Dimethylsulfoniopropionate Uptake Research Articles

Ubiquitous occurrence of a dimethylsulfoniopropionate ABC transporter in abundant marine bacteria

Dimethylsulfoniopropionate (DMSP) is a ubiquitous organosulfur compound in marine environments with important functions in both microorganisms and global biogeochemical carbon and sulfur cycling. The SAR11 clade and marine Roseobacter group (MRG) represent two major groups of heterotrophic bacteria in Earth’s surface oceans, which can accumulate DMSP to high millimolar intracellular concentrations. However, few studies have investigated how SAR11 and MRG bacteria import DMSP. Here, through comparative genomics analyses, genetic manipulations, and biochemical analyses, we identified an ABC (ATP-binding cassette)-type DMSP-specific transporter, DmpXWV, in Ruegeria pomeroyi DSS-3, a model strain of the MRG. Mutagenesis suggested that DmpXWV is a key transporter responsible for DMSP uptake in strain DSS-3. DmpX, the substrate binding protein of DmpXWV, had high specificity and binding affinity towards DMSP. Furthermore, the DmpX DMSP-binding mechanism was elucidated from structural analysis. DmpX proteins are prevalent in the numerous cosmopolitan marine bacteria outside the SAR11 clade and the MRG, and dmpX transcription was consistently high across Earth’s entire global ocean. Therefore, DmpXWV likely enables pelagic marine bacteria to efficiently import DMSP from seawater. This study offers a new understanding of DMSP transport into marine bacteria and provides novel insights into the environmental adaption of marine bacteria.

Uptake of Dimethylsulfoniopropionate (DMSP) by Natural Microbial Communities of the Great Barrier Reef (GBR), Australia.

Dimethylsulfoniopropionate (DMSP) is a key organic sulfur compound that is produced by many phytoplankton and macrophytes and is ubiquitous in marine environments. Following its release into the water column, DMSP is primarily metabolised by heterotrophic bacterioplankton, but recent evidence indicates that non-DMSP producing phytoplankton can also assimilate DMSP from the surrounding environment. In this study, we examined the uptake of DMSP by communities of bacteria and phytoplankton within the waters of the Great Barrier Reef (GBR), Australia. We incubated natural GBR seawater with DMSP and quantified the uptake of DMSP by different fractions of the microbial community (>8 µm, 3–8 µm, <3 µm). We also evaluated how microbial community composition and the abundances of DMSP degrading genes are influenced by elevated dissolved DMSP levels. Our results showed uptake and accumulation of DMSP in all size fractions of the microbial community, with the largest fraction (>8 µm) forming the dominant sink, increasing in particulate DMSP by 44–115% upon DMSP enrichment. Longer-term incubations showed however, that DMSP retention was short lived (<24 h) and microbial responses to DMSP enrichment differed depending on the community carbon and sulfur demand. The response of the microbial communities from inside the reef indicated a preference towards cleaving DMSP into the climatically active aerosol dimethyl sulfide (DMS), whereas communities from the outer reef were sulfur and carbon limited, resulting in more DMSP being utilised by the cells. Our results show that DMSP uptake is shared across members of the microbial community, highlighting larger phytoplankton taxa as potentially relevant DMSP reservoirs and provide new information on sulfur cycling as a function of community metabolism in deeper, oligotrophic GBR waters.

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, 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.

The abundant marine bacterium Pelagibacter simultaneously catabolizes dimethylsulfoniopropionate to the gases dimethyl sulfide and methanethiol.

Marine phytoplankton produce ∼10(9) tonnes of dimethylsulfoniopropionate (DMSP) per year(1,2), an estimated 10% of which is catabolized by bacteria through the DMSP cleavage pathway to the climatically active gas dimethyl sulfide(3,4). SAR11 Alphaproteobacteria (order Pelagibacterales), the most abundant chemo-organotrophic bacteria in the oceans, have been shown to assimilate DMSP into biomass, thereby supplying this cell's unusual requirement for reduced sulfur(5,6). Here, we report that Pelagibacter HTCC1062 produces the gas methanethiol, and that a second DMSP catabolic pathway, mediated by a cupin-like DMSP lyase, DddK, simultaneously shunts as much as 59% of DMSP uptake to dimethyl sulfide production. We propose a model in which the allocation of DMSP between these pathways is kinetically controlled to release increasing amounts of dimethyl sulfide as the supply of DMSP exceeds cellular sulfur demands for biosynthesis.

