TY - JOUR
T1 - Metabolic basis of brain-like electrical signalling in bacterial communities
AU - Martinez-Corral, Rosa
AU - Liu, Jintao
AU - Prindle, Arthur
AU - Süel, Gürol M.
AU - Garcia-Ojalvo, Jordi
N1 - Funding Information:
for Units of Excellence in R&D (Spanish Ministry of Economy and Competitiveness, MDM-2014-0370). G.M.S. acknowledges support for this research from the San Diego Center for Systems Biology (NIH grant no. P50 GM085764), the National Institute of General Medical Sciences (grant no. R01 GM121888), the Defense Advanced
Funding Information:
Data accessibility. This article has no additional data. Competing interests. We declare we have no competing interests. Funding. This work was supported by the Spanish Ministry of Economy and Competitiveness and FEDER (project no. FIS2015-66503-C3-1-P), and by the Generalitat de Catalunya (project no. 2017 SGR 1054). R.M.C. acknowledges financial support from La Caixa Foundation. J.G.O. acknowledges support from the ICREA Academia Programme and from the ‘María de Maeztu’ Programme
Publisher Copyright:
© 2019 The Author(s) Published by the Royal Society. All rights reserved.
PY - 2019
Y1 - 2019
N2 - Information processing in the mammalian brain relies on a careful regulation of the membrane potential dynamics of its constituent neurons, which propagates across the neuronal tissue via electrical signalling. We recently reported the existence of electrical signalling in a much simpler organism, the bacterium Bacillus subtilis. In dense bacterial communities known as biofilms, nutrient-deprived B. subtilis cells in the interior of the colony use electrical communication to transmit stress signals to the periphery, which interfere with the growth of peripheral cells and reduce nutrient consumption, thereby relieving stress from the interior. Here, we explicitly address the interplay between metabolism and electrophysiology in bacterial biofilms, by introducing a spatially extended mathematical model that combines the metabolic and electrical components of the phenomenon in a discretized reaction - diffusion scheme. The model is experimentally validated by environmental and genetic perturbations, and confirms that metabolic stress is transmitted through the bacterial population via a potassium wave. Interestingly, this behaviour is reminiscent of cortical spreading depression in the brain, characterized by a wave of electrical activity mediated by potassium diffusion that has been linked to various neurological disorders, calling for future studies on the evolutionary link between the two phenomena. This article is part of the theme issue 'Liquid brains, solid brains: How distributed cognitive architectures process information'.
AB - Information processing in the mammalian brain relies on a careful regulation of the membrane potential dynamics of its constituent neurons, which propagates across the neuronal tissue via electrical signalling. We recently reported the existence of electrical signalling in a much simpler organism, the bacterium Bacillus subtilis. In dense bacterial communities known as biofilms, nutrient-deprived B. subtilis cells in the interior of the colony use electrical communication to transmit stress signals to the periphery, which interfere with the growth of peripheral cells and reduce nutrient consumption, thereby relieving stress from the interior. Here, we explicitly address the interplay between metabolism and electrophysiology in bacterial biofilms, by introducing a spatially extended mathematical model that combines the metabolic and electrical components of the phenomenon in a discretized reaction - diffusion scheme. The model is experimentally validated by environmental and genetic perturbations, and confirms that metabolic stress is transmitted through the bacterial population via a potassium wave. Interestingly, this behaviour is reminiscent of cortical spreading depression in the brain, characterized by a wave of electrical activity mediated by potassium diffusion that has been linked to various neurological disorders, calling for future studies on the evolutionary link between the two phenomena. This article is part of the theme issue 'Liquid brains, solid brains: How distributed cognitive architectures process information'.
KW - Bacterial biofilms
KW - Cellular excitability
KW - Electrical signalling
KW - Membrane potential
KW - Potassium waves
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U2 - 10.1098/rstb.2018.0382
DO - 10.1098/rstb.2018.0382
M3 - Article
C2 - 31006362
AN - SCOPUS:85065087829
VL - 374
JO - Philosophical Transactions of the Royal Society B: Biological Sciences
JF - Philosophical Transactions of the Royal Society B: Biological Sciences
SN - 0800-4622
IS - 1774
M1 - 20180382
ER -