The Kermadec Trench is a hadal ecosystem in the South Pacific, reaching 10,047 m water depth and characterized by permanent darkness, extreme hydrostatic pressure, and strong habitat differentiation between trench slopes and the trench axis. In contrast to more productive trench systems, the overlying waters of the Kermadec Trench have low primary productivity of approximately 380 mg C m⁻² d⁻¹, and sedimentary total organic carbon is only 0.21–0.35 wt%. Together with shallow oxygen penetration of around 10 cm, these conditions create a carbon-limited and redox-constrained environment, raising a central ecological question: how do microbial communities sustain metabolic activity in oligotrophic hadal sediments.
Here, we integrated 42 metagenomes and 16 metatranscriptomes, including in situ RNA-preserved sediment samples collected by the Fendouzhe manned submersible, to investigate both the metabolic potential and transcriptional activity of microbial communities in the Kermadec Trench. We reconstructed 1,369 metagenome-assembled genomes and observed clear community differentiation between slope sediments shallower than 9 km and bottom sediments deeper than 9 km. Heterotrophic lineages dominated the community and encoded diverse carbohydrate-active enzymes targeting structurally complex macromolecules, including peptidoglycan, sialylated polysaccharides, and β-1,4-mannan. The transcription of these degradation genes, together with their association with central carbon metabolism, indicates that microbial necromass and refractory detrital polymers are important substrates supporting microbial activity.
Among the 651 MAGs predicted to utilize macromolecules, metatranscriptomic profiles indicated active expression of genes associated with respiratory flexibility, suggesting a functional coupling between refractory organic matter degradation and redox-stratified energy metabolism. Rather than relying solely on oxygen, these populations expressed pathways linked to alternative electron acceptors, particularly nitrate- and nitrite-related respiration, with bottom communities showing stronger reductive signatures than slope communities. These findings suggest that microbial survival in the Kermadec Trench is supported by coordinated macromolecule recycling and redox-adapted respiration. By linking genome-resolved functional potential with in situ gene expression, this study provides insight into how hadal microbial biodiversity mediates organic matter remineralization in carbon-limited deep-ocean ecosystems, with implications for predicting their responses to future changes in organic matter supply and redox conditions under a changing climate.