The organosulfur compound dimethylsulfoniopropionate (DMSP) is utilized as an osmoprotectant byVibriospecies

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.

Function and wide distribution of DMSOP cleaving enzymes in marine organisms

“…Given the abundance of DMSOP in the salt marsh sediments, above, and that Thume et al demonstrated that diverse bacteria import DMSOP 1 , we proposed that diverse microorganisms could utilise it as an osmoprotectant, as was known to be the case for its precursor molecule DMSP 17,18 . To test this hypothesis, the osmosensitive E. coli strain, FF4169, deficient in trehalose production 19 , was grown under saline conditions in the presence and absence of DMSOP, DMSP and the nitrogenous osmoprotectant glycine betaine (GB).…”

Recent insights into oceanic dimethylsulfoniopropionate biosynthesis and catabolism

“…The marine halophile Vibrio parahaemolyticus contains four BCCT carriers (BccT1 to BccT4). It is indicated that BccT1 and BccT2 are carriers of DMSP in V. parahaemolyticus , whereas BccT3 and BccT4 do not play a significant role in DMSP transport in V. parahaemolyticus (Gregory et al ., 2020). Of the four additional Vibrio species that used DMSP as an osmolyte, V. harveyi and V. fluvialis contain homologues of BccT1 and BccT2 while V. vulnificus and V. cholerae can utilize DMSP as an osmolyte and contained only a BccT3 homologue.…”

“…Of the four additional Vibrio species that used DMSP as an osmolyte, V. harveyi and V. fluvialis contain homologues of BccT1 and BccT2 while V. vulnificus and V. cholerae can utilize DMSP as an osmolyte and contained only a BccT3 homologue. In V. vulnificus strains, an additional BCCT family transporter, named BccT5, was also a carrier for DMSP (Gregory et al ., 2020). The second transporter family found to carry DMSP across the membrane is the ATP binding cassette (ABC) transporter, a commonly used primary transporter that can be found in all three domains of life (Eitinger et al ., 2011).…”