AbstractMicrobial lysis of dimethylsulfoniopropionate (DMSP) is a key step in marine organic sulfur cycling and has been recently demonstrated to play an important role in mediating interactions between bacteria, algae, and zooplankton. To date, microbes that have been found to lyse DMSP are largely confined to free‐living and surface‐attached bacteria. In this study, we report for the first time that a symbiont (termed “Rhodobiaceae bacterium HWgs001”) in the gill of the marine scallop Argopecten irradians irradians can lyse and metabolize DMSP. Analysis of 16S rRNA gene sequences suggested that HWgs001 accounted for up to 93% of the gill microbiota. Microscopic observations suggested that HWgs001 lived within the gill tissue. Unlike symbionts of other bivalves, HWgs001 belongs to Alphaproteobacteria rather than Gammaproteobacteria, and no genes for carbon fixation were identified in its small genome. Moreover, HWgs001 was found to possess a dddP gene, responsible for the lysis of DMSP to acrylate. The enzymatic activity of dddP was confirmed using the heterologous expression, and in situ transcription of the gene in scallop gill tissues was demonstrated using reverse‐transcription PCR. Together, these results revealed a taxonomically and functionally unique symbiont, which represents the first‐documented DMSP‐metabolizing symbiont likely to play significant roles in coastal marine ecosystems.