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

Abstract

BackgroundThe 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.ResultsTwo 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.ConclusionsDiet has important effects on the complement of AMR genes in the rumen microbial community, with potential implications for human and animal health.Electronic supplementary materialThe online version of this article (10.1186/s40168-017-0378-z) contains supplementary material, which is available to authorized users.

A catalog of microbial genes from the bovine rumen unveils a specialized and diverse biomass-degrading environment

“…Similar to this study, tetracycline resistance was reported as highly abundant in the rumen, otherwise prevalence of resistance to other antibiotics varies between studies [36,37]. Although the methodologies used to detect ARGs could play a role in these differences [35][36][37], it is probable that variation in the rumen resistome may differ between countries and regions as it can reflect decades of exposure since antibiotics started to be used in farms.…”

“…Information from ruminants is predominantly from the fecal microbiome [34], and although the importance of the rumen microbiome has also been highlighted [35,36], data on the rumen resistome is still fragmented. As an example of the useful information than can be retrieved from a gene catalog, we evaluated the presence of ARG in the rumen microbiome as previously reported [12].…”

“…Forty-two ARGs encoding resistance to 27 antibiotics were detected in the catalog. The most abundant resistances were to tetracycline and bacitracin with Charolais animals harboring globally a higher proportion of these genes ( Supplementary Figure 15), probably reflecting the effect of diet [35]. It is noted that antibiotics as growth promoters were never used on these animals.…”

Whole genome sequencing and metagenomics for outbreak investigation, source attribution and risk assessment of food‐borne microorganisms

“…However, there are some examples available in the literature. For instance, the role of the rumen as a reservoir of virulence‐associated genes has been monitored by (Singh et al., ) and (Auffret et al., ). The benefits (rapidity; simultaneous detection of a range of virulence genes; potential for obtaining information on the genetic background of the virulence determinants), limitations (results will depend on the quality of the databases; uncertainty on the agreement between virulence genes detection and phenotype), and opportunities (potential to re‐analyse previously sequenced genomes and to link sequencing data with metadata from the samples) of using shotgun metagenomics with this aim are similar to those previously described for the resistome.…”

The genomic and proteomic landscape of the rumen microbiome revealed by comprehensive genome-resolved metagenomics

“…Fibrobacteres devote the highest percentage of their proteome to carbohydrate metabolism (over 6.6%), as is expected due to their fibre-attached, high cellulolytic activity. Only a few studies exist on the role of Planctomycetes in the rumen [52][53][54] , however whilst they contribute a relatively low number of proteins in our dataset (30172), just over 5% of those proteins are predicted to be CAZymes, suggesting a role in and adaptation to carbohydrate metabolism. Most phyla encode relatively similar proportions of each of the eight classes of CAZyme; however, the archaea encode proportionally more glycosyl transferases, and the Fibrobacteres encode proportionally more carbohydrate binding molecules.…”