Sulfur oxidation through rDsr in a novel Sox-free marine Roseobacter lineage

Abstract

Sulfur oxidation is an essential biogeochemical process in coastal sediments. Of the two typical sulfur-oxidizing metabolic pathways, the reverse dissimilatory sulfite reductase pathway (rDsr) is recognized for its superior energy conservation efficiency compared to the Sox multi-enzyme system and thus might be important in intertidal habitats where electron acceptors are periodically limited. Here, we isolated 10 intertidal sediment strains that compose a novelRuegerialineage in the globally abundant marine Roseobacter group. They possess a complete rDsr pathway but lack the entire Sox system, whereas all known sulfur-oxidizing Roseobacters rely on Sox. In fact, rDsr-carrying but Sox-free bacteria are rare among all sequenced bacterial genomes (only 20 out of 35798), and how sulfur oxidation is driven exclusively by rDsr has not been investigated. Physiological assays, sulfur intermediate measurements, and transcriptomic analyses reveal that rDsr activation in thisRuegerialineage occurs exclusively under microaerobic conditions and is coupled with thiosulfate oxidation in tandem with denitrification. Metagenomic analysis shows that rDsr sequences are enriched in marine habitats characterized by oxygen depletion, consistent with our physiological data. Further, theRhodobacteralesorder whereRuegeriabelongs accounts for approximately 5% of the rDsr-bearing bacterial community in intertidal sediments globally, underscoring its significant role in sulfur oxidation in this important marine environment.