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Ion channels enable electrical communication in bacterial communities

Author

Listed:
  • Arthur Prindle

    (University of California San Diego)

  • Jintao Liu

    (University of California San Diego)

  • Munehiro Asally

    (Warwick Integrative Synthetic Biology Centre, School of Life Sciences, University of Warwick)

  • San Ly

    (University of California San Diego)

  • Jordi Garcia-Ojalvo

    (Universitat Pompeu Fabra)

  • Gürol M. Süel

    (University of California San Diego)

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.

Suggested Citation

  • Arthur Prindle & Jintao Liu & Munehiro Asally & San Ly & Jordi Garcia-Ojalvo & Gürol M. Süel, 2015. "Ion channels enable electrical communication in bacterial communities," Nature, Nature, vol. 527(7576), pages 59-63, November.
    • Handle: RePEc:nat:nature:v:527:y:2015:i:7576:d:10.1038_nature15709
    DOI: 10.1038/nature15709
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    Cited by:

    1. Na Chen & Na Du & Ruichen Shen & Tianpei He & Jing Xi & Jie Tan & Guangkai Bian & Yanbing Yang & Tiangang Liu & Weihong Tan & Lilei Yu & Quan Yuan, 2023. "Redox signaling-driven modulation of microbial biosynthesis and biocatalysis," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Christwardana, Marcelinus & Frattini, Domenico & Accardo, Grazia & Yoon, Sung Pil & Kwon, Yongchai, 2018. "Early-stage performance evaluation of flowing microbial fuel cells using chemically treated carbon felt and yeast biocatalyst," Applied Energy, Elsevier, vol. 222(C), pages 369-382.
    3. Ashty S. Karim & Dylan M. Brown & Chloé M. Archuleta & Sharisse Grannan & Ludmilla Aristilde & Yogesh Goyal & Josh N. Leonard & Niall M. Mangan & Arthur Prindle & Gabriel J. Rocklin & Keith J. Tyo & L, 2024. "Deconstructing synthetic biology across scales: a conceptual approach for training synthetic biologists," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. Xiaoling Zhai & Joseph W Larkin & Kaito Kikuchi & Samuel E Redford & Ushasi Roy & Gürol M Süel & Andrew Mugler, 2019. "Statistics of correlated percolation in a bacterial community," PLOS Computational Biology, Public Library of Science, vol. 15(12), pages 1-19, December.
    5. Yan, Xuejun & Lee, Hyung-Sool & Li, Nan & Wang, Xin, 2020. "The micro-niche of exoelectrogens influences bioelectricity generation in bioelectrochemical systems," Renewable and Sustainable Energy Reviews, Elsevier, vol. 134(C).
    6. Michael F. Fuss & Jan-Philip Wieferig & Robin A. Corey & Yvonne Hellmich & Igor Tascón & Joana S. Sousa & Phillip J. Stansfeld & Janet Vonck & Inga Hänelt, 2023. "Cyclic di-AMP traps proton-coupled K+ transporters of the KUP family in an inward-occluded conformation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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