Metabolic basis of brain-like electrical signalling in bacterial communities

Author:

Martinez-Corral Rosa1ORCID,Liu Jintao2,Prindle Arthur34,Süel Gürol M.5,Garcia-Ojalvo Jordi1ORCID

Affiliation:

1. Department of Experimental and Health Sciences, Universitat Pompeu Fabra, Barcelona Biomedical Research Park, Barcelona 08003, Spain

2. Center for Infectious Diseases Research and Tsinghua-Peking Center for Life Sciences, School of Medicine, Tsinghua University, Beijing 100084, People's Republic of China

3. Department of Biochemistry and Molecular Genetics, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA

4. Center for Synthetic Biology, Northwestern University, Evanston, IL 60208, USA

5. Division of Biological Sciences, San Diego Center for Systems Biology and Center for Microbiome Innovation, University of California San Diego, La Jolla, CA 92093, USA

Abstract

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’.

Funder

National Institute of General Medical Sciences

Secretaría de Estado de Investigación, Desarrollo e Innovación

Agència de Gestió d'Ajuts Universitaris i de Recerca

Defense Advanced Research Projects Agency

National Institutes of Health

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Biochemistry, Genetics and Molecular Biology

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