Depth-governed ecological and evolutionary partitioning of ocean trench viromes

Viruses influence microbial mortality and carbon flux in the ocean, yet how water-column depth shapes their ecology and evolution from surface waters to the hadal zone remains unexplored. To address this gap, we profiled a continuous 2–6,000 m transect in the Yap Trench in the Pacific Ocean, amongst the world’s deepest ocean trenches using depth-resolved metagenomics. We reconstructed a total of 8,520 viral operational taxonomic units and observed the viral communities to be strongly stratified, with diversity peaking in the mesopelagic. Virulent Kyanoviridae dominated upper layers, while temperate Peduoviridae increased and stabilized with depth, indicating a shift from "kill the winner" to "piggyback the winner" dynamics. Auxiliary metabolic genes mirrored this partitioning but were less defining than lifestyle transitions. Viruses infecting Gammaproteobacteria and Firmicutes encoded cell motility and stress-response genes, suggesting adaptation to energy limitation. Evolutionary dynamics were depth-dependent: mutation rates declined with depth, while positive selection intensified in key viral genes. Overall, our results identify ocean depth as a central axis shaping viral community dynamics and evolutionary trajectories in marine ecosystems.