Metagenomic insights into the characteristics and co-migration of antibiotic resistome and metal(loid) resistance genes in urban landfill soil and groundwater.

The heavy metals and antibiotic resistance genes (ARGs) in landfills showed a significant correlation; however, the relationship between metal(loid) resistance genes (MRGs) and ARGs in contaminated environments, as well as whether they co-migrate with human pathogenic bacteria (HPB), remains unclear. This study is the first to report the characteristics and co-migration of ARGs and MRGs in the soil and groundwater of aged urban landfill sites. Our findings indicated that quinolone, efflux, and macrolide-lincosamide-streptogramin represented the most abundant ARGs identified. Notably, ARG abundance was higher in groundwater compared to soil, with subtype diversity reflecting a similar trend; however, microbial diversity in soil was greater. Metagenome-assembled genomes data indicated a higher risk of antibiotic-resistant HPB in groundwater. It is imperative to focus on HPB that co-carry ARGs and MRGs alongside mobile genetic elements (MGEs), such as Ralstonia pickettii and Pseudomonas stutzeri. Genes conferring resistance to copper and mercury, as well as MGEs such as qacEdelta and intI1, played a critical role in promoting horizontal gene transfer of antibiotic resistance. MRG may promote ARG migration by affecting the permeability of the cell membrane. Procrustes analysis revealed a strong similarity (87 %) between heavy metals and MRG structures. Variance partitioning analyses demonstrated that both heavy metals and biological factors jointly governed landfill ARGs (96.2 %), exerting a more substantial influence in groundwater than in soil. This study serves as a reference for managing landfill, while emphasizing the importance of addressing the co-migration of MRGs and ARGs in pathogens when controlling the spread of risks.