Bacterial phylogeny structures soil resistomes across habitats

Ancient and diverse antibiotic resistance genes (ARGs) have previously been identified from soil(1–3), including genes identical to those in human pathogens(4). Despite the apparent overlap between soil and clinical resistomes(4–6), factors influencing ARG composition in soil and their movement between genomes and habitats remain largely unknown(3). General metagenome functions often correlate with the underlying structure of bacterial communities(7–12). However, ARGs are hypothesized to be highly mobile(4,5,13), prompting speculation that resistomes may not correlate with phylogenetic signatures or ecological divisions(13,14). To investigate these relationships, we performed functional metagenomic selections for resistance to 18 antibiotics from 18 agricultural and grassland soils. The 2895 ARGs we discovered were predominantly novel, and represent all major resistance mechanisms(15). We demonstrate that distinct soil types harbor distinct resistomes, and that nitrogen fertilizer amendments strongly influenced soil ARG content. Resistome composition also correlated with microbial phylogenetic and taxonomic structure, both across and within soil types. Consistent with this strong correlation, mobility elements syntenic with ARGs were rare in soil compared to sequenced pathogens, suggesting that ARGs in the soil may not transfer between bacteria as readily as is observed in the clinic. Together, our results indicate that bacterial community composition is the primary determinant of soil ARG content, challenging previous hypotheses that horizontal gene transfer effectively decouples resistomes from phylogeny(13,14).