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

Author

Listed:
  • 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
    The Hebrew University of Jerusalem)

  • Bennett S. Lambert

    (Environmental and Geomatic Engineering, ETH Zurich)

  • Valerio Anelli

    (Environmental and Geomatic Engineering, ETH Zurich)

  • Flora Vincent

    (Weizmann Institute of Science
    European Molecular Biological Laboratory)

  • 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)

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.

Suggested Citation

  • 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 & Andrea, 2023. "Strong chemotaxis by marine bacteria towards polysaccharides is enhanced by the abundant organosulfur compound DMSP," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43143-z
    DOI: 10.1038/s41467-023-43143-z
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    References listed on IDEAS

    as
    1. Flora Vincent & Matti Gralka & Guy Schleyer & Daniella Schatz & Miguel Cabrera-Brufau & Constanze Kuhlisch & Andreas Sichert & Silvia Vidal-Melgosa & Kyle Mayers & Noa Barak-Gavish & J. Michel Flores , 2023. "Viral infection switches the balance between bacterial and eukaryotic recyclers of organic matter during coccolithophore blooms," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Huang Lin & Shyamal Das Peddada, 2020. "Analysis of compositions of microbiomes with bias correction," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    3. Chris R. Reisch & Melissa J. Stoudemayer & Vanessa A. Varaljay & I. Jonathan Amster & Mary Ann Moran & William B. Whitman, 2011. "Novel pathway for assimilation of dimethylsulphoniopropionate widespread in marine bacteria," Nature, Nature, vol. 473(7346), pages 208-211, May.
    4. Jean-Baptiste Raina & Bennett S. Lambert & Donovan H. Parks & Christian Rinke & Nachshon Siboni & Anna Bramucci & Martin Ostrowski & Brandon Signal & Adrian Lutz & Himasha Mendis & Francesco Rubino & , 2022. "Chemotaxis shapes the microscale organization of the ocean’s microbiome," Nature, Nature, vol. 605(7908), pages 132-138, May.
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