Increased Transmission of Antibiotic Resistance Occurs in a Soil Food Chain under Pesticide Stress

Abstract

The rising spread of antibiotic resistance is a global concern, but the pathways of dissemination within soil ecosystems remain poorly understood. Here, we quantified the occurrence of antibiotic resistance genes (ARGs) in gut microbiomes of soil collembolans (Folsomia candida) under pesticide stress (zinc thiazole, ZT) and analyzed the trophic transfer of ARGs to the microbiomes of predatory mites (Hypoaspis aculeifer), natural predators of collembolans. High throughput quantitative PCR was used to quantify ARGs, whereas gut microbiomes of collembolans and mites were characterized using 16S rRNA gene amplicon sequencing, and potential pathogens were identified. Our results revealed that ZT exposure significantly elevated the abundance of ARGs (e.g., AAC(6’)-Ir) in soil collembolan microbiomes. With the increase of ARGs in prey collembolan microbiomes, an increase of ARGs in predatory mite microbiomes was observed through trophic transfer. Mobile genetic elements (MGEs) significantly contribute to the transmission of ARGs within this food chain. Additionally, co-occurrence analysis indicated a strong association between gut resistomes and pathogens, such as Brevundimonas diminuta, in the collembolans and predatory mites. Overall, our study provides evidence for the dissemination of ARGs through the collembolan-predatory mite food chain following pesticide exposure, which is important for understanding the broader dynamics of antibiotic resistance spreading in soil ecosystems.