High Hydrostatic Pressure Activates Microbes to Accelerate Deep-Sea Carbon Recalcitrance

The recalcitrant dissolved organic carbon (RDOC) pool in the deep ocean is crucial for long-term carbon sequestration, yet the mechanisms sustaining its stability below 1,000 m remain unclear. While high hydrostatic pressure (HHP) is traditionally viewed as inhibiting microbial activity, its role in regulating DOC transformation is poorly resolved. Here, we isolated the effect of pressure by incubating natural deep-sea DOC with a hadal microbial consortium across a gradient of 20–115 MPa at 4 °C, simulating depths from 2,000 to 11,000 m.

Over 25-day incubations, bulk DOC concentrations remained stable, yet microbial biomass exhibited a non-linear pressure response, peaking at intermediate pressures (20–60 MPa) and declining under higher pressures. Molecular-level analysis via FT-ICR MS revealed that increasing pressure systematically shifted the DOC pool toward higher oxidation states and O/C ratios, lower H/C ratios, and enrichment of carboxyl-rich, heteroatom-poor compounds. These changes were potentially driven by pressure-stimulated formation and persistence of thermodynamically stable DOC, rather than preferential removal of labile substrates. Metagenomic and metatranscriptomic analyses further indicated that HHP enhances oxidative stress responses and upregulates high-energy carbon oxidation pathways, suggesting microbial metabolic reprogramming toward energy maximization under extreme conditions.

Our findings demonstrate that HHP actively reprograms deep-sea microbial metabolism to accelerate DOC recalcitrance, transforming the deep biosphere into an active driver of long-term carbon storage. This challenges the paradigm of the deep sea as a passive carbon reservoir and underscores the need to incorporate pressure-dependent microbial metabolic flexibility into carbon cycle models to better predict oceanic carbon responses under global change.