Tracking antibiotic resistance genes from vermicompost through the food chain: implications for soil-plant-animal health risk

Despite the widespread use of vermicomposting in organic agriculture, the fate of antibiotic resistance genes (ARGs) along the soil plant animal continuum remains poorly understood. Here, we constructed a multi niche system spanning manure treatment (fresh manure, earthworm gut, vermicompost), environmental compartments (soil, rhizosphere, phyllosphere), and rabbit feces, and used metagenomic sequencing to track ARG transmission under vermicompost amendment versus unfertilized controls. Our results show that vermicompost reshapes the resistome in a niche specific manner rather than uniformly reducing ARG loads. The rhizosphere exhibited the greatest shifts in ARG diversity, abundance, and community structure, alongside more complex and interconnected ARG-mobile genetic element (MGE) co-occurrence networks. These effects attenuated progressively along the ecological chain, with the rabbit gut showing the weakest response. Nevertheless, several ARG carrying pathogens, particularly Escherichia coli , persisted across niches. MGEs were closely associated with ARGs, with clinically relevant ARGs physically co localized with insertion sequences, suggesting potential for horizontal transfer. Structural equation modeling indicated that vermicompost’s effects are largely indirect, mediated through microbial and MGE diversity. Overall, vermicomposting may inadvertently facilitate the spread of high risk ARG MGE combinations along food chains, underscoring the need for One Health oriented risk assessment that considers ARG mobility and host association.