Soil management strategies drive divergent impacts on pathogens and environmental resistomes

土壤管理策略对病原体和环境抗性组产生不同的影响

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Abstract

Antimicrobial resistance (AMR) is a growing global health threat, and the genes that confer drug resistance are increasingly recognized as widespread environmental contaminants. Livestock manure, widely used as a non-synthetic fertilizer, is a potential source of AMR contamination in the environment. Manure fertilizers are well-documented reservoirs of AMR genes (ARGs) and drug-resistant pathogens. However, the role of soil management practices in shaping the persistence and spread of these genes after manure application remains poorly understood. We conducted a large-scale field experiment to evaluate how soil management practices influence the resistome (the genomic content involved in resistance to antimicrobial agents) and the overall microbiome of agricultural soils. Specifically, we ask: Does the use of composted poultry manure in organic soil management practices increase the risk of transmitting ARGs and drug-resistant pathogens? We integrated metagenomic sequencing with risk score analyses to assess the abundance, diversity, and mobility of resistance genes. Contrary to expectations, our results indicate that non-organic practices, despite not applying poultry manure, posed greater risks for transmitting AMR genes and human pathogens - due to significantly higher co-occurrence of ARGs with mobile genetic elements (MGEs), which facilitate horizontal gene transfer. In contrast, organic practices, that applied composted poultry manure, increased overall ARG and metal resistance gene (MRG) abundance, but the genes were less diverse and less mobile. These findings show that focusing solely on ARG and MRG abundance can misrepresent AMR risks and underscore the importance of evaluating gene mobility and management context when assessing AMR hazards. Our study highlights how soil management can be strategically leveraged to mitigate AMR transmission, offering actionable insights for sustainable agriculture, environmental stewardship, and public health protection.

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