Deep-sea hydrothermal regions host vital chemosynthetic ecosystems supporting unique extreme life. A key factor underpinning the establishment and maintenance of thriving communities lies in the sharp chemical and thermal gradient created by vigorous mixing between venting fluid and oxygen-rich seawater, characterized by drastic variations in redox potential, pH, and temperature. To systematically investigate how microbial composition and function evolve along hydrothermal gradient, we implemented human-occupied vehicle (HOV)-guided gradient sampling strategy across 15 global hydrothermal regions, including Tianxiu (Carlsberg ridge, northwest Indian ocean), Logatchev (mid-Atlantic ridge), Semyenov (mid-Atlantic ridge), Longqi (southwest Indian ridge), Onnuri (Central Indian ridge) and Ashadze (mid-Atlantic ridge). Within each region, push-core sediment and chimney samples were collected along the path of declining hydrothermal activity to capture the environmental and microbial transition from active to inactive hydrothermal conditions for deep metagenomic sequencing. As a result, 280 sequencing metagenomes (>50 Gbp paired-end data per sample) yielded 31,454 mid-quality metagenome-assembled genomes (completeness > 50%, contamination < 10%) spanning in 157 microbial phyla. Primary composition and functional profile revealed that pronounced microbial heterogeneity existed within distance of a few hundred meters to active venting sites, exceeding those observed between different ridge systems. Distinct functional shifts in lifestyle-related traits, carbon fixation, and organic degradation were detected, indicating the transitions of microbial survival strategies from active exploitation of resource-rich and dynamic hydrothermal activities to passive adaptation to oligotrophic deep-sea conditions. Ultimately, these findings underscore that hydrothermal activities are fundamental drivers of long-term microbial persistence and evolution, rather than barriers of life. In addition, the hydrothermal genomic resource reported here is also expected to expand the knowledge of microbial diversity and evolutional dynamics in extreme marine habitats, and provide a scientific basis for the conservation of invaluable deep-sea ecosystem in the context of growing deep-sea mining activities.

 

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