Tick-vectored mobilization of antibiotic resistance genes: transboundary dissemination across wildlife-livestock-vector-environment interfaces

Antibiotic resistance genes (ARGs) are emerging as critical environmental contaminants across diverse ecological interfaces. To dissect evidence of microbiome and resistome in the different interconnected interfaces of ecotone, we conducted a field investigation of the microbiome and resistome of marmots, along with coexisting domestic sheep, ticks and their cave soils within the same ecological habitat. We used shotgun metagenomics with metagenome-assembled genomes (MAGs), species-resolved binning, ARG identification, source-tracker analyses, and horizontal gene transfer (HGT) network analysis to examine potential cross-interface dissemination. The composition of the mammalian gut microbiome was primarily comprised of Firmicutes, while ticks and soils exhibited distinct clusters that were predominantly dominated by Proteobacteria. The observed resistance mechanisms manifested niche-specific patterns, with target alteration predominating in mammals, whereas ticks exhibited elevated antibiotic inactivation/efflux strategies, and soils prioritized efflux mechanisms. Metagenomic assembly from these four groups yielded 5339 metagenome-assembled genomes (MAGs), of which 1481 met medium- or high-quality standards. Ticks exhibited 72% species similarity and 52% ARG concordance with marmots, while soils conserved 32% ARGs and >86% toxin genes with mammals. Our findings demonstrate that the transboundary dissemination of ARGs across different ecological interfaces, necessitates integrated surveillance of antimicrobial resistance at ecological boundaries to mitigate public health risks.