A global atlas of deep-sea cold seep viruses uncovers extensive genomic novelty, pervasive viral dark matter, and biotechnological potential

Cold seeps are globally distributed deep-sea ecosystems hosting diverse chemosynthetic microbiomes, yet their viral communities remain poorly characterized. Here, we establish the Global Cold Seep Virome (GCSV), a comprehensive catalog of 193,465 species-level viral operational taxonomic units (vOTUs) and over five million viral proteins reconstructed from 314 short- and long-read metagenomes across 18 seep sites. More than 99% of vOTUs are unique relative to existing environmental viromes, revealing an exceptionally novel viral reservoir shaped by low microdiversity and strong purifying selection. Host prediction and phylogenomics uncover a disproportionately rich archaeal viral component, including extensive viral lineages associated with Halobacteriota, Asgardarchaeota, and DPANN archaea. Structure-based annotation of 2.56 million viral protein clusters reveals pervasive viral dark matter and ecologically specialized hallmark genes, including hydrophilic and flexible major capsid proteins and terminases potentially adapted to deep-sea pressure and temperature. We identified 7,154 auxiliary metabolic genes linked to carbon fixation, methane oxidation, alkane degradation, and sulfur, nitrogen, and phosphorus transformations, suggesting that viruses modulate key pathways underlying seep biogeochemistry. Cold seep viruses also encode a broad anti-defense repertoire targeting diverse prokaryotic immunity systems, with functional assays confirming potent antagonism of Thoeris, Gabija, and CBASS defenses. Finally, we predicted 15,710 viral lysins, including experimentally validated enzymes with strong antibacterial activity and structurally novel domain architectures. Overall, the newly discovered viral diversity in cold seeps broadens our understanding of viral contributions to ecosystem function and microbial metabolism, and offers a rich repertoire of viral proteins for future mechanistic studies and biotechnological applications.