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Strong chemotaxis by marine bacteria towards polysaccharides is enhanced by the abundant organosulfur compound DMSP.

ABSTRACT: The ability of marine bacteria to direct their movement in response to chemical gradients influences inter-species interactions, nutrient turnover, and ecosystem productivity. While many bacteria are chemotactic towards small metabolites, marine organic matter is predominantly composed of large molecules and polymers. Yet, the signalling role of these large molecules is largely unknown. Using in situ and laboratory-based chemotaxis assays, we show that marine bacteria are strongly attracted to the abundant algal polysaccharides laminarin and alginate. Unexpectedly, these polysaccharides elicited stronger chemoattraction than their oligo- and monosaccharide constituents. Furthermore, chemotaxis towards laminarin was strongly enhanced by dimethylsulfoniopropionate (DMSP), another ubiquitous algal-derived metabolite. Our results indicate that DMSP acts as a methyl donor for marine bacteria, increasing their gradient detection capacity and facilitating their access to polysaccharide patches. We demonstrate that marine bacteria are capable of strong chemotaxis towards large soluble polysaccharides and uncover a new ecological role for DMSP in enhancing this attraction. These navigation behaviours may contribute to the rapid turnover of polymers in the ocean, with important consequences for marine carbon cycling.

SUBMITTER: Clerc EE

PROVIDER: S-EPMC10700628 | biostudies-literature | 2023 Dec

REPOSITORIES: biostudies-literature

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Strong chemotaxis by marine bacteria towards polysaccharides is enhanced by the abundant organosulfur compound DMSP.

Clerc Estelle E EE Raina Jean-Baptiste JB Keegstra Johannes M JM Landry Zachary Z Pontrelli Sammy S Alcolombri Uria U Lambert Bennett S BS Anelli Valerio V Vincent Flora F Masdeu-Navarro Marta M Sichert Andreas A De Schaetzen Frédéric F Sauer Uwe U Simó Rafel R Hehemann Jan-Hendrik JH Vardi Assaf A Seymour Justin R JR Stocker Roman R

Nature communications 20231206 1

The ability of marine bacteria to direct their movement in response to chemical gradients influences inter-species interactions, nutrient turnover, and ecosystem productivity. While many bacteria are chemotactic towards small metabolites, marine organic matter is predominantly composed of large molecules and polymers. Yet, the signalling role of these large molecules is largely unknown. Using in situ and laboratory-based chemotaxis assays, we show that marine bacteria are strongly attracted to t ...[more]

PMID: 38057294

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Project description: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.

Project description:Emiliania huxleyi is a unicellular micro-alga that forms massive oceanic blooms and plays key roles in global biogeochemical cycles. Mounting studies demonstrate various stimulatory and inhibitory influences that bacteria have on the E. huxleyi physiology. To investigate these algal-bacterial interactions, laboratory co-cultures have been established by us and by others. Owing to these co-cultures, various mechanisms of algal-bacterial interactions have been revealed, many involving bacterial pathogenicity towards algae. However, co-cultures represent a significantly simplified system, lacking the complexity of bacterial communities. In order to investigate bacterial pathogenicity within an ecologically relevant context, it becomes imperative to enhance the microbial complexity of co-culture setups. Phaeobacter inhibens bacteria are known pathogens that cause the death of E. huxleyi algae in laboratory co-culture systems. The bacteria depend on algal exudates for growth, but when algae senesce, bacteria switch to a pathogenic state and induce algal death. Here we investigate whether P. inhibens bacteria can induce algal death in the presence of a complex bacterial community. We show that an E. huxleyi-associated bacterial community protects the alga from the pathogen, although the pathogen occurs within the community. To study how the bacterial community regulates pathogenicity, we reduced the complex bacterial community to a five-member synthetic community (syncom). The syncom is comprised of a single algal host and five isolated bacterial species, which represent major bacterial groups that are naturally associated with E. huxleyi. We discovered that a single bacterial species in the reduced community, Sulfitobacter pontiacus, protects the alga from the pathogen. We further found that algal protection from P. inhibens pathogenicity is a shared trait among several Sulfitobacter species. Algal protection by bacteria might be a common phenomenon with ecological significance, which is overlooked in reduced co-culture systems.

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Strong chemotaxis by marine bacteria towards polysaccharides is enhanced by the abundant organosulfur compound DMSP.

Publications

Strong chemotaxis by marine bacteria towards polysaccharides is enhanced by the abundant organosulfur compound DMSP.

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