Coordinated regulation of DMSP demethylation and cleavage in abundant marine bacteria

Abstract

Abstract Dimethylsulfoniopropionate (DMSP) catabolism by ubiquitous marine Roseobacters is important in global carbon and sulfur cycling, chemotaxis, and climate-active gas production. Many Roseobacters contain competing DMSP demethylation and cleavage pathways, the latter generating the climate-cooling gas dimethylsulfide (DMS). The mechanism partitioning flux through these pathways, referred to as “the switch”, is unknown. Here, we identify a FadR family transcriptional regulator “DmdR” in Roseobacters that represses transcription of the DMSP demethylation gene dmdA and acuI, central to DMSP cleavage pathways, under low intracellular DMSP levels. Increased DMSP levels induces DMSP cleavage and accumulation of the toxic intermediate and AcuI substrate acryloyl-CoA. DmdR binds acryloyl-CoA as its effector and derepresses dmdA-acuI transcription. Roseobacterial DmdR-dependent regulation, together with transcriptional and kinetic regulation of DMSP cleavage, likely ensures cellular DMSP concentrations that allow its antistress functions and accelerated DMSP demethylation and catabolism of toxic cleavage pathway intermediates at higher DMSP levels. In other abundant marine bacteria that lack dmdA, e.g., Oceanospirillales, DmdR is predicted to still regulate acuI transcription and, thus, acryloyl-CoA catabolism/detoxification. DmdR regulation is widespread in Earth’s oceans and their margins and is an important step in global biogeochemical cycling and climate-active gas production.