Regulation of DMSP organosulfur cycling in ubiquitous Roseobacter 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. Here, we identify the "switch" regulator in Roseobacters, DmdR, which transcriptionally represses demethylation (dmdA, encoding DMSP demethylase), cleavage (acuI, encoding acryloyl-CoA reductase) and oxidative stress protection (dmdEF, dinB) genes under low intracellular DMSP levels. Increased DMSP levels lead to DMSP cleavage and accumulation of cytotoxic cleavage product acryloyl-CoA. Acryloyl-CoA binding to DmdR derepresses dmdA-acuI transcription to stimulate acryloyl-CoA catabolism and DMSP demethylation. Upregulation of the newly identified peroxidase DmdF, and possibly also of DmdE and DinB, counteracts oxidative stress associated with DMSP demethylation. Thus, DmdR, along with DmdR-independent regulators of DMSP cleavage, likely maintains cellular DMSP levels to allow its antistress functions, but accelerates demethylation and catabolism of toxic intermediates at higher DMSP levels. Of note, DmdR appears to control acryloyl-CoA catabolism/detoxification even in abundant marine bacteria lacking dmdA, suggesting additional mechanisms. DmdR and DmdEF are widespread in Earth's oceans and important for biogeochemical cycling and climate-active gas production.