Hydrothermal ecosystems, including marine hydrothermal vents and terrestrial hot springs, are extreme environments characterized by high temperatures, extreme pH, and sharp redox gradients. These ecosystems support a diverse and distinctive microbial community that has adapted to these extreme conditions through a range of strategies. Notably, the viral community structure and environmental response mechanisms within these ecosystems have received relatively limited attention. Here we analyzed over 580 metagenomic and metatranscriptomic datasets from globally distributed hydrothermal systems, identifying 47,547 viral operational taxonomic units (vOTUs). Our findings revealed a vast diversity of viruses, including thermophilic and hyperthermophilic viruses, many of which were novel and demonstrated remarkable adaptations to extreme conditions, such as high genomic GC%, high mutation rates, lysogenic infections, and the encoding of stress-response genes. Viruses contribute to host adaptation by encoding auxiliary metabolic genes (AMGs) involved in protein refolding, DNA repair, and oxidative stress mitigation, thereby enhancing host survival under extreme conditions. Notably, our research revealed that thermophilic and hyperthermophilic Caudoviricetes exhibit distinct responses to high temperatures. Our research elucidated the environmental pressures shaping viral communities and their adaptation strategies, as well as the connectivity of viruses across different hydrothermal vents and the dispersal of viruses to various ecosystems on a global scale.  These findings provide new insights into the ecological and evolutionary roles of viruses in hydrothermal systems, highlighting their contributions to the resilience and diversity of life in extreme environments. Furthermore, the discovery of heat-stable enzymes encoded by these viruses offers potential applications in biotechnology and molecular biology.

Hydrothermal environments,Viruses,Stess response,Extremophiles