Microbial communities and plasmids mediate biodegradation of polycyclic aromatic hydrocarbons (PAHs) in coastal sediments

Polycyclic aromatic hydrocarbons are persistent coastal pollutants, yet the ecological and genomic strategies governing the persistence and function of degraders under in-situ stress remain elusive. Here we decode these adaptive mechanisms using metagenomics and cultivation in the Pearl River Estuary, integrated with global comparative analyses. We reveal a multi-level adaptive strategy where high PAH stress drives ecological network densification and selectively enriches the thermodynamically favorable catechol ortho-cleavage pathway. Crucially, we elucidate a conserved genomic “division of labor”, where chromosomes encode stable upstream activation steps, while plasmids serve as specialized, mobile reservoirs for downstream central aromatic processing. This plasmid-mediated functional partitioning is globally conserved across diverse coastal ecosystems, although the reliance on mobile vectors is dynamically tuned by environmental stability. Collectively, these findings unveil a holistic adaptive framework that integrates ecological cooperation with genomic partitioning, highlighting a plasmid-mediated “plug-and-play” mechanism that underpins microbial resilience and guides precision bioremediation. Coastal microbiomes adapt to polycyclic aromatic hydrocarbon stress via a conserved genomic division of labor where chromosomes retain upstream specificity, while plasmids mobilize downstream detoxification modules, shown by sampling in China’s Pearl River Estuary.