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The rumen microbiome as a reservoir of antimicrobial resistance and pathogenicity genes is directly affected by diet in beef cattle

BACKGROUND: The emergence and spread of antimicrobial resistance is the most urgent current threat to human and animal health. An improved understanding of the abundance of antimicrobial resistance genes and genes associated with microbial colonisation and pathogenicity in the animal gut will have a...

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Autores principales: Auffret, Marc D., Dewhurst, Richard J., Duthie, Carol-Anne, Rooke, John A., John Wallace, R., Freeman, Tom C., Stewart, Robert, Watson, Mick, Roehe, Rainer
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5725880/
https://www.ncbi.nlm.nih.gov/pubmed/29228991
http://dx.doi.org/10.1186/s40168-017-0378-z
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author Auffret, Marc D.
Dewhurst, Richard J.
Duthie, Carol-Anne
Rooke, John A.
John Wallace, R.
Freeman, Tom C.
Stewart, Robert
Watson, Mick
Roehe, Rainer
author_facet Auffret, Marc D.
Dewhurst, Richard J.
Duthie, Carol-Anne
Rooke, John A.
John Wallace, R.
Freeman, Tom C.
Stewart, Robert
Watson, Mick
Roehe, Rainer
author_sort Auffret, Marc D.
collection PubMed
description BACKGROUND: The emergence and spread of antimicrobial resistance is the most urgent current threat to human and animal health. An improved understanding of the abundance of antimicrobial resistance genes and genes associated with microbial colonisation and pathogenicity in the animal gut will have a major role in reducing the contribution of animal production to this problem. Here, the influence of diet on the ruminal resistome and abundance of pathogenicity genes was assessed in ruminal digesta samples taken from 50 antibiotic-free beef cattle, comprising four cattle breeds receiving two diets containing different proportions of concentrate. RESULTS: Two hundred and four genes associated with antimicrobial resistance (AMR), colonisation, communication or pathogenicity functions were identified from 4966 metagenomic genes using KEGG identification. Both the diversity and abundance of these genes were higher in concentrate-fed animals. Chloramphenicol and microcin resistance genes were dominant in samples from forage-fed animals (P < 0.001), while aminoglycoside and streptomycin resistances were enriched in concentrate-fed animals. The concentrate-based diet also increased the relative abundance of Proteobacteria, which includes many animal and zoonotic pathogens. A high ratio of Proteobacteria to (Firmicutes + Bacteroidetes) was confirmed as a good indicator for rumen dysbiosis, with eight cases all from concentrate-fed animals. Finally, network analysis demonstrated that the resistance/pathogenicity genes are potentially useful as biomarkers for health risk assessment of the ruminal microbiome. CONCLUSIONS: Diet has important effects on the complement of AMR genes in the rumen microbial community, with potential implications for human and animal health. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-017-0378-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-57258802017-12-13 The rumen microbiome as a reservoir of antimicrobial resistance and pathogenicity genes is directly affected by diet in beef cattle Auffret, Marc D. Dewhurst, Richard J. Duthie, Carol-Anne Rooke, John A. John Wallace, R. Freeman, Tom C. Stewart, Robert Watson, Mick Roehe, Rainer Microbiome Research BACKGROUND: The emergence and spread of antimicrobial resistance is the most urgent current threat to human and animal health. An improved understanding of the abundance of antimicrobial resistance genes and genes associated with microbial colonisation and pathogenicity in the animal gut will have a major role in reducing the contribution of animal production to this problem. Here, the influence of diet on the ruminal resistome and abundance of pathogenicity genes was assessed in ruminal digesta samples taken from 50 antibiotic-free beef cattle, comprising four cattle breeds receiving two diets containing different proportions of concentrate. RESULTS: Two hundred and four genes associated with antimicrobial resistance (AMR), colonisation, communication or pathogenicity functions were identified from 4966 metagenomic genes using KEGG identification. Both the diversity and abundance of these genes were higher in concentrate-fed animals. Chloramphenicol and microcin resistance genes were dominant in samples from forage-fed animals (P < 0.001), while aminoglycoside and streptomycin resistances were enriched in concentrate-fed animals. The concentrate-based diet also increased the relative abundance of Proteobacteria, which includes many animal and zoonotic pathogens. A high ratio of Proteobacteria to (Firmicutes + Bacteroidetes) was confirmed as a good indicator for rumen dysbiosis, with eight cases all from concentrate-fed animals. Finally, network analysis demonstrated that the resistance/pathogenicity genes are potentially useful as biomarkers for health risk assessment of the ruminal microbiome. CONCLUSIONS: Diet has important effects on the complement of AMR genes in the rumen microbial community, with potential implications for human and animal health. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-017-0378-z) contains supplementary material, which is available to authorized users. BioMed Central 2017-12-11 /pmc/articles/PMC5725880/ /pubmed/29228991 http://dx.doi.org/10.1186/s40168-017-0378-z Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Auffret, Marc D.
Dewhurst, Richard J.
Duthie, Carol-Anne
Rooke, John A.
John Wallace, R.
Freeman, Tom C.
Stewart, Robert
Watson, Mick
Roehe, Rainer
The rumen microbiome as a reservoir of antimicrobial resistance and pathogenicity genes is directly affected by diet in beef cattle
title The rumen microbiome as a reservoir of antimicrobial resistance and pathogenicity genes is directly affected by diet in beef cattle
title_full The rumen microbiome as a reservoir of antimicrobial resistance and pathogenicity genes is directly affected by diet in beef cattle
title_fullStr The rumen microbiome as a reservoir of antimicrobial resistance and pathogenicity genes is directly affected by diet in beef cattle
title_full_unstemmed The rumen microbiome as a reservoir of antimicrobial resistance and pathogenicity genes is directly affected by diet in beef cattle
title_short The rumen microbiome as a reservoir of antimicrobial resistance and pathogenicity genes is directly affected by diet in beef cattle
title_sort rumen microbiome as a reservoir of antimicrobial resistance and pathogenicity genes is directly affected by diet in beef cattle
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5725880/
https://www.ncbi.nlm.nih.gov/pubmed/29228991
http://dx.doi.org/10.1186/s40168-017-0378-z
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