Microbial communities in coastal marine ecosystems are constantly shaped by environmental disturbance, yet how such pressures coordinate ecological and evolutionary responses across viruses and their microbial hosts remains poorly understood. Here we integrated cross-domain metagenomic and population genomic analyses of prokaryotic, eukaryotic and viral communities. Our results reveal that marine ranching-associated disturbance drives a clear ecological restructuring: prokaryotic connectivity decreased, whereas the centrality of eukaryotic and viral components increased in the water column. Functionally, viral auxiliary metabolic genes (AMGs) showed enhanced contributions to carbon, nitrogen, phosphorus, and sulfur cycling, while host-encoded metabolic potential remained stable or declined—highlighting a shift in metabolic burden toward viruses. At the microevolutionary level, both viral and prokaryotic populations exhibited a significantly elevated ratio of nonsynonymous to synonymous polymorphisms accompanied by reduced linkage disequilibrium, indicating coordinated responses under disturbance. Furthermore, the density of single-nucleotide variations in functional genes across multiple metabolic categories was significantly associated with total nitrogen, temperature and pH. Collectively, this study advances current understanding of virus-host interactions and functional adaptation in coastal microbial communities, emphasizing the previously underappreciated role of viruses in mediating both ecological and evolutionary responses to environmental disturbance.

Keywords: marine ranching; virus-host interactions; viral auxiliary metabolic genes; microevolution; coastal ecosystem