Soil co-occurring bacterial communities serve as assembly hubs of antibiotic resistance determinants under organic...

Environmental transmission of antibiotic resistance poses a significant threat to human health by undermining the efficacy of therapeutic interventions against bacterial infections. Agricultural practices, particularly the application of organic fertilizers derived from animal manure, are major contributors to the spread of antibiotic resistance determinants (ARDs) in soil ecosystems. However, the fates of ARDs and their bacterial hosts in soil following organic fertilization as well as the impact of water management regimes remain poorly understood. We investigated the attenuation and persistence of ARDs in soil following organic fertilization under water management practices of upland, continuous flooding, and intermittent flooding. Most ARDs introduced via the organic fertilizer exhibited significant attenuation, with half-lives ranging from 19 to 50 days, primarily due to the decline of fertilizer-derived bacterial hosts. Specific ARDs, such as aph(3')-IIIa and tetO, persisted across all treatments. Upland conditions accelerated the attenuation of ARDs and their pathogenic hosts compared to flooding conditions, which prolonged their survival and promoted horizontal gene transfer. The divergent responses of ARD composition and soil bacterial communities to the environmental variables revealed a unique dissemination pattern, wherein the soil co-occurring bacterial communities served as critical hubs for the dissemination of ARDs and their bacterial hosts from organic fertilizers. The soil co-occurring bacterial communities exhibited strong interspecies interactions and high sensitivity to environmental changes. Targeted strategies to disrupt these assembly hubs may provide an effective way to mitigate the spread of antibiotic resistance from organic fertilizers to soil ecosystems.