Literature DB >> 33355097

The organosulfur compound dimethylsulfoniopropionate (DMSP) is utilized as an osmoprotectant by Vibrio species.

Gwendolyn J Gregory1, Katherine E Boas1, E Fidelma Boyd2.   

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.
Copyright © 2020 American Society for Microbiology.

Entities:  

Year:  2020        PMID: 33355097      PMCID: PMC8090876          DOI: 10.1128/AEM.02235-20

Source DB:  PubMed          Journal:  Appl Environ Microbiol        ISSN: 0099-2240            Impact factor:   4.792


  92 in total

Review 1.  Dimethylsulfoniopropionate: its sources, role in the marine food web, and biological degradation to dimethylsulfide.

Authors:  Duane C Yoch
Journal:  Appl Environ Microbiol       Date:  2002-12       Impact factor: 4.792

2.  Dimethylsulfoniopropionate biosynthesis in marine bacteria and identification of the key gene in this process.

Authors:  Andrew R J Curson; Ji Liu; Ana Bermejo Martínez; Robert T Green; Yohan Chan; Ornella Carrión; Beth T Williams; Sheng-Hui Zhang; Gui-Peng Yang; Philip C Bulman Page; Xiao-Hua Zhang; Jonathan D Todd
Journal:  Nat Microbiol       Date:  2017-02-13       Impact factor: 17.745

Review 3.  Back to log phase: sigma S as a global regulator in the osmotic control of gene expression in Escherichia coli.

Authors:  R Hengge-Aronis
Journal:  Mol Microbiol       Date:  1996-09       Impact factor: 3.501

Review 4.  Osmoadaptation in bacteria.

Authors:  E A Galinski
Journal:  Adv Microb Physiol       Date:  1995       Impact factor: 3.517

5.  Taxonomy and description of Vibrio fluvialis sp. nov. (synonym group F vibrios, group EF6).

Authors:  J V Lee; P Shread; A L Furniss; T N Bryant
Journal:  J Appl Bacteriol       Date:  1981-02

6.  Synthesis of the osmoprotectant glycine betaine in Bacillus subtilis: characterization of the gbsAB genes.

Authors:  J Boch; B Kempf; R Schmid; E Bremer
Journal:  J Bacteriol       Date:  1996-09       Impact factor: 3.490

7.  Genetic diversity of clinical and environmental Vibrio parahaemolyticus strains from the Pacific Northwest.

Authors:  Rohinee Paranjpye; Owen S Hamel; Asta Stojanovski; Martin Liermann
Journal:  Appl Environ Microbiol       Date:  2012-10-05       Impact factor: 4.792

8.  DddQ, a novel, cupin-containing, dimethylsulfoniopropionate lyase in marine roseobacters and in uncultured marine bacteria.

Authors:  Jonathan D Todd; Andrew R J Curson; Mark Kirkwood; Matthew J Sullivan; Robert T Green; Andrew W B Johnston
Journal:  Environ Microbiol       Date:  2010-09-30       Impact factor: 5.491

9.  Bacterial Catabolism of Dimethylsulfoniopropionate (DMSP).

Authors:  Chris R Reisch; Mary Ann Moran; William B Whitman
Journal:  Front Microbiol       Date:  2011-08-12       Impact factor: 5.640

10.  The ability of algal organic matter and surface runoff to promote the abundance of pathogenic and non-pathogenic strains of Vibrio parahaemolyticus in Long Island Sound, USA.

Authors:  Jake D Thickman; Christopher J Gobler
Journal:  PLoS One       Date:  2017-10-11       Impact factor: 3.240

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  1 in total

Review 1.  Climate Change Impacts on the Marine Cycling of Biogenic Sulfur: A Review.

Authors:  Rebecca Jackson; Albert Gabric
Journal:  Microorganisms       Date:  2022-08-05
  1 in total

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