Quantitative microbial risk assessment of antibiotic resistance genes and mobile genetic elements in orchard soils across South Korea

Abstract

Antibiotic resistance is a global health crisis, but environmental pathways of resistance dissemination to farm workers remain poorly understood. Agricultural soils represent critical but underexplored reservoirs of antibiotic resistance genes (ARGs) and mobile genetic elements (MGEs), particularly in orchards where antibiotics such as streptomycin and oxytetracycline are widely used for fireblight control. Here, we conducted a nationwide investigation of orchard soils in South Korea, integrating high-throughput qPCR, 16S rRNA gene sequencing, and quantitative microbial risk assessment (QMRA). We detected 297 ARGs and 52 MGEs, with eight core genes [aac(3)-VIa, tetL, aadE, sul1, qacH_351, tnpA-1, IS6100, and intI1] significantlyenriched in orchard soils but absent in non-orchard soils, such as national parks or mountain soils. Aminoglycoside- and tetracycline-resistance genes were dominant, directly reflectingthe application of streptomycin and oxytetracycline. QMRA estimated that orchard farmers ingest resistance genes through soil contact, with aac(3)-VIa posing the highest risk (∼29 ingestion events per farmer annually), followed by qacH_351, tetL, and tnpA-1. These results demonstrate the quantifiableoccupational risks of ARG exposure in orchard environments. By combining resistome profiling,microbial networks, and QMRA, this study establishes a framework for assessing the public health implications. Although the ingestion of ARGs may not immediately cause impacts on human health, such exposure has the potential to enrich antibiotic resistance within the gut microbiome of farm workers, thereby increasing the probability of treatment complications if infections occur.