Osmoprotective role of dimethylsulfoniopropionate (DMSP) for estuarine bacterioplankton
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AME Aquatic Microbial Ecology Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsSpecials AME 76:133-147 (2015) - DOI: https://doi.org/10.3354/ame01772 Osmoprotective role of dimethylsulfoniopropionate (DMSP) for estuarine bacterioplankton Jessie Motard-Côté1,2,*, Ronald P. Kiene1,2 1Department of Marine Sciences, University of South Alabama, Mobile, Alabama 36688, USA 2Dauphin Island Sea Lab, 101 Bienville Blvd, Dauphin Island, Alabama 36528, USA *Corresponding author: jmotard-cote@disl.org ABSTRACT: Dimethylsulfoniopropionate (DMSP) is synthesized and used by marine phytoplankton as an osmolyte. Previous studies have shown that some of the dissolved DMSP (DMSPd) in seawater is taken up by bacterioplankton and not degraded. We tested the hypothesis that retention of DMSP provides some benefits to marine bacteria. In experiments with coastal seawater filtrates containing mainly bacteria, acute osmotic stresses of +5 and +10 ppt NaCl significantly inhibited bacterial production (BP) over 6 h, while the availability of 20 nM DMSPd relieved most of the BP inhibition. Partial relief of salt-induced inhibition of BP was observed with DMSPd concentrations as low as 2.5 nM, and DMSP was more effective at relieving osmotic stress than other compounds tested. Osmotic stresses resulted in a faster and greater overall uptake of DMSPd and accumulation of untransformed DMSP in bacterial cells (DMSPcell). Retained DMSP reached osmotically-significant intracellular concentrations of 54 mM in salt-stressed bacterial populations. Retention of DMSP was accompanied by a lower production of methanethiol (MeSH), suggesting a down-regulation of the demethylation/demethiolation pathway under osmotic stress. These results show that estuarine bacterioplankton can use DMSP as an osmoprotectant, retaining up to 54% of the available dissolved DMSP untransformed in their cells. This benefit provided by DMSP may help explain why some DMSP is retained in bacteria in the ocean, even under unchanging salinity. This retention slows down the cycling of DMSP, with potential implications for the trophic transfer of DMSP and its contributions to sulfur and carbon fluxes in the ocean. KEY WORDS: Osmolyte · Compatible solute · Salinity stress · Salt inhibition · Osmolarity · Sulfur cycle · DMSP retention · DMSP function Full text in pdf format PreviousNextCite this article as: Motard-Côté J, Kiene RP (2015) Osmoprotective role of dimethylsulfoniopropionate (DMSP) for estuarine bacterioplankton. Aquat Microb Ecol 76:133-147. https://doi.org/10.3354/ame01772 Export citation RSS - Facebook - Tweet - linkedIn Cited by Published in AME Vol. 76, No. 2. Online publication date: October 22, 2015 Print ISSN: 0948-3055; Online ISSN: 1616-1564 Copyright © 2015 Inter-Research.Keywords:
Dimethylsulfoniopropionate
Bacterioplankton
Osmolyte
Osmotic shock
Methanethiol
Dimethylsulfoniopropionate
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Dimethyl sulfide
Deltaproteobacteria
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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.
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Dimethylsulfoniopropionate (DMSP) is abundant in marine environments and an important source of reduced carbon and sulfur for marine bacteria. While both Ruegeria pomeroyi and Ruegeria lacuscaerulensis possessed genes encoding the DMSP demethylation and cleavage pathways, their responses to DMSP differed. A glucose-fed, chemostat culture of R. pomeroyi consumed 99% of the DMSP even when fed a high concentration of 5 mM. At the same time, cultures released 19% and 7.1% of the DMSP as dimethylsulfide (DMS) and methanethiol, respectively. Under the same conditions, R. lacuscaerulensis consumed only 28% of the DMSP and formed one-third of the amount of gases. To examine the pathways of sulfur and methyl C assimilation, glucose-fed chemostats of both species were fed 100 μM mixtures of unlabeled and doubly labeled [dimethyl-13C, 34S]DMSP. Both species derived nearly all of their sulfur from DMSP despite high sulfate availability. In addition, only 33% and 50% of the methionine was biosynthesized from the direct capture of methanethiol in R. pomeroyi and R. lacuscaerulensis, respectively. The remaining methionine was biosynthesized by the random assembly of free sulfide and methyl-tetrahydrofolate derived from DMSP. Thus, although the two species possessed similar genes encoding DMSP metabolism, their growth responses were very different.IMPORTANCE Dimethylsulfoniopropionate (DMSP) is abundant in marine environments and an important source of reduced carbon and sulfur for marine bacteria. DMSP is the precursor for the majority of atmospheric dimethylsulfide (DMS), a climatically active gas that connects the marine and terrestrial sulfur cycles. Although research into the assimilation of DMSP has been conducted for over 20 years, the fate of DMSP in microbial biomass is not well understood. In particular, the biosynthesis of methionine from DMSP has been a focal point, and it has been widely believed that most methionine was synthesized via the direct capture of methanethiol. Using an isotopic labeling strategy, we have demonstrated that the direct capture of methanethiol is not the primary pathway used for methionine biosynthesis in two Ruegeria species, a genus comprised primarily of globally abundant marine bacteria. Furthermore, although the catabolism of DMSP by these species varied greatly, the anabolic pathways were highly conserved.
