Redox-stratified macromolecule degradation supports microbial survival in the oligotrophic Kermadec Trench sediments

Abstract Kermadec Trench is a hadal ecosystem in the South Pacific with the water depth 10,047 m. The trench bottom harbors a highly active and populated microbial community, despite the surface sediment is characterized as extremely pressurized, oligotrophic and with low oxygen concentration. It is intriguing, as well as technically challenging, to investigate the microbial adaptation strategies therein. Here we performed the in situ RNA fixation on sediment samples with the assistant of Fendouzhe manned submersible, to approach natural status of microbial metabolisms on both genomic and transcriptomic levels. We reconstructed 1369 metagenome-assembled genomes (MAGs), revealing dominant heterotrophic lineages encoding carbohydrate-active enzymes targeting complex macromolecules such as peptidoglycan and β−1,4-mannan. These degradation processes were transcriptionally coupled with flexible respiratory pathways utilizing oxygen, nitrate, and nitrite as electron acceptors. Co-expression analyses and microbial co-occurrence networks demonstrated niche partitioning driven by redox stratification, with slope communities favoring oxidative pathways and bottom communities enriched in reductive metabolisms, including denitrification and N₂O reduction. Despite compositional divergence, both habitats exhibited conserved functional strategies centered on macromolecule recycling and redox-coupled respiration. Our findings highlight a coordinated system of organic matter remineralization and electron acceptor versatility that underpins microbial survival in Earth’s deepest seafloor ecosystems.