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Surface remodeling and inversion of cell-matrix interactions underlie community recognition and dispersal in Vibrio cholerae biofilms

Author

Listed:
  • Alexis Moreau

    (Yale University)

  • Danh T. Nguyen

    (University of Wisconsin-Madison)

  • Alexander J. Hinbest

    (Wesleyan University)

  • Anthony Zamora

    (University of California Irvine)

  • Ranjuna Weerasekera

    (Wesleyan University)

  • Katherine Matej

    (Yale University)

  • Xuening Zhou

    (The University of Texas at Austin)

  • Sandra Sanchez

    (Tufts University School of Medicine)

  • Ignacio Rodriguez Brenes

    (University of California Irvine)

  • Jung-Shen Benny Tai

    (Yale University)

  • Carey D. Nadell

    (Dartmouth Colleague
    Geisel school of Medicine at Dartmouth)

  • Wai-Leung Ng

    (Tufts University School of Medicine)

  • Vernita Gordon

    (The University of Texas at Austin
    The University of Texas at Austin)

  • Natalia L. Komarova

    (University of California San Diego)

  • Rich Olson

    (Wesleyan University)

  • Ying Li

    (University of Wisconsin-Madison)

  • Jing Yan

    (Yale University
    Yale University)

Abstract

Biofilms are ubiquitous surface-associated bacterial communities embedded in an extracellular matrix. It is commonly assumed that biofilm cells are glued together by the matrix; however, how the specific biochemistry of matrix components affects the cell-matrix interactions and how these interactions vary during biofilm growth remain unclear. Here, we investigate cell-matrix interactions in Vibrio cholerae, the causative agent of cholera. We combine genetics, microscopy, simulations, and biochemical analyses to show that V. cholerae cells are not attracted to the main matrix component (Vibrio polysaccharide, VPS), but can be attached to each other and to the VPS network through surface-associated VPS and crosslinks formed by the protein Bap1. Downregulation of VPS production and surface trimming by the polysaccharide lyase RbmB cause surface remodeling as biofilms age, shifting the nature of cell-matrix interactions from attractive to repulsive and facilitating cell dispersal as aggregated groups. Our results shed light on the dynamics of diverse cell-matrix interactions as drivers of biofilm development.

Suggested Citation

  • Alexis Moreau & Danh T. Nguyen & Alexander J. Hinbest & Anthony Zamora & Ranjuna Weerasekera & Katherine Matej & Xuening Zhou & Sandra Sanchez & Ignacio Rodriguez Brenes & Jung-Shen Benny Tai & Carey , 2025. "Surface remodeling and inversion of cell-matrix interactions underlie community recognition and dispersal in Vibrio cholerae biofilms," Nature Communications, Nature, vol. 16(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-024-55602-2
    DOI: 10.1038/s41467-024-55602-2
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    References listed on IDEAS

    as
    1. Peter J. Lu & Emanuela Zaccarelli & Fabio Ciulla & Andrew B. Schofield & Francesco Sciortino & David A. Weitz, 2008. "Gelation of particles with short-range attraction," Nature, Nature, vol. 453(7194), pages 499-503, May.
    2. Jing Yan & Carey D. Nadell & Howard A. Stone & Ned S. Wingreen & Bonnie L. Bassler, 2017. "Extracellular-matrix-mediated osmotic pressure drives Vibrio cholerae biofilm expansion and cheater exclusion," Nature Communications, Nature, vol. 8(1), pages 1-11, December.
    3. Japinder Nijjer & Changhao Li & Qiuting Zhang & Haoran Lu & Sulin Zhang & Jing Yan, 2021. "Mechanical forces drive a reorientation cascade leading to biofilm self-patterning," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
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