Phylogenetically and structurally diverse reductive dehalogenases link biogeochemical cycles in deep-sea cold seeps

Abstract

Reductive dehalogenation is crucial for halogen cycling and environmental remediation, yet its ecological role is incompletely understood, especially in deep-sea environments. To address this gap, we investigated the diversity of reductive dehalogenases (RDases) and ecophysiology of organohalide reducers in deep-sea cold seeps, which are environments rich in halogenated compounds. Through genome-resolved metagenomic analysis of 165 global cold seep sediment samples, we identified four types of RDases, namely prototypical respiratory, transmembrane respiratory, and cytosolic RDases, and one novel clade. These RDases are encoded by physiologically diverse microbes across four archaeal and 36 bacterial phyla, significantly broadening the known diversity of organohalide reducers. Halogen geochemistry, metatranscriptomic data, and metabolomic profiling confirm that organohalides occur at as high as 18 mg/g in these sediments and are actively reduced by microorganisms. This process is tightly linked to other biogeochemical cycles, including carbon, hydrogen, nitrogen, sulfur, and trace elements. RDases from cold seeps have diverse N-terminal structures across different gene groups, and reductive dehalogenase genes in these environments are mostly functionally constrained and conserved. Altogether, these findings suggest that reductive dehalogenation is a central rather than supplemental process in deep-sea environments, mediated by numerous diverse microbes and novel enzymes.