Collective polarization dynamics in bacterial colonies signify the occurrence of distinct subpopulations

PLoS Biol. 2023 Jan 18;21(1):e3001960. doi: 10.1371/journal.pbio.3001960. eCollection 2023 Jan.


Membrane potential in bacterial systems has been shown to be dynamic and tightly related to survivability at the single-cell level. However, little is known about spatiotemporal patterns of membrane potential in bacterial colonies and biofilms. Here, we discovered a transition from uncorrelated to collective dynamics within colonies formed by the human pathogen Neisseria gonorrhoeae. In freshly assembled colonies, polarization is heterogeneous with instances of transient and uncorrelated hyper- or depolarization of individual cells. As colonies reach a critical size, the polarization behavior transitions to collective dynamics: A hyperpolarized shell forms at the center, travels radially outward, and halts several micrometers from the colony periphery. Once the shell has passed, we detect an influx of potassium correlated with depolarization. Transient hyperpolarization also demarks the transition from volume to surface growth. By combining simulations and the use of an alternative electron acceptor for the respiratory chain, we provide strong evidence that local oxygen gradients shape the collective polarization dynamics. Finally, we show that within the hyperpolarized shell, tolerance against aminoglycoside antibiotics increases. These findings highlight that the polarization pattern can signify the differentiation into distinct subpopulations with different growth rates and antibiotic tolerance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aminoglycosides
  • Anti-Bacterial Agents / pharmacology
  • Biofilms*
  • Electron Transport
  • Humans
  • Neisseria gonorrhoeae*


  • Anti-Bacterial Agents
  • Aminoglycosides

Grants and funding

This work was supported by the Center for Molecular Medicine Cologne ( through grant B6 and the Deutsche Forschungsgemeinschaft ( through grant MA3898 granted to BM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.