Elucidation of a key mechanism regulating organosulfur cycling in ubiquitous marine bacteria

Dimethylsulfoniopropionate (DMSP) catabolism by marine Roseobacters is important for global biogeochemical cycling and the climate. Many Roseobacters contain competing DMSP demethylation and cleavage pathways, but only cleavage produces the climate-cooling gas dimethylsulfide. We identify the “switch” regulator in Roseobacters, DmdR, that represses the transcription of DMSP demethylation (dmdA, encoding DMSP demethylase), cleavage (acuI, encoding acryloyl-CoA reductase) and often novel oxidative stress protection (dmdEF, dinB) genes under low intracellular DMSP levels. Increased DMSP levels induce DMSP cleavage and accumulation of cytotoxic acryloyl-CoA. DmdR binds acryloyl-CoA as its effector and derepresses dmdA-acuI transcription to stimulate acryloyl-CoA catabolism and DMSP demethylation. Co-upregulation of the novel peroxidase DmdF and likely DmdE and DinB counteract oxidative stress associated with DMSP demethylation. Thus, DmdR, with DmdR-independent regulation of DMSP cleavage, likely balances cellular DMSP levels to allow its antistress functions, but accelerated demethylation and catabolism of toxic intermediates at higher DMSP levels. In abundant marine bacteria lacking dmdA, DmdR still likely controls acryloyl-CoA catabolism/detoxification. DmdR and DmdEF are widespread in Earth’s oceans and important in biogeochemical cycling and climate-active gas production.