Deep sea cold seep sediments have been discovered to harbor novel, abundant, and diverse bacterial and archaeal viruses. However, little is known about viral genetic features and evolutionary patterns in these environments. Here, we examined the evolutionary ecology of viruses across active and extinct seep stages in the area of Haima cold seeps in the South China Sea. A total of 338 viral operational taxonomic units are identified and linked to 36 bacterial and archaeal phyla. The dynamics of host-virus interactions are informed by diverse antiviral defense systems across 43 families found in 487 microbial genomes. Cold seep viruses are predicted to harbor diverse adaptive strategies to persist in this environment, including counter-defense systems, auxiliary metabolic genes, reverse transcriptases, and alternative genetic code assignments. Extremely low nucleotide diversity is observed in cold seep viral populations, being influenced by factors including microbial host, sediment depth, and cold seep stage. Most cold seep viral genes are under strong purifying selection with trajectories that differ depending on whether cold seeps are active or extinct. This work sheds light on the understanding of environmental adaptation mechanisms and evolutionary patterns of viruses in the sub-seafloor biosphere.

人们发现深海冷泉沉积物中含有新颖、丰富且多样的细菌和古菌病毒。然而，人们对这些环境中的病毒遗传特征和进化模式知之甚少。在这里，我们研究了南海海马冷泉地区病毒在活跃和灭绝渗透阶段的进化生态学。总共鉴定了 338 个病毒操作分类单元，并与 36 个细菌和古菌门相关。宿主与病毒相互作用的动态由 487 个微生物基因组中 43 个家族的不同抗病毒防御系统决定。预计冷泉病毒将拥有多种适应策略以在这种环境中持续存在，包括反防御系统、辅助代谢基因、逆转录酶和替代遗传密码分配。在冷泉病毒种群中观察到极低的核苷酸多样性，受到微生物宿主、沉积物深度和冷泉阶段等因素的影响。大多数冷泉病毒基因都处于强烈的纯化选择之下，其轨迹根据冷泉是否活跃或灭绝而有所不同。这项工作有助于理解海底生物圈中的环境适应机制和病毒的进化模式。