Literature DB >> 31006362

Metabolic basis of brain-like electrical signalling in bacterial communities.

Rosa Martinez-Corral1, Jintao Liu2, Arthur Prindle3,4, Gürol M Süel5, Jordi Garcia-Ojalvo1.   

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'.

Entities:  

Keywords:  bacterial biofilms; cellular excitability; electrical signalling; membrane potential; potassium waves

Mesh:

Year:  2019        PMID: 31006362      PMCID: PMC6553584          DOI: 10.1098/rstb.2018.0382

Source DB:  PubMed          Journal:  Philos Trans R Soc Lond B Biol Sci        ISSN: 0962-8436            Impact factor:   6.237


  32 in total

1.  How amoeboids self-organize into a fruiting body: multicellular coordination in Dictyostelium discoideum.

Authors:  A F Marée; P Hogeweg
Journal:  Proc Natl Acad Sci U S A       Date:  2001-03-27       Impact factor: 11.205

Review 2.  Phylogeny of ion channels: clues to structure and function.

Authors:  P A Anderson; R M Greenberg
Journal:  Comp Biochem Physiol B Biochem Mol Biol       Date:  2001-05       Impact factor: 2.231

Review 3.  Perspective of ions and messengers: an intricate link between potassium, glutamate, and cyclic di-AMP.

Authors:  Jan Gundlach; Fabian M Commichau; Jörg Stülke
Journal:  Curr Genet       Date:  2017-08-20       Impact factor: 3.886

4.  Fruiting body formation by Bacillus subtilis.

Authors:  S S Branda; J E González-Pastor; S Ben-Yehuda; R Losick; R Kolter
Journal:  Proc Natl Acad Sci U S A       Date:  2001-09-25       Impact factor: 11.205

5.  Coupling between distant biofilms and emergence of nutrient time-sharing.

Authors:  Jintao Liu; Rosa Martinez-Corral; Arthur Prindle; Dong-Yeon D Lee; Joseph Larkin; Marçal Gabalda-Sagarra; Jordi Garcia-Ojalvo; Gürol M Süel
Journal:  Science       Date:  2017-04-06       Impact factor: 47.728

6.  Characterization of the proton/glutamate symport protein of Bacillus subtilis and its functional expression in Escherichia coli.

Authors:  B Tolner; T Ubbink-Kok; B Poolman; W N Konings
Journal:  J Bacteriol       Date:  1995-05       Impact factor: 3.490

7.  NAD+ binding to the Escherichia coli K(+)-uptake protein TrkA and sequence similarity between TrkA and domains of a family of dehydrogenases suggest a role for NAD+ in bacterial transport.

Authors:  A Schlösser; A Hamann; D Bossemeyer; E Schneider; E P Bakker
Journal:  Mol Microbiol       Date:  1993-08       Impact factor: 3.501

8.  Dynamics of Ionic Shifts in Cortical Spreading Depression.

Authors:  Rune Enger; Wannan Tang; Gry Fluge Vindedal; Vidar Jensen; P Johannes Helm; Rolf Sprengel; Loren L Looger; Erlend A Nagelhus
Journal:  Cereb Cortex       Date:  2015-04-02       Impact factor: 5.357

9.  Gating of the TrkH ion channel by its associated RCK protein TrkA.

Authors:  Yu Cao; Yaping Pan; