Unveiling the dynamic viral landscape across developmental stages of cold seep ecosystems: Implications for global marine biogeochemistry.

Cold seeps are methane-rich ecosystems playing pivotal roles in global biogeochemical cycling, yet their viral communities remain underexplored. We present the first comprehensive viral metagenomic analysis across developmental stages of the Haima Cold Seep. Characterizing viral assemblages from chemoautotrophic, mature, and extinct seep sediments revealed 4272 viral operational taxonomic units, with 77 % representing novel lineages, highlighting cold seeps' unique viral diversity. Viral community structure and diversity varied significantly by seep stage, with highest diversity in the chemoautotrophic stage. While Siphoviridae and Microviridae dominated, their relative abundances shifted with maturity. Gammaproteobacteria emerged as predominant viral hosts, exhibiting distinct interaction patterns across stages. Notably, the chemoautotrophic stage harbored the highest abundance and diversity of virus-encoded auxiliary metabolic genes (AMGs; ∼450 AMGs), with significantly enriched carbohydrate metabolism and central carbon pathway genes (2.2-fold and 1.8-fold higher respectively, p < 0.005), amino acid metabolism (1.9-fold, p = 0.003), and sulfur relay system genes (2.0-fold, p = 0.002). In contrast, the mature stage exhibited distinct enrichment in energy metabolism genes (up to 3.9-fold difference between sites, p < 0.001) and xenobiotics degradation pathways, suggesting stage-specific viral impacts on biogeochemical cycling. Lytic lifestyles prevailed across stages, indicating dynamic virus-host interactions during seep development. These findings unveil complex viral ecology in cold seeps, with potential influences on microbial community structure and biogeochemical processes. Providing a foundation for understanding viral roles in cold seep ecosystem functioning and biogeochemical cycles, this study has implications for marine microbial ecology and environmental biotechnology.