Evidence for co-selection of antibiotic resistance genes and mobile genetic elements in metal polluted urban soils

Abstract

Antibiotic resistance genes (ARGs) constitute emerging environmental pollutants and pose risks to public health. Toxic metals are known to select for metal-resistant bacteria in metal-contaminated soils, but there is growing concern that metal contaminants can also act as co-selective agents thereby causing environmental proliferation of antibiotic resistance. In this study, we quantified ARGs and selected mobile genetic elements (MGEs) known to constitute potential ARG hosts in 50 archived urban and suburban soils from the Belfast metropolitan area using a high-throughput qPCR ARG chip. ARG prevalence was linked to concentrations of individual metals and a soil metal toxicity index calculated based on the relative toxicity of different metals to soil microbial processes. A total of 164 ARGs were detected across the 50 soils analyzed with an average absolute abundance of 3.4 × 107 ARG gene copies per gram of soil. A significant correlation between abundance of ARGs and MGEs was observed, suggesting the importance of horizontal gene transfer for ARG dissemination. Network analysis revealed significant co-occurrence patterns between specific metals (As, Cd, Co, Cr, Cu. Hg, Ni and Zn) and associated ARGs. Path analysis further indicated that the soil metal toxicity index significantly affected the number of detected ARGs (λ = 0.32, P < 0.001) and the abundance of metal co-occurring ARGs (λ = 0.612, P < 0.001) via effects on MGEs. Collectively, our results indicate a role of soil metals in co-selection of ARGs and MGEs in urban and semi-urban soils and suggest a risk for environmental ARG dissemination via horizontal gene transfer.