The organosulfur compound dimethylsulfoniopropionate (DMSP) is utilized as an osmoprotectant by Vibrio species

Abstract

Dimethylsulfoniopropionate (DMSP) is a key component of the global geochemical sulfur cycle that is a secondary metabolite produced in large quantities by marine phytoplankton and utilized as an osmoprotectant. Bacterial DMSP lyases convert DMSP to the climate active gas dimethylsulfide (DMS). Whether marine bacteria can also accumulate DMSP as an osmoprotectant to maintain the turgor pressure of the cell in response to changes in external osmolarity remains unknown. The marine halophile Vibrio parahaemolyticus, contains at least six osmolyte transporters, four betaine carnitine choline transport (BCCT) carriers BccT1-BccT4 and two ABC-family ProU transporters. In this study, we showed that DMSP is used as an osmoprotectant by V. parahaemolyticus and several other Vibrio species including V. cholerae and V. vulnificus. Using a V. parahaemolyticus proU double mutant, we demonstrated that these ABC transporters are not required for DMSP uptake. However, a bccT null mutant lacking all four BCCTs had a growth defect compared to wild type in high salt media supplemented with DMSP. Using bccT triple mutants, possessing only one functional BCCT, in growth pattern assays, we identified two BCCT-family transporters, BccT1 and BccT2 are carriers of DMSP. Vibrio cholerae and V. vulnificus, only contain a homolog of BccT3 and functional complementation in Escherichia coli MKH13 showed only V. cholerae BccT3 could transport DMSP. In V. vulnificus strains, we identified and characterized an additional BCCT transporter that was also a carrier for DMSP. Phylogenetic analysis uncovered at least 11 distinct BCCT transporters among members of the Harveyi clade, with some species having up to 9 BCCTs as exemplified by V. jasicida. ImportanceDMSP is present in the marine environment, produced in large quantities by marine phytoplankton as an osmoprotectant, and is an important component of the global geosulfur cycle. The bacterial family Vibrionaceae is comprised of marine species, many of which are halophiles such as V. parahaemolyticus, which can utilize a wide range of osmolytes and possesses at least six transporters for the uptake of these compounds. Here, we demonstrated that V. parahaemolyticus and other Vibrio species can accumulate DMSP as an osmoprotectant and show that the BCCT family transporters were required. DMSP was transported by four different BCCT transporters; BccT1, BccT2, BccT3 and BccT5 depending on the species. Bioinformatics and phylogenetics demonstrated that Vibrio species contain a large number of BCCTs and that many of these are associated with different metabolic pathways.