The Organosulfur Compound Dimethylsulfoniopropionate (DMSP) Is Utilized as an Osmoprotectant by Vibrio Species

Dimethylsulfoniopropionate (DMSP), a key component of the global geochemical sulfur cycle, is a secondary metabolite produced in large quantities by marine phytoplankton and utilized as an osmoprotectant, thermoprotectant, and antioxidant. Marine bacteria can use two pathways to degrade and catabolize DMSP, a demethylation pathway and a cleavage pathway that produces 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 has received little attention. The marine halophile Vibrio parahaemolyticus contains at least six osmolyte transporters, namely four betaine carnitine choline transport (BCCT) carriers (BccT1 to BccT4) and two ATP-binding cassette (ABC) family ProU transporters. In this study, we showed that DMSP is used as an osmoprotectant by V. parahaemolyticus and by several other Vibrio species, including Vibrio cholerae and Vibrio 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 the wild type (WT) in high-salinity medium supplemented with DMSP. Using mutants possessing only one functional BCCT in growth pattern assays, we identified two BCCT family transporters, BccT1 and BccT2, that are carriers of DMSP. The only V. parahaemolyticus BccT homolog that V. cholerae and V. vulnificus possess is BccT3, and functional complementation in Escherichia coli MKH13 showed that V. cholerae VcBccT3 could transport DMSP. In V. vulnificus strains, we identified and characterized an additional BCCT family transporter, which we named BccT5, that was also a carrier for DMSP. IMPORTANCE DMSP is present in the marine environment, produced in large quantities by marine phytoplankton as an osmoprotectant, and is an important component of the global geochemical sulfur cycle. This algal osmolyte has not been previously investigated for its role in marine heterotrophic bacterial osmotic stress response. Vibrionaceae species are marine species, many of which are halophiles exemplified by V. parahaemolyticus, a species that possesses at least six transporters for the uptake of osmolytes. Here, we demonstrated that V. parahaemolyticus and other Vibrio species can accumulate DMSP as an osmoprotectant and show that several BCCT family transporters uptake DMSP. These studies suggest that DMSP is a significant bacterial osmoprotectant that may be important for understanding the fate of DMSP in the environment. DMSP is produced and present in coral mucus, and Vibrio species form part of the microbial communities associated with corals. The function of DMSP in these interactions is unclear, but it could be an important driver for these associations, allowing Vibrio proliferation. This work suggests that DMSP likely has a more important role in heterotrophic bacteria ecology than previously appreciated.

Automated summary

DMSP is a key component of the global geochemical sulfur cycle, produced in large quantities by marine phytoplankton and utilized by marine bacteria as an osmoprotectant. Vibrio species, including V. parahaemolyticus, can accumulate DMSP as an osmoprotectant using specific BCCT family transporters, suggesting a potentially important role of DMSP in marine bacterial ecology.