Resilience of agricultural soils to antibiotic resistance genes introduced by agricultural management practices

Abstract

Antimicrobial resistance (AR) represents a global threat in human and veterinary medicine. In that regard, AR proliferation and dissemination in agricultural soils after manure application raises concerns on the enrichment of endogenous soil bacterial population with allochthonous antibiotic resistance genes (ARGs). Natural resilience of agricultural soils and background concentrations of ARGs play key roles in the mitigation of AR propagation in natural environments. In the present study, we carried out a longitudinal sampling campaign for two crop vegetation periods to monitor spatial and temporal changes in the abundance of seven clinically relevant ARGs (sul1, ermB, vanA, aph(3')-IIa, aph(3′)-IIIa, blaTEM-1 and tet(W)) and ribosomal 16S RNA. The absolute and relative abundances of the selected ARGs were quantified in total community DNA extracted from agricultural (manured and non-manured) and forest soils, fresh pig faeces and manure slurry. We observed that ARG concentrations return to background levels after manure-induced exposure within a crop growing season, highlighting the resilience capacity of soil. Naturally occurring high background concentrations of ARGs can be found in forest soil in due distance under low anthropogenic influences. It was observed that pesticide application increases the concentrations of three out of seven ARGs tested (ermB, aph(3′)-IIIa and tet(W)). Moreover, we noticed that the absolute abundances of sul1, vanA, ermB and blaTEM-1 resistance genes show an increase by 100- to 10,000- fold, from maturation of fresh pig faeces to manure. Outcomes of our study suggest that agricultural soil environments show a strong capacity to alleviate externally induced disturbances in endogenous ARG concentrations. Naturally occurring high concentrations of ARGs are present also in low human impacted environments represented by the indigenous resistome.