Host genetics affected the resistome and its expression patterns in the rumen of beef cattle raised without antibiotics used in humans

Abstract

Background: The rumen microbiome is a potential reservoir of antimicrobial-resistant genes (ARGs), termly resistome. However, the activity of ARGs and what factors affect expression of ARGs in the rumen is unknown. Here, the rumen resistome was evaluated using metagenomic and metatranscriptomic datasets, with the aim to identify the active rumen resistome and whether it can be affected by cattle breed and feed efficiency.Results: Genes encoding resistance to 12 ARG classes representing 62 individual ARGs were detected in the rumen metagenomes of Angus, Charolais or Kinsella composite hybrid (KC) beef steers (n = 48) with high and low feed efficiency. Three genes encoding tetracycline (tetQ, tetW) and macrolide (mefA) resistance constituted 75.3% of abundance of total ARGs identified in all animals, suggesting they are ‘core’ resistome in the rumen of steers. Only about 20.96% (13/62) of the total ARGs identified were expressed, among which genes encoding resistance to tetracycline, macrolide-licosamide-streptogramin (MLS), aminoglycoside, and multidrug exhibited the highest level of expression. More than half (56.2%) of the ARGs identified were plasmid-associated, while only 5 plasmid-associated ARGs were expressed. The abundance of 17, 14, and 5 individual ARGs were significantly affected by breed, feed efficiency, and breed × feed efficiency, respectively, while the expression of ARGs did not differ among breeds or between feed efficiency groups. In KC cattle, less number of total ARGs, ARG transcripts, as well as total active bacteria (estimated by 16S rRNA copies) was observed than AN. The total active bacteria were negatively correlated with expression of MLS and tetracycline ARG (mefA, tet40, tetM, tetW, and an unidentified tet), and tended to be negatively correlated with the expression of plasmid-associated tetracycline ARG t only in the rumen of KC cattle.Conclusions: Our results suggest that a large portion of the ARGs are not expressed in the rumen of cattle raised without antibiotics used in humans. The identified less diversified active resistome and total active bacteria, and the significant correlation between total active bacteria and the abundance of ARG transcripts in KC cattle suggest that the expression of resistome in the rumen may be breed specific and driven by ruminal microbiota.