Pollution duration drives divergent pathways of antibiotic and metal resistance gene dissemination in coastal mangrove sediments.

Coastal mangrove sediments are critical reservoirs of antibiotic and heavy metal resistance genes (ARGs/HMRGs). Yet, how pollution history shapes their dissemination remains unclear. We elucidated this by comparing sedimentary resistomes across three distinct ecosystems: a pristine site (BH), a site under mid-term copper stress (BHCu), and a chronically multi-polluted site (FT). Chronic multi-pollution generated a persistent co-resistance reservoir, significantly enriching ARGs, HMRGs, mobile genetic elements (MGEs), and transferable ARG-MGE clusters. Bioavailable metal fractions cooperated with MGEs to promote horizontal gene transfer (HGT) and resistome dispersal, despite limited direct ARG-HMRG co-selection, and restructured communities toward MGE-rich, cross-resistant taxa. In contrast, the three-year Cu treatment increased bioavailable Cu and enriched stress-response genes, but showed little MGE enrichment and no significant ARG-HMRG networks; resistance spread depended mainly on vertical selection within tolerant specialist taxa. The pristine site maintained low, stochastic resistance, intrinsic regulation of ARGs/HMRGs, and suppressed MGE activity in a diverse, stable community. Multivariate analyses further showed that host-MGE and duration-metal interactions dominated resistome variation, with metal speciation providing a key mechanistic link. Pollution duration therefore governed resistome architecture: chronic exposure transformed mangroves into resistance hotspots via co-reservoir expansion and HGT-driven dispersal, whereas mid-term Cu stress caused transient disruption without sustained transfer capacity. This "pollution gradient-time scale" paradigm identifies duration as a fundamental but neglected parameter for forecasting environmental resistome risks.