonized with ESBL-EC compared to time points whenESBL-EC were not detected. In conclusion, our study highlights the importance to study the microbial diversity in companion animals, as gut colonization of particular antimicrobial resistant bacteria might be an indication of a changed microbial composition that is associated with the selection of particular ARGs. American Society for Microbiology 2023-07-05 /pmc/articles/PMC10434115/ /pubmed/37404183 http://dx.doi.org/10.1128/spectrum.00063-23 Text en Copyright © 2023 Stege et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Stege, Paul B.
Hordijk, Joost
Sandholt, Arnar K. S.
Zomer, Aldert L.
Viveen, Marco C.
Rogers, Malbert R. C.
Salomons, Moniek
Wagenaar, Jaap A.
Mughini-Gras, Lapo
Willems, Rob J. L.
Paganelli, Fernanda L.
Gut Colonization by ESBL-Producing Escherichia coli in Dogs Is Associated with a Distinct Microbiome and Resistome Composition
title Gut Colonization by ESBL-Producing Escherichia coli in Dogs Is Associated with a Distinct Microbiome and Resistome Composition
title_full Gut Colonization by ESBL-Producing Escherichia coli in Dogs Is Associated with a Distinct Microbiome and Resistome Composition
title_fullStr Gut Colonization by ESBL-Producing Escherichia coli in Dogs Is Associated with a Distinct Microbiome and Resistome Composition
title_full_unstemmed Gut Colonization by ESBL-Producing Escherichia coli in Dogs Is Associated with a Distinct Microbiome and Resistome Composition
title_short Gut Colonization by ESBL-Producing Escherichia coli in Dogs Is Associated with a Distinct Microbiome and Resistome Composition
title_sort gut colonization by esbl-producing escherichia coli in dogs is associated with a distinct microbiome and resistome composition
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10434115/
https://www.ncbi.nlm.nih.gov/pubmed/37404183
http://dx.doi.org/10.1128/spectrum.00063-23
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