Nutrition cycling microbiomes drive the succession of antibiotic resistome in long-term manured soils

INTRODUCTION: The spread of antibiotic resistance genes (ARGs) in the environment has received widespread attention. Nutrition cycling microbiomes specifically refer to microorganisms capable of mineralizing nitrogen and phosphorus, which dominate the microbial community in long-term manured soils. However, changes in nutrition cycling genes/microbiomes and the mechanisms by which these microbiomes mediate ARG transfer through vertical and horizontal gene transfer remain poorly understood. OBJECTIVES: This study aimed to elucidate how nutrition cycling microbiomes mediate the dissemination and ecological risk of antibiotic resistance genes (ARGs) in long-term manure-amended soils. METHODS: Here, we employed metagenomic assembly and binning to investigate the distribution of nutrition mineralization genes, nutrition cycling microbiomes, mobile genetic elements (MGEs), and ARGs in rapeseed cake, pig manure, duck manure and their corresponding long-term amended soils. RESULTS: Long-term application of organic manures led to the dominance of nutrition cycling microbiomes associated with methanogenesis (pmoA and mmoX) and incomplete denitrification (norBC), thereby exacerbating soil nutrient loss. Nutrition cycling microbiomes, particularly Rhodanobacter and Pseudomonas, served as the primary host for ARGs and harbored multiple clinically relevant resistance genes, including MexF, ceoB, and mdtB. Notably, the abundance of ARGs in rapeseed cake and pig manure was 2.09-2.23-fold and 6.74-7.38-fold higher, respectively, than in duck manure, promoting the vertical transmission of ARGs via nutrition cycling microbiomes under long-term application. Furthermore, a significant positive correlation between nutrition mineralization genes and ARGs revealed a co-dispersal mechanism between nutrition cycling microbiomes and ARGs in long-term manured soils. CONCLUSIONS: It is concluded that the nutrition cycling microbiome plays a more prominent role in shaping antibiotic resistome through vertical transfer in manured soils, compared to horizontal gene transfer mediated by MGEs.