Microplastic-driven carbon availability differentiates phage-host interactions in shaping soil resistome

The growing prevalence of microplastics (MPs) in agroecosystem has raised significant concerns regarding their ability in facilitating the dissemination of antibiotic resistance genes (ARGs). Biodegradable and nondegradable MPs exhibited inherently different degradation rates, resulting in divergent carbon bioavailability that might trigger distinct microbial response and ARG profiles. Here, by integrating multi-omics (metagenomics, virome, and metatranscriptomics) with experimental validation, we explored how microbial responses to MPs impacted ARG dissemination in a long-term field experiment. We showed that both biodegradable and nondegradable MPs significantly increased ARG abundance and transcriptional activity, differing in the drive mechanisms. Biodegradable MPs triggered bacterial oxidative stress and DNA damage response, increasing mobile genetic elements abundance and horizontal gene transfer of ARGs. Accordingly, increasing proportion of lysogenic phages and intensified phage-host interactions might promote ARG transduction through lysogenic conversion. In contrast, nondegradable MPs increased recalcitrant carbon, which enriched bacteria harboring genes for complex compound degradation. ARG-carrying bacteria within these taxa gained fitness advantages, facilitating their enrichment and ARG proliferation. Concurrently, phages infecting ARG-carrying bacteria encoded more auxiliary metabolic genes in complex carbohydrate metabolism, thereby enhancing host competitiveness and promoting ARG spread. In vitro validation experiments confirmed that lysogenic phages facilitated transduction of ARGs under biodegradable MPs, while phage-encoded auxiliary metabolic genes conferred growth advantages on ARG-carrying bacteria utilizing recalcitrant carbon source, consistent with conditions induced by nondegradable MPs. Our findings clarify how phages differentially impacted ARG profiles under biodegradable and nondegradable MPs, underscoring the importance of considering phage-mediated processes in assessing the risks of MPs and ARG dissemination.