Microbially-mediated halogenation and dehalogenation cycling of organohalides in the ocean.

Abstract

Microbially mediated organohalide cycling in the ocean has profound implications for global biogeochemical cycles and climate, but the geographic distribution and diversity of the halogenation-dehalogenation cycling microorganisms remain unknown. Here, we constructed an organohalide-cycling gene database (HaloCycDB) to explore the global atlas of halogenation-dehalogenation cycling microorganisms and genes from 1473 marine metagenomes. Strikingly, 6204 out of 15,252 metagenome-assembled genomes (MAGs) carry organohalide-cycling genes, of which 84.30% are dehalogenating populations. Microorganisms of Pseudomonadota with even spatial distribution dominate both halogenation and dehalogenation potentials in the ocean, in contrast to lineages of Asgardarchaeota and Thermoproteota solely mediating dehalogenation in the Northern hemisphere. Notably, 80.91% of reductive dehalogenase (RDase) genes and 91.35% of RDase-containing prokaryotes represent uncharacterized lineages, substantially expanding known dehalogenation diversity. Further integration of microbial cultivation, protein structure prediction, and molecular docking revealed four unique "microorganism-RDase-organohalide" patterns for marine dehalogenation and its coupling with carbon/sulfur cycles, being distinctively different from their terrestrial patterns. These results advance our understanding of microbial organohalide cycling by providing insights into the halogenation-dehalogenation microbiomes in the ocean.