Fungi are overlooked dimethylsulfoniopropionate degraders in marine environments

Abstract

Abstract Dimethylsulfoniopropionate (DMSP) is a key marine organosulfur compound, whose microbial catabolism is critical to global sulfur cycling and is the major source of the climate-active gas dimethyl sulfide (DMS). Research has focused on bacterial and algal DMSP catabolism, potentially overlooking the importance of fungi. Here, we vastly extend the known diversity of fungi that cleave DMSP to DMS, showing that many lacked known DMSP lyases, and Pezizomycotina members were most active. The marine-derived yeast-like fungus Aureobasidium melanogenum imported DMSP for osmoprotection, and assimilated it via a previously unreported and efficient cupin-family cytoplasmic DMSP lyase, termed DddF. The DddF co-product, acrylate, was catabolized to acryloyl-CoA in the cytoplasm, with subsequent metabolism occurring in mitochondria. Functional dddF genes are widely found across major fungal classes (e.g., Dothideomycetes, Sordariomycetes) common throughout marine ecosystems. Thus, the fungal capacity to catabolize DMSP is far more prevalent than previously believed, highlighting their potential importance in marine sulfur cycling and DMS production.