Enrichment of halogenated organic compounds and their degrading microorganisms in the deepest ocean

The hadal trenches, the deepest regions of the ocean, serve as the final resting place for marine particles and as "tunnels" for material exchange between the ocean and Earth's interior. Despite their extreme conditions, the trenches contain high content of organic carbon (OC) and active microbial carbon turnover, are hotspots for deep-sea OC degradation and unique microbial processes. However, little is known about the OC components and microbial metabolisms driving the OC degradation in the trenches. This study reveals unexpectedly high concentrations of halogenated organic compounds (HOCs) in the Mariana Trench sediments, with about 1 halogen per 58 carbon atoms in the OC pool. Systematic analysis of deep-sequenced metagenomes and metagenome-assembled-genomes from the global ocean shows significantly higher abundance of the genes for biodegradation of HOCs (dehalogenation) in trench microbes, with microorganisms capable of dehalogenation belonging to 16 phyla and 52 orders, 75% of which identified as HOCs degraders for the first time. Microcosms simulating trench conditions showed rapid degradation of typical HOCs and transcription of genes related with HOCs metabolisms, demonstrating the active HOCs degradation by the trench microorganisms. The findings suggest the HOCs metabolism as an important process in the OC remineralization of deep-sea trenches, advancing understanding of deep-sea carbon cycling and microbial survival strategies.