Diversity, transfer potential, and transcriptional activity of virus‐carried antibiotic resistance genes in global estuaries

Abstract Estuaries, the transition zones between terrestrial and marine ecosystems, are vital hotspots for antibiotic resistance genes (ARGs) due to substantial antibiotic pollution. Although viruses have been considered as reservoirs and vectors of ARGs in various environments, the composition, transmission, and ecological drivers of virus‐carried ARGs (vARGs) in estuarine ecosystems remain poorly understood. Here, we constructed a Global Estuarine Virome (GEV) dataset by recovering 136,443 viral operational taxonomic units (vOTUs) from 534 worldwide estuarine metagenomes. Based on this GEV dataset, we identified 282 (temperate: 217; lytic: 65) vOTUs that carried 462 ARGs. These ARGs encompassed 108 ARG subtypes conferring resistance to 13 antibiotic classes, with their richness and abundances in estuaries being directly and indirectly correlated with changes in temperatures and coastal human activities. Network approach further revealed temperature‐dependent vARG transfers between viruses and prokaryotes. Moreover, ARG‐carrying vOTUs could target abundant prokaryotic taxa (e.g., Rhodobacteraceae and Flavobacteriaceae ) and potential pathogens, including Acinetobacter venetianus and Pseudomonas marginalis . Notably, leveraging 188 estuarine metatranscriptomes, we found that over half of the vARGs (51%) were active in estuaries, and the expression levels of vARGs were sometimes comparable to their prokaryotic counterparts. The relative contribution of viruses to ARG expression also increased under warmer conditions. Overall, although the ARGs were only detected in a small fraction (0.2%) of the estuarine vOTUs, this study reveals that the potential risks of vARGs in estuarine ecosystems warrant attention, especially in the context of global warming and socioeconomic development. This underscores the necessity of incorporating vARGs into future surveillance and management of estuaries.