Article | Published:

Ion channels enable electrical communication in bacterial communities

Nature volume 527, pages 5963 (05 November 2015) | Download Citation

Abstract

The study of bacterial ion channels has provided fundamental insights into the structural basis of neuronal signalling; however, the native role of ion channels in bacteria has remained elusive. Here we show that ion channels conduct long-range electrical signals within bacterial biofilm communities through spatially propagating waves of potassium. These waves result from a positive feedback loop, in which a metabolic trigger induces release of intracellular potassium, which in turn depolarizes neighbouring cells. Propagating through the biofilm, this wave of depolarization coordinates metabolic states among cells in the interior and periphery of the biofilm. Deletion of the potassium channel abolishes this response. As predicted by a mathematical model, we further show that spatial propagation can be hindered by specific genetic perturbations to potassium channel gating. Together, these results demonstrate a function for ion channels in bacterial biofilms, and provide a prokaryotic paradigm for active, long-range electrical signalling in cellular communities.

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Acknowledgements

We would like to thank S. Lockless, K. Süel, R. Wollman, T. Çağatay and M. Elowitz for comments during the writing of the manuscript, and C. Piggott for cloning help. A.P. is a Simons Foundation Fellow of the Helen Hay Whitney Foundation. J.G.-O. is supported by the Ministerio de Economia y Competitividad (Spain) and FEDER, under project FIS2012-37655-C02-01, and by the ICREA Academia Programme. This research was funded by the National Institutes of Health, National Institute of General Medical Sciences Grant R01 GM088428 and the National Science Foundation Grant MCB-1450867 50867 (both to G.M.S.). This work was also supported by the San Diego Center for Systems Biology (NIH Grant P50 GM085764).

Author information

Author notes

    • Jintao Liu
    •  & Munehiro Asally

    These authors contributed equally to this work.

Affiliations

  1. Division of Biological Sciences, University of California San Diego, California 92093, USA

    • Arthur Prindle
    • , Jintao Liu
    • , San Ly
    •  & Gürol M. Süel
  2. Warwick Integrative Synthetic Biology Centre, School of Life Sciences, University of Warwick, Coventry CV4 7AL, UK

    • Munehiro Asally
  3. Department of Experimental and Health Sciences, Universitat Pompeu Fabra, 08003 Barcelona, Spain

    • Jordi Garcia-Ojalvo

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Contributions

G.M.S., A.P., J.L., M.A. and J.G.-O. designed the research, A.P. and J.L. performed the experiments, J.L. and A.P. performed the data analysis, J.G.O. performed the mathematical modelling, S.L. made the bacteria strains, and G.M.S., A.P., J.L. and J.G.-O. wrote the manuscript. All authors discussed the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Gürol M. Süel.

Extended data

Supplementary information

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    Supplementary Information

    This file contains Supplementary Text and Data and Supplementary References.

Videos

  1. 1.

    Video 1: Global oscillations in membrane potential (ThT) in a growing biofilm.

    Global oscillations in membrane potential (ThT) in a growing biofilm.

  2. 2.

    Video 2: Waves of extracellular potassium (APG-4) in a growing biofilm.

    Waves of extracellular potassium (APG-4) in a growing biofilm.

  3. 3.

    Video 3: Oscillations in membrane potential (ThT) in a wild type and yugOΔtrkA mutant biofilm

    The yugOΔtrkA mutant strain lacks the gating domain for the YugO potassium channel and is unable to signal the edge of the biofilm.

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DOI

https://doi.org/10.1038/nature15709

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