Surface remodeling and inversion of cell-matrix interactions underlie community recognition and dispersal in Vibrio cholerae biofilms
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 in...
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| Language: | English |
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Nature Portfolio
2025-01-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-55602-2 |
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| author | 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 D. Nadell Wai-Leung Ng Vernita Gordon Natalia L. Komarova Rich Olson Ying Li Jing Yan |
| author_facet | 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 D. Nadell Wai-Leung Ng Vernita Gordon Natalia L. Komarova Rich Olson Ying Li Jing Yan |
| author_sort | Alexis Moreau |
| collection | DOAJ |
| description | 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. |
| format | Article |
| id | doaj-art-38f970a9a95d42f6af97df194f561929 |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-38f970a9a95d42f6af97df194f5619292025-01-05T12:37:55ZengNature PortfolioNature Communications2041-17232025-01-0116111610.1038/s41467-024-55602-2Surface remodeling and inversion of cell-matrix interactions underlie community recognition and dispersal in Vibrio cholerae biofilmsAlexis Moreau0Danh T. Nguyen1Alexander J. Hinbest2Anthony Zamora3Ranjuna Weerasekera4Katherine Matej5Xuening Zhou6Sandra Sanchez7Ignacio Rodriguez Brenes8Jung-Shen Benny Tai9Carey D. Nadell10Wai-Leung Ng11Vernita Gordon12Natalia L. Komarova13Rich Olson14Ying Li15Jing Yan16Department of Molecular, Cellular and Developmental Biology, Yale UniversityDepartment of Mechanical Engineering, University of Wisconsin-MadisonDepartment of Molecular Biology and Biochemistry, Molecular Biophysics Program, Wesleyan UniversityDepartment of Mathematics, University of California IrvineDepartment of Molecular Biology and Biochemistry, Molecular Biophysics Program, Wesleyan UniversityDepartment of Molecular, Cellular and Developmental Biology, Yale UniversityInterdisciplinary Life Sciences Graduate Program, Center for Nonlinear Dynamics, The University of Texas at AustinDepartment of Molecular Biology and Microbiology, Tufts University School of MedicineDepartment of Mathematics, University of California IrvineDepartment of Molecular, Cellular and Developmental Biology, Yale UniversityDepartment of Biological Sciences, Dartmouth ColleagueDepartment of Molecular Biology and Microbiology, Tufts University School of MedicineInterdisciplinary Life Sciences Graduate Program, Center for Nonlinear Dynamics, The University of Texas at AustinDepartment of Mathematics, University of California San DiegoDepartment of Molecular Biology and Biochemistry, Molecular Biophysics Program, Wesleyan UniversityDepartment of Mechanical Engineering, University of Wisconsin-MadisonDepartment of Molecular, Cellular and Developmental Biology, Yale UniversityAbstract 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.https://doi.org/10.1038/s41467-024-55602-2 |
| spellingShingle | 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 D. Nadell Wai-Leung Ng Vernita Gordon Natalia L. Komarova Rich Olson Ying Li Jing Yan Surface remodeling and inversion of cell-matrix interactions underlie community recognition and dispersal in Vibrio cholerae biofilms Nature Communications |
| title | Surface remodeling and inversion of cell-matrix interactions underlie community recognition and dispersal in Vibrio cholerae biofilms |
| title_full | Surface remodeling and inversion of cell-matrix interactions underlie community recognition and dispersal in Vibrio cholerae biofilms |
| title_fullStr | Surface remodeling and inversion of cell-matrix interactions underlie community recognition and dispersal in Vibrio cholerae biofilms |
| title_full_unstemmed | Surface remodeling and inversion of cell-matrix interactions underlie community recognition and dispersal in Vibrio cholerae biofilms |
| title_short | Surface remodeling and inversion of cell-matrix interactions underlie community recognition and dispersal in Vibrio cholerae biofilms |
| title_sort | surface remodeling and inversion of cell matrix interactions underlie community recognition and dispersal in vibrio cholerae biofilms |
| url | https://doi.org/10.1038/s41467-024-55602-2 |
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