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Organic sulfur compounds are present in all aquatic systems, but their use as sources of sulfur for bacteria is generally not considered important because of the high sulfate concentrations in natural waters. This study investigated whether dimethylsulfoniopropionate (DMSP), an algal osmolyte that is abundant and rapidly cycled in seawater, is used as a source of sulfur by bacterioplankton. Natural populations of bacterioplankton from subtropical and temperate marine waters rapidly incorporated 15 to 40% of the sulfur from tracer-level additions of [(35)S]DMSP into a macromolecule fraction. Tests with proteinase K and chloramphenicol showed that the sulfur from DMSP was incorporated into proteins, and analysis of protein hydrolysis products by high-pressure liquid chromatography showed that methionine was the major labeled amino acid produced from [(35)S]DMSP. Bacterial strains isolated from coastal seawater and belonging to the alpha-subdivision of the division Proteobacteria incorporated DMSP sulfur into protein only if they were capable of degrading DMSP to methanethiol (MeSH), whereas MeSH was rapidly incorporated into macromolecules by all tested strains and by natural bacterioplankton. These findings indicate that the demethylation/demethiolation pathway of DMSP degradation is important for sulfur assimilation and that MeSH is a key intermediate in the pathway leading to protein sulfur. Incorporation of sulfur from DMSP and MeSH by natural populations was inhibited by nanomolar levels of other reduced sulfur compounds including sulfide, methionine, homocysteine, cysteine, and cystathionine. In addition, propargylglycine and vinylglycine were potent inhibitors of incorporation of sulfur from DMSP and MeSH, suggesting involvement of the enzyme cystathionine gamma-synthetase in sulfur assimilation by natural populations. Experiments with [methyl-(3)H]MeSH and [(35)S]MeSH showed that the entire methiol group of MeSH was efficiently incorporated into methionine, a reaction consistent with activity of cystathionine gamma-synthetase. Field data from the Gulf of Mexico indicated that natural turnover of DMSP supplied a major fraction of the sulfur required for bacterial growth in surface waters. Our study highlights a remarkable adaptation by marine bacteria: they exploit nanomolar levels of reduced sulfur in apparent preference to sulfate, which is present at 10(6)- to 10(7)-fold higher concentrations.
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Theconcentrations ofthevolatile organic sulfur compounds methanethiol, dimethyl disulfide, anddimethyl sulfide (DMS)andtheviable population capable ofDMS utilization inlaminated microbial ecosystems were evaluated. Significant levels ofDMS anddimethyl disulfide (maximum concentrations of220and24nmolcm3 ofsediment-', respectively) couldbedetected onlyatthetop20mm ofthemicrobial mat,whereas methanethiol wasfoundonlyatdepth horizons from20to50mm (maximum concentration of42nmolcm3of sediment- l).DMS concentrations inthesurface layer doubled after coldhydrolysis ofitsprecursor, dimethylsulfoniopropionate. Most-probable-number counts revealed 2.2x 105cells cm3ofsediment-', inthe 0-to5-mm depthhorizon, capable ofgrowthon DMS asthesolesourceofenergy. An obligately chemolithoautotrophic bacillus designated strain T5wasisolated fromthetoplayer ofthemarine sediment. Continuous culture studies inwhichDMS wasthegrowth-limiting substrate revealed amaximumspecific growth rateof0.10h-1andasaturation constant of90,umol liter-' foraerobic growth onthis substrate. Microbial decomposition ofsulfur-containing aminoacids
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Three strains of aerobic bacteria were isolated from water and sediment samples of Mono Lake, a moderately hypersaline (90 ppt), alkaline (pH 9.7) lake in California. The organisms, Gram-negative rods, grew fastest at about pH 9.7 with no growth or much slower growth at pH 7.0. All three isolates grew on glycine betaine (GB) and respirometric experiments indicated that catabolism was by sequential demethylation with dimethyl glycine and sarcosine as intermediates. Two of the isolates also grew on dimethylsulfoniopropionate (DMSP), one with cleavage of the DMSP to yield dimethyl sulfide (DMS) and acrylate, and the other by demethylation with 3-methiolpropionate (MMPA) as an intermediate and the production of methanethiol from MMPA. The methylated osmolytes supported growth at salinities similar to those in Mono Lake, but, at higher salinities, catabolism was suppressed and GB and DMSP functioned as osmolytes. GB and DMSP probably originate from cyanobacteria and/or phytoplankton in Mono Lake and this report is the first indication of both the DMS and demethylation/methanethiol-producing pathways for DMSP degradation in a nonmarine environment.
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