Dimethylsulfoniopropionate assimilation by marine bacteria

Abstract

Dimethylsulfoniopropionate (DMSP) is ubiquitous in marine surface waters where it is produced by marine phytoplankton for use as an osmolyte amongst other functions. Some marine bacteria, including the model organism Ruegeria pomeroyi DSS-3, maintain two competing pathways for the degradation of DMSP. Only recently have the genes and biochemical pathways that degrade DMSP been investigated and identified. The DMSP-dependent demethylase, designated DmdA, was the first enzyme identified to directly catalyze a reaction involving DMSP. Upon purification and characterization of the enzyme it was confirmed that methylmercaptopropionate (MMPA) and 5-methyl-tetrahydrofolate were the reaction products. Interestingly, the enzyme possessed a low affinity for DMSP and the host bacterium was shown to accumulate DMSP to high intracellular concentrations, promoting maximal enzyme activity. The complete biochemical pathway for the catabolism of methylmercaptopropionate (MMPA), the product of DMSP demethylation, was also elucidated. This pathway was composed of four enzymes, three of which catalyzed novel reactions that had never been previously observed. The genes that encoded for these novel enzymes were identified by purification from crude cell extracts. Phylogenetic analysis showed that these genes were remarkably widespread in bacteria from marine and non-marine origin. Lastly, the biochemical pathway for assimilation of acrylate, the three carbon intermediate of the DMSP cleavage reaction, was also elucidated. This pathway was also composed of several CoA-mediated reactions that led to the production of propionyl-CoA. Two of the three novel enzymes that composed this pathway were identified. A 13C tracer was used to investigate the assimilation of DMSP carbon and support the physiological significance of the proposed pathways for MMPA and acrylate assimilation. This work has tremendously advanced the understanding of microbial DMSP metabolism on both the molecular and biochemical levels.