Resistome flow in global landfill systems

Antibiotic resistance genes (ARGs) represent a critical global public health threat. Effective resistome management within the One Health framework requires a comprehensive understanding of the sources and movement of ARGs across environmental media. This study provides a detailed analysis of resistome characteristics and dynamics in global landfill systems. Landfill systems were found to harbor diverse and highly mobile ARGs, with multidrug-resistant genes (MDRGs) comprising 32.63% of total ARGs, and comparable or even higher levels of associated ARG subtypes than in other environmental media, such as acidic mine wastewater. The ARG density on plasmids was 3.5 times higher than that on chromosomal sequences, with five times more abundant ARG-carrying plasmid-associated contigs in landfill systems than that in wastewater. At the metagenome-assembled genome level, members of the phylum Pseudomonadota were identified as the most abundant hosts (29.72%), harboring 47.74% and 56.47% of the total ARGs and MDRGs, respectively. Genomic analysis of 35 Pseudomonas spp. strains revealed unique Pseudomonas species in landfill systems, including P. aeruginosa. Resistome flow pathways were further mapped, including inflows into landfill (via soil, wastewater, freshwater, and the human and pig gut), movement within landfills (across landfill refuse, leachate, and airborne particles), and outflows from landfills (via landfill leachate effluent, gas emissions, and refuse evacuation). The results emphasized diverse resistome development and movement within landfill systems, ultimately contributing to the environmental spread of ARGs. Thus, our study highlights the urgent need for comprehensive policies and management strategies to mitigate resistome proliferation at every stage of municipal solid waste management.