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

Abstract 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 wil...

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Main Authors: Marc D. Auffret, Richard J. Dewhurst, Carol-Anne Duthie, John A. Rooke, R. John Wallace, Tom C. Freeman, Robert Stewart, Mick Watson, Rainer Roehe
Format: Article
Language:English
Published: BMC 2017-12-01
Series:Microbiome
Subjects:
AMR
Online Access:http://link.springer.com/article/10.1186/s40168-017-0378-z
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spelling doaj-2e84acb575c04d7d97a448b85a48feab2020-11-25T01:46:54ZengBMCMicrobiome2049-26182017-12-015111110.1186/s40168-017-0378-zThe rumen microbiome as a reservoir of antimicrobial resistance and pathogenicity genes is directly affected by diet in beef cattleMarc D. Auffret0Richard J. Dewhurst1Carol-Anne Duthie2John A. Rooke3R. John Wallace4Tom C. Freeman5Robert Stewart6Mick Watson7Rainer Roehe8SRUCSRUCSRUCSRUCRowett Institute, University of AberdeenDivision of Genetics and Genomics, The Roslin Institute and R(D)SVS, University of EdinburghEdinburgh Genomics, The Roslin Institute and R(D)SVS, University of EdinburghDivision of Genetics and Genomics, The Roslin Institute and R(D)SVS, University of EdinburghSRUCAbstract 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.http://link.springer.com/article/10.1186/s40168-017-0378-zRumen microbiomeAMRDietsMetagenomicsProteobacteria ratio
collection DOAJ
language English
format Article
sources DOAJ
author Marc D. Auffret
Richard J. Dewhurst
Carol-Anne Duthie
John A. Rooke
R. John Wallace
Tom C. Freeman
Robert Stewart
Mick Watson
Rainer Roehe
spellingShingle Marc D. Auffret
Richard J. Dewhurst
Carol-Anne Duthie
John A. Rooke
R. John Wallace
Tom C. Freeman
Robert Stewart
Mick Watson
Rainer Roehe
The rumen microbiome as a reservoir of antimicrobial resistance and pathogenicity genes is directly affected by diet in beef cattle
Microbiome
Rumen microbiome
AMR
Diets
Metagenomics
Proteobacteria ratio
author_facet Marc D. Auffret
Richard J. Dewhurst
Carol-Anne Duthie
John A. Rooke
R. John Wallace
Tom C. Freeman
Robert Stewart
Mick Watson
Rainer Roehe
author_sort Marc D. Auffret
title 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_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_sort rumen microbiome as a reservoir of antimicrobial resistance and pathogenicity genes is directly affected by diet in beef cattle
publisher BMC
series Microbiome
issn 2049-2618
publishDate 2017-12-01
description Abstract 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.
topic Rumen microbiome
AMR
Diets
Metagenomics
Proteobacteria ratio
url http://link.springer.com/article/10.1186/s40168-017-0378-z
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