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

Abstract

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, 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 salinity media supplemented with DMSP. Using mutants possessing only one functional BCCT in growth pattern assays, we identified two BCCT-family transporters, BccT1 and BccT2, which 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 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 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, which 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 them. The function of DMSP in these interactions is unclear, but could be an important driver for these associations allowing Vibrio proliferation. This work suggests that DMSP likely has an important role in heterotrophic bacteria ecology than previously appreciated.

Marine natural products

“…dynemicin A) that has delivered insights into the biosynthetic enzymes and pathways associated with this rare chemotype, 100 and identification of a C -glycosyltransferase involved in the biosynthesis of the pyranonaphthoquinone medermycin. 101 Dimethylsulfoniopropionate, an organosulfur metabolite produced in large quantities by phytoplankton and a key component of the global geochemical sulfur cycle, was shown to be utilised as an osmoprotectant by various Vibrio species, 102 mathermycin's cytotoxic MOA involves the targeting of cell surface phospholipids with a specificity towards phosphatidylethanolamine, 103 while the discovery of an unusual type II PKS system, which consists of three phylogenetically different ketosynthase/chain length factor complexes, has been linked to the generation of cinnamoyl containing lipids belonging to the youssoufene structure class. 104…”

Climate Change Impacts on the Marine Cycling of Biogenic Sulfur: A Review

“…The annual global production of DMSP by deep ocean phytoplankton (excluding coastal) is conservatively estimated as 3.8 Pg C year −1 [62]-this is a substantial amount for a single compound, equal to approximately 10% of the total carbon fixed annually by marine phytoplankton [63]. DMSP is also critical to the structure of the marine food web as it provides a substantial source of reduced carbon and sulfur for heterotrophic bacteria [49,64] and can also be concentrated internally to serve as an osmolyte, reaching concentrations of 70 mM in some marine bacteria [21,65]. Field studies indicate that particulate DMSP concentration can span a very large range depending on the phytoplankton speciation and bloom dynamics, from 5 to >4000 nM [66,67], whereas dissolved DMSP is often present in lower concentrations (1-25 nM) and has a turnover rate of 1-129 nM d −1 [49].…”

“…It has been long recognized that different phytoplankton genera synthesize DMSP to varying degrees [17], with coccolithophorids and small flagellates having higher intracellular concentrations of DMSP, which was originally thought to act as an osmolyte in the algal cell. Further research has identified several other roles for DMSP, such as a response to oxidative stress in algae and corals [18], and giant clams [19], and as an osmoregulant and reduced carbon/sulfur source in marine heterotrophic bacteria [20][21][22]. In addition, DMS can act as a scavenger of reactive oxygen species (ROS) via conversion to dimethylsulfoxide (DMSO) [18,23].…”

A Density Functional Theory Investigation of Cleavage Mechanism of Dimethylsulphoniopropionate by Lyase DddQ

“…DMSP in the ocean undergoes two primary metabolic pathways. The first metabolic pathway involves demethylation reactions, while the second pathway is catalyzed by lyases present in algae and various marine bacteria, resulting in the cleavage of DMSP and the production of dimethylsulfide (DMS) and acrylate (Figure 1) [2] . DddQ, one of the DMSP lyases, has a more widespread distribution in the ocean.…”