Residual cells and nutrient availability guide wound healing in bacterial biofilms

Research output: Contribution to journalResearch articleContributedpeer-review

Contributors

  • Yusong Ye - , Friedrich-Alexander University Erlangen-Nürnberg, Max-Planck-Zentrum für Physik und Medizin (Author)
  • Mnar Ghrayeb - , Hebrew University of Jerusalem (Author)
  • Sarah Miercke - , Chair of General Microbiology (Author)
  • Sania Arif - , Helmholtz Centre for Environmental Research (Author)
  • Susann Müller - , Helmholtz Centre for Environmental Research (Author)
  • Thorsten Mascher - , Chair of General Microbiology (Author)
  • Liraz Chai - , Hebrew University of Jerusalem (Author)
  • Vasily Zaburdaev - , Friedrich-Alexander University Erlangen-Nürnberg, Max-Planck-Zentrum für Physik und Medizin (Author)

Abstract

Biofilms are multicellular heterogeneous bacterial communities characterized by social-like division of labor, and remarkable robustness with respect to external stresses. Increasingly often an analogy between biofilms and arguably more complex eukaryotic tissues is being drawn. One illustrative example of where this analogy can be practically useful is the process of wound healing. While it has been extensively studied in eukaryotic tissues, the mechanism of wound healing in biofilms is virtually unexplored. Combining experiments in Bacillus subtilis bacteria, a model organism for biofilm formation, and a lattice-based theoretical model of biofilm growth, we studied how biofilms recover after macroscopic damage. We suggest that nutrient gradients and the abundance of proliferating cells are key factors augmenting wound closure. Accordingly, in the model, cell quiescence, nutrient fluxes, and biomass represented by cells and self-secreted extracellular matrix are necessary to qualitatively recapitulate the experimental results for damage repair. One of the surprising experimental findings is that residual cells, persisting in a damaged area after removal of a part of the biofilm, prominently affect the healing process. Taken together, our results outline the important roles of nutrient gradients and residual cells on biomass regrowth on macroscopic scales of the whole biofilm. The proposed combined experiment-simulation framework opens the way to further investigate the possible relation between wound healing, cell signaling and cell phenotype alternation in the local microenvironment of the wound.

Details

Original languageEnglish
Pages (from-to)1047-1060
Number of pages14
JournalSoft matter
Volume20
Issue number5
Early online date22 Dec 2023
Publication statusPublished - 7 Feb 2024
Peer-reviewedYes

External IDs

PubMed 38205608

Keywords