Extensive halogenated organic compound reservoirs and active microbial dehalogenation in Mariana Trench sediments

The hadal trenches, the deepest regions of the ocean, serve as the final sinks for marine particles and "tunnels" for material exchange between the ocean and Earth's interior. Despite their extreme conditions, the trench sediments contain high content of organic carbon and active microbial carbon turnover, are hotspots for deep-sea organic carbon degradation and unique microbial processes. However, little is known about the organic carbon components and microbial metabolisms driving their degradation in trench sediments. This study provides the first comprehensive quantification of total halogenated organic compounds (organohalides) in Mariana Trench sediments. The measured bulk organic halogen concentrations exceeded all previously reported individual compounds by orders of magnitude, with a mean stoichiometric ratio of 1:49 (halogen:carbon) in the sedimentary organic carbon pool. These findings suggest the trench sediments may represent a significant reservoir for organohalides. Metagenomic analysis of global ocean data shows significant enrichment of the genes for organohalides biodegradation (dehalogenation) in trench microbiomes than those in other marine environments. Putative dehalogenating microorganisms in trench sediments encompassed 16 phyla and 52 orders, capable of metabolizing 18 structurally diverse organohalide compounds, revealing an unexpectedly broad phylogenetic distribution of organohalides metabolism and versatile substrate specificity among trench microbial communities. High pressure microcosm experiments demonstrated rapid degradation of typical organohalide compounds and transcription of genes related to organohalides metabolisms, confirming an active organohalides degradation by trench microorganisms. These findings underscore the role of organohalides metabolism in organic carbon remineralization in hadal trenches, advancing our understanding of deep-sea carbon cycling and microbial survival.