Metabolic Regulation of Dimethylsulfoniopropionate Cleavage and Dimethyl Sulfide Production in Halomonas sp. D47.

Dimethylsulfoniopropionate (DMSP) is a globally significant marine organosulfur compound with diverse ecological roles, including environmental stress protection, chemotaxis, and nutrient cycling. Its microbial catabolism is crucial for the marine sulfur cycle, generating dimethyl sulfide (DMS), a volatile gas that influences global sulfur fluxes, cloud formation, and climate regulation. Despite its importance, the metabolic regulatory mechanisms governing bacterial DMSP cleavage and DMS production remain unclear. Here, using the model DMSP-catabolizing bacterium Halomonas sp. D47, a complex regulatory mechanism involving two transcriptional regulators, AcuR and AcuZ, was elucidated through integrated genetic and biochemical analyses, in which they coordinate the orderly progression of DMSP catabolism. These regulators sense external signals from DMSP and its metabolites, fine-tuning gene expression to balance metabolism and detoxification, thereby maintaining cellular integrity. Bioinformatics analyses suggest that this regulatory scheme is conserved among certain efficient DMSP-metabolizing bacteria. Our findings provide key insights into the regulation of DMSP catabolism and highlight a potentially bacterial strategy for balancing metabolic demands with cellular homeostasis.