# Regulation of DMSP organosulfur cycling in ubiquitous Roseobacter marine bacteria

## TL;DR

This paper identifies a key regulator, DmdR, in marine bacteria that controls how DMSP is processed, affecting climate-cooling gas production and cellular stress.

## Contribution

The discovery of DmdR as a regulatory switch for DMSP metabolism and its role in oxidative stress protection in Roseobacter bacteria.

## Key findings

- DmdR represses DMSP demethylation and cleavage pathways when DMSP is scarce.
- At higher DMSP levels, DmdR derepresses genes to detoxify acryloyl-CoA and demethylate DMSP.
- DmdR-regulated genes dmdE and dmdF are essential for DMSP demethylation and stress protection.

## Abstract

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.

Ubiquitous marine roseobacters utilize competing dimethylsulfoniopropionate (DMSP) cleavage and demethylation pathways, but only cleavage yields the climate-cooling gas dimethyl sulfide (DMS). This work identifies the DmdR “switch regulator” that controls Roseobacter DMSP catabolism and oxidative stress protection.

The Roseobacter “switch” regulator DmdR represses both DMSP demethylation and cleavage pathways when DMSP is scarce.At higher DMSP levels, binding of the cytotoxic DMSP cleavage catabolite acryloyl-CoA to DmdR causes derepression of enzymes which detoxify and assimilate acryloyl-CoA, demethylate DMSP, and protect against oxidative stress.Novel DmdR-regulated genes, dmdE and dmdF, are essential for DMSP demethylation; with DmdF being a peroxidase that ameliorates oxidative stress linked to this pathway.The DmdR mechanism is widespread in marine bacterioplankton, coordinating DMSP catabolism and influencing global sulfur and climate-active gas cycling.

The Roseobacter “switch” regulator DmdR represses both DMSP demethylation and cleavage pathways when DMSP is scarce.

At higher DMSP levels, binding of the cytotoxic DMSP cleavage catabolite acryloyl-CoA to DmdR causes derepression of enzymes which detoxify and assimilate acryloyl-CoA, demethylate DMSP, and protect against oxidative stress.

Novel DmdR-regulated genes, dmdE and dmdF, are essential for DMSP demethylation; with DmdF being a peroxidase that ameliorates oxidative stress linked to this pathway.

The DmdR mechanism is widespread in marine bacterioplankton, coordinating DMSP catabolism and influencing global sulfur and climate-active gas cycling.

This research identifies novel Roseobacter genes playing key roles in dimethylsulfoniopropionate catabolism in the marine environment.