The organosulfur compound dimethylsulfoniopropionate (DMSP) is a valuable commodity for both the phytoplankton that produce it and the marine bacteria that degrade it. While phytoplankton use DMSP primarily as an osmolyte, for marine bacteria DMSP is also a source of reduced carbon and sulfur. The enzymes involved in the pathways for bacterial DMSP metabolism, the cleavage and demethylation pathways, were identified in the roseobacter Ruegeria pomeroyi DSS-3. These advances have allowed for in-depth studies of the pathways enzymes, their regulation, and diversity. Characterization of the DmdB methylmercaptopropionate (MMPA)-CoA ligase isozymes, RPO_DmdB1 and RPO_DmdB2, from R. pomeroyi revealed these enzymes have activity with a range of substrates but have adapted specific regulatory features for catalyzing reactions with the demethylation pathway intermediate MMPA. The DmdB isozymes were differentially regulated with RPO_DmdB1 being stimulated by increasing ADP levels while RPO_DmdB2 responded to increasing MMPA. DmdB may also be regulated by acetylation. RPO_DmdB2 showed reduced activity when acetylated with a protein N-acetyltransferase. Multiple deacetylases from R. pomeroyi could reverse the acetylation. The methylthioacryloyl (MTA)-CoA hydratase DmdD catalyzes the final reaction of the demethylation pathway, but is not widely distributed phylogenetically. An alternative enzyme, AcuH, was identified in R. pomeroyi and Ruegeria lacuscaerulensis. AcuH was present in diverse microorganisms and exhibited activity towards MTA-CoA and the cleavage pathway intermediate acryloyl-CoA. The regulation of the demethylation and cleavage pathways is still under investigation. While ADP influenced the activity of both DmdB and AcuH, the availability of free tetrahydrofolate (THF) and turnover of methyl-THF may also play a regulatory role. The first step of the demethylation pathway utilizes THF and produces methyl-THF. When THF availability was limited, dimethyl sulfide (DMS) production increased indicating elevated use of the cleavage pathway. Additionally, the specific activities of enzymes required for the turnover of methyl-THF were two-fold higher in cell extracts grown on DMSP compared with acetate. Based on the current evidence, the DMSP degradation enzymes have likely been recruited from preexisting metabolic pathways. While DmdB and AcuH clearly function in DMSP metabolism, they have broader substrate specificities allowing them to carrying out a range of reactions for other pathways.