The hadal ocean, with depths exceeding 6,000 m, is characterized by extreme high pressures and unique funnel-shaped topography. This depocenter for organic materials accumulates matter through vertical sedimentation and lateral transport, enriching diverse heterotrophic microorganisms. However, our understanding of how these enigmatic microbial ecosystems are fueled is still limited. Through combined culture-dependent and culture-independent methods, we investigated the microbial community compositions, metabolic capabilities and evolutionary trajectories in the hadal waters and sediments of the Mariana Trench. The hadal waters harbored distinct microbial communities capable of degrading hydrocarbon and cell-wall derived polysaccharides under physiologically relevant conditions, suggesting the accumulation of structurally complex organic “leftovers” that may serve as significant carbon sources for these microorganisms. Additionally, high-rate episodic sedimentation events triggered by earthquakes introduced large amounts of "old carbon" and microbial cells into the hadal bottom sediments, significantly altering the subseafoor microbiosphere by promoting the growth and extracellular enzymatic activity of in situ microbial communities. Correspondingly, aerobic and anaerobic hydrocarbon-degrading capabilities were observed in hadal subseafloor microorganisms. Furthermore, significant adaptive evolution occurred in microorganisms transported to the hadal ocean. Using ammonia-oxidizing archaea as an example, we provided evidence for a direct niche expansion into the hadal realm from the coastal/surface ocean rather than from the mesopelagic/bathypelagic waters that are spatially closer to the hadal zone. These findings are crucial for understanding microbial ecology and evolution in these extreme hadal environments and the biogeochemical processes they drive.

carbon degradation,evolutionary adaptation,hadal trench,deep ocean