Biodegradable microplastics show greater potential than conventional types in facilitating antibiotic resistance gene enrichment and transfer through viral communities

Whether and how conventional (CP) and biodegradable microplastics (BP) affect viral communities and virus-carried antibiotic resistance genes (ARGs) in agricultural soils remains largely unknown. Here, we established a soil microcosm incubation with addition of 1 % (w/w) microplastics (MPs) in maize-cultivated soil that had been treated with different fertilizers for over 10 years, and the dynamic variations of viral communities and ARG profiles were investigated using a combination of metagenomic and metatranscriptomic methods. Our results revealed that BP, but not CP, significantly decreased viral α-diversity, changed viral community structure, community resistance and taxonomic turnover in all fertilized treatments. Caudoviricetes was the most dominate viral class and BP significantly increased the abundances of viral families (i.e. Phycodnaviridae) in all fertilized treatments, while CP altered the viral family abundance mainly observed in manure-amended soils. Also, BP was associated with increased ARG α-diversity, altered ARG community structure and community resistance, especially at the transcriptional level. Particularly, BP significantly enriched high-risk ARGs and mobile genetic elements (MGEs) in soils regardless of fertilization regimes. Correlation analysis revealed the important role of lytic viruses in shaping the abundance of high-risk ARGs and MGEs. Furthermore, BP induced more variations in reconstructed metagenome-assembled genome (MAGs), and significantly enriched high-risk ARGs carried by phage genomes. Co-occurrence patterns revealed three Actinobacteriota MAGs as primary viral hosts sharing high-risk ARGs with phages and containing multiple MGEs. Notably, we identified four viral genomes carrying ARG transcripts identical to their hosts. Both CP and BP differentially stimulated ARG expression in these virus-host systems, with markedly stronger effects observed in manure-amended soils. In conclusion, this study revealed a high risk of ARG dissemination induced by biodegradable MP residues regardless of fertilization regimes, while conventional MPs strengthen the ARG health risks mainly in manure-amended soils.