Signal Percolation within a Bacterial Community

Joseph W. Larkin, Xiaoling Zhai, Kaito Kikuchi, Samuel E. Redford, Arthur Prindle, Jintao Liu, Sacha Greenfield, Aleksandra M. Walczak, Jordi Garcia-Ojalvo, Andrew Mugler, Gürol M. Süel*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

27 Scopus citations

Abstract

Signal transmission among cells enables long-range coordination in biological systems. However, the scarcity of quantitative measurements hinders the development of theories that relate signal propagation to cellular heterogeneity and spatial organization. We address this problem in a bacterial community that employs electrochemical cell-to-cell communication. We developed a model based on percolation theory, which describes how signals propagate through a heterogeneous medium. Our model predicts that signal transmission becomes possible when the community is organized near a critical phase transition between a disconnected and a fully connected conduit of signaling cells. By measuring population-level signal transmission with single-cell resolution in wild-type and genetically modified communities, we confirm that the spatial distribution of signaling cells is organized at the predicted phase transition. Our findings suggest that at this critical point, the population-level benefit of signal transmission outweighs the single-cell level cost. The bacterial community thus appears to be organized according to a theoretically predicted spatial heterogeneity that promotes efficient signal transmission. Long-range electrical signal transmission allows dense bacterial communities known as biofilms to coordinate their actions and collectively enhance their fitness. However, it remains unclear how the community is organized to enable efficient long-range signal transmission, especially given that the community-level benefit comes at a cost to individual cells that relay the signal. Here, we find that the biofilm copes with this cost-benefit problem by self-organizing at a theoretically defined tipping point (critical phase transition). At this critical point, the system transitions from having only short-range connectivity among a few cells to a fully connected conduit of signaling cells that span the entire community. Using mutant biofilms, we show that this regimen optimally balances the cost and benefit of electrical signal transmission. The opposing constraints of performing a function that inherently carries a cost thus appear to drive a biological system to self-organize its heterogeneity at a critical phase transition.

Original languageEnglish (US)
Pages (from-to)137-145.e3
JournalCell Systems
Volume7
Issue number2
DOIs
StatePublished - Aug 22 2018

Keywords

  • biofilms
  • criticality
  • percolation
  • self-organization
  • signal transmission

ASJC Scopus subject areas

  • Pathology and Forensic Medicine
  • Histology
  • Cell Biology

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