Bacterial DMSP metabolism during the senescence of the spring diatom bloom in the Northwest Atlantic

MEPS Marine Ecology Progress Series Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections MEPS 369:1-11 (2008) - DOI: https://doi.org/10.3354/meps07664 FEATURE ARTICLE Bacterial DMSP metabolism during the senescence of the spring diatom bloom in the Northwest Atlantic Anissa Merzouk1,*, Maurice Levasseur2, Michael Scarratt3, Sonia Michaud3, Martine Lizotte2, Richard B. Rivkin4, Ronald P. Kiene5 1University of British Columbia, Earth and Ocean Sciences/Oceanography, 1461-6270 University Boulevard, Vancouver, British Columbia V6T 1Z4, Canada 2Université Laval, Département de biologie (Québec-Océan), Pavillon Alexandre-Vachon, Quebec, Quebec G1K 7P4, Canada 3Fisheries and Oceans Canada, Maurice Lamontagne Institute, 850 Route de la mer, Mont-Joli, Quebec G5H 3Z4, Canada 4Ocean Sciences Centre, Memorial University of Newfoundland, St. John’s, Newfoundland A1C 5S7, Canada 5University of South Alabama, Department of Marine Sciences, Mobile, Alabama 36688, USA *Email: amerzouk@eos.ubc.ca ABSTRACT: The impact of the decline of the vernal bloom on the bacterial metabolism of dimethylsulfoniopropionate (DMSP), the precursor of dimethylsulfide (DMS), was investigated during a 7 d Lagrangian study conducted in the Northwest Atlantic in spring 2003. Daily variations in bacterial leucine incorporation, dissolved DMSP (DMSPd) uptake and DMS production rates were measured in the surface mixed layer (SML) and in the deep chlorophyll a maximum (DCM) that formed as the bloom collapsed. Seawater samples were amended with 35S-DMSPd, and the products of bacterial DMSPd degradation were measured during 3 h on-board incubations. The gradual decrease in phytoplankton biomass and diatom abundance measured in the SML was accompanied by a sharp doubling of the bacterial abundance and a peak in leucine incorporation rate on Day 2, suggesting that bacteria responded to a transient pulse in dissolved organic matter. Bacterial DMSPd uptake and DMS production were highest on Days 1 and 2 (1.2 and 0.10 nmol l-1 h-1, respectively), but rapidly decreased by Day 3, suggesting that DMSPd was becoming a less important substrate for the growing bacterial assemblage as other substrates became available. Bacterial DMSPd uptake and DMS production rates were also low in the DCM despite very high DMS yields (40 to 50%), showing that neither the decline of the diatom spring bloom in the SML nor the accumulation of cells in the DCM resulted in a stimulation of bacterial DMSP metabolism or accumulation of DMS. The present study provides new field evidence for the potential uncoupling between bacterial production and DMS dynamics likely due to variations in the availability of other S-containing organic compounds released during the decay of phytoplankton blooms. KEY WORDS: DMSP cycling · Bacterial metabolism · Bloom senescence · Northwest Atlantic Ocean Full text in pdf format Information about this Feature Article NextCite this article as: Merzouk A, Levasseur M, Scarratt M, Michaud S, Lizotte M, Rivkin RB, Kiene RP (2008) Bacterial DMSP metabolism during the senescence of the spring diatom bloom in the Northwest Atlantic. Mar Ecol Prog Ser 369:1-11. https://doi.org/10.3354/meps07664Export citation RSS - Facebook - Tweet - linkedIn Cited by Published in MEPS Vol. 369. Online publication date: October 13, 2008 Print ISSN: 0171-8630; Online ISSN: 1616-1599 Copyright © 2008 Inter-Research.

Dimethylsulfoniopropionate Uptake by Marine Phytoplankton

Dimethylsulfoniopropionate (DMSP) accounts for most of the organic sulfur fluxes from primary to secondary producers in marine microbial food webs. Incubations of natural communities and axenic cultures with radio-labeled DMSP showed that dominant phytoplankton groups of the ocean, the unicellular cyanobacteria Prochlorococcus and Synechococcus and diatoms, as well as heterotrophic bacteria take up and assimilate DMSP sulfur, thus diverting a proportion of plankton-produced organic sulfur from emission into the atmosphere.

In Vivo Characterization of Dimethylsulfoniopropionate Lyase in the Fungus Fusarium lateritium

A fungus, Fusarium lateritium, with dimethylsulfoniopropionate (DMSP) lyase activity was isolated from both seawater and a salt marsh due to its ability to grow on DMSP (with the evolution of dimethyl sulfide) as the sole source of carbon. This is the first reported case of DMSP lyase activity in a fungus. Several other common fungal genera tested did not have DMSP lyase activity. DMSP was taken up more rapidly by F. lateritium than it was utilized, leading to its intracellular accumulation. Inhibitor studies with nystatin and cyanide indicated that DMSP uptake was an energy-dependent process. The lyase was inducible by its substrate, DMSP (K(m), 1.2 mM), and by the substrate analogs choline and glycine betaine. During induction, DMSP lyase activity increased with time and then dropped rapidly. This loss of activity could be prevented by spiking the culture with fresh DMSP or choline. The V(max) for DMSP lyase was 34.7 mU . mg of protein. The inhibitory effects of nystatin, and p-chloromercuriphenylsulfonate on DMSP lyase activity suggested that the enzyme is cytosolic. Because plants like Spartina (a marsh grass) and marine algae contain high concentrations of DMSP, we speculate that DMSP-utilizing fungi may be involved in their decay.

Evidence for Intracellular and Extracellular Dimethylsulfoniopropionate (DMSP) Lyases and DMSP Uptake Sites in Two Species of Marine Bacteria

Volume 63, no. 4, p. 1600: The caption to Table 2 should read as follows: "Inactivation of Clostridium perfringens spores by 5-mg/liter doses of mixed oxidants or free chlorine in buffer at pH 7 at 25(deg)C." [This corrects the article on p. 1598 in vol. 63.].

Evidence for Intracellular and Extracellular Dimethylsulfoniopropionate (DMSP) Lyases and DMSP Uptake Sites in Two Species of Marine Bacteria

The kinetics of dimethylsulfoniopropionate (DMSP) uptake and dimethylsulfide (DMS) production from DMSP in two bacterial species, Alcaligenes sp. strain M3A, an isolate from estuarine surface sediments, and Pseudomonas doudoroffii, from seawater, were investigated. In Alcaligenes cells induced for DMSP lyase (DL) activity, DMS production occurred without DMSP uptake. In DL-induced suspensions of P. doudoroffii, uptake of DMSP preceded the production of DMS, indicating an intracellular location of DL; intracellular DMSP levels reached ca. 7 mM. DMSP uptake rates in noninduced cells showed saturation at three concentrations (K(inft) [transport] values, 3.4, 127, and 500 (mu)M). In DL-induced cells of P. doudoroffii, DMSP uptake rates increased ca. threefold (V(infmax), 0.022 versus 0.065 (mu)mol of DMSP taken up min(sup-1) mg of cell protein(sup-1)), suggesting that the uptake binding proteins were inducible. DMSP uptake and DL activity in P. doudoroffii were both inhibited by CN(sup-), 2,4-dinitrophenol, and membrane-impermeable thiol-binding reagents, further indicating active uptake of DMSP by cell surface components. The respiratory inhibitors had limited or no effect on DL activity by the Alcaligenes sp. Of the structural analogs of DMSP tested for their effect on DMSP metabolism, glycine betaine (GBT), but not methyl-3-mercaptopropionic acid (MMPA), inhibited DMSP uptake by P. doudoroffii, suggesting that GBT shares a binding protein with DMSP and that MMPA is taken up at a separate site. Two models of DMSP uptake, induction, and DL location found in marine bacteria are presented.

Microbial cycling of DMSP and DMS in coastalandoligotrophicseawater

The rates and concentration dependence of microbial dimethylsulfide (DMS) and dimethylsulfoniopropionate (DMSP) cycling were assessed in Vineyard Sound, Massachusetts, and the Sargasso Sea. Net rates of dissolved DMSP loss, DMS production from DMSP, and DMS consumption were measured at ambient and near‐ambient substrate levels. Turnover times of dissolved DMSP, based on loss rates, were short, usually ranging from 1.5 d to several hours. However, the specific process of DMSP cleavage to form DMS accounted for only a portion of total DMSP turnover. Short‐term variability obscured possible regional or seasonal trends in these data. Dissolved DMSP removal and cleavage exhibited saturable kinetics in spring in Vineyard Sound and in winter in the Sargasso Sea. In fall and spring in the Sargasso Sea, where dissolved DMSP levels ranged from 2 to 9 nM, DMSP cleavage did not saturate at DMSP levels as high as 1 µM. Kinetic parameters of DMSP uptake appeared to increase with proximity to summer, as did the proportion of DMSP uptake resulting in DMS production.