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

Estelle E. Clerc, Jean-Baptiste Raina (), Johannes M. Keegstra, Zachary Landry, Sammy Pontrelli, Uria Alcolombri, Bennett S. Lambert, Valerio Anelli, Flora Vincent, Marta Masdeu-Navarro, Andreas Sichert, Frédéric Schaetzen, Uwe Sauer, Rafel Simó, Jan-Hendrik Hehemann, Assaf Vardi, Justin R. Seymour and Roman Stocker ()
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Estelle E. Clerc: Environmental and Geomatic Engineering, ETH Zurich
Jean-Baptiste Raina: University of Technology Sydney
Johannes M. Keegstra: Environmental and Geomatic Engineering, ETH Zurich
Zachary Landry: Environmental and Geomatic Engineering, ETH Zurich
Sammy Pontrelli: Institute of Molecular Systems Biology, Department of Biology, ETH Zurich
Uria Alcolombri: Environmental and Geomatic Engineering, ETH Zurich
Bennett S. Lambert: Environmental and Geomatic Engineering, ETH Zurich
Valerio Anelli: Environmental and Geomatic Engineering, ETH Zurich
Flora Vincent: Weizmann Institute of Science
Marta Masdeu-Navarro: Institut de Ciències del Mar, CSIC
Andreas Sichert: Max Planck Institute for Marine Microbiology
Frédéric Schaetzen: Environmental and Geomatic Engineering, ETH Zurich
Uwe Sauer: Institute of Molecular Systems Biology, Department of Biology, ETH Zurich
Rafel Simó: Institut de Ciències del Mar, CSIC
Jan-Hendrik Hehemann: Max Planck Institute for Marine Microbiology
Assaf Vardi: Weizmann Institute of Science
Justin R. Seymour: University of Technology Sydney
Roman Stocker: Environmental and Geomatic Engineering, ETH Zurich

Nature Communications, 2023, vol. 14, issue 1, 1-14

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-43143-z

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