Active microorganisms and potential metabolic pathways mediating anaerobic degradation of DMSP in anoxic saltmarsh sediment

Dimethylsulfoniopropionate (DMSP) is a globally abundant organosulfur compound produced by marine organisms, where it plays key physiological roles in stress protection and serves as a major source of carbon, sulfur, and energy for microbial communities. Importantly, DMSP degradation contributes to the formation of the climate-active gas dimethyl sulfide (DMS), which can drive the production of potent greenhouse gases, methane and carbon dioxide, in anoxic environments. While aerobic DMSP degradation is well studied, its fate under anoxic conditions remains poorly understood, and the microbial populations and metabolic pathways underlying these biotransformations are virtually unknown. Here, we present the first detailed investigation of microbial DMSP cycling in anoxic saltmarsh sediments. Our sediment samples had high in situ DMSP concentrations (up to 7.7 μmol/g) and the conversion efficiencies of DMSP to DMS under anoxic conditions (~68%) were comparable to those in oxic environments. Furthermore, using ¹³C-labelled DMSP in stable isotope probing (SIP) experiments, combined with 16S rRNA gene sequencing and metagenomics, we identified Amphritea (Oceanospirillales) as a key active DMSP degrader, likely operating via the dddD-encoded lysis pathway. Additional taxa, including Geopsychrobacter, were implicated as potential secondary consumers, while Arcobacteraceae may contribute to sulfur cycling rather than direct DMSP catabolism. This study uncovers a previously overlooked route for DMSP transformation via anaerobic metabolism, expands the known metabolic roles of saltmarsh microorganisms and highlights the potential for DMSP to drive climate-active gas production in anoxic coastal ecosystems.