Environmental gradients shape viral-host dynamics in the Pearl River estuary

Marine viruses play critical roles in shaping microbial communities and driving biogeochemical cycles, yet their dynamics in estuarine systems are not well characterized. Here, we conducted a comprehensive metagenomic analysis of viral communities and virus-host interactions across the Pearl River estuary, a dynamic subtropical estuary in southern China. Using 24 metagenomic libraries from eight sampling sites, we identified 29,952 viral populations, with Uroviricota and potential Uroviricota accounted for 80.48% of taxa, underscoring their ecological importance. A key finding of our integrated analysis is the unexpectedly high abundance of nucleocytoplasmic large DNA viruses in offshore waters, which suggests a more significant role for eukaryotic viruses in coastal ecosystems than previously acknowledged and correlates with elevated levels of their eukaryotic hosts. Environmental variables, particularly salinity and nutrient availability, emerged as key drivers of viral and host distribution patterns. By linking environmental gradients to distinct community "envirotypes" and their underlying genomic features, we revealed novel virus-host interactions and highlighted the impact of environmental gradients on microbial ecology. Additionally, viral auxiliary metabolic genes linked to phosphorus and nitrogen metabolism suggest critical roles in modulating host metabolic pathways and influencing nutrient cycling. Our findings demonstrate how spatial heterogeneity and environmental gradients shape viral and microbial ecology in estuarine ecosystems. Our findings provide a holistic, multi-domain view of microbial and viral ecology, demonstrating how integrating prokaryotic, eukaryotic, and viral community analyses offers a more complete understanding of ecosystem function in these critical transition zones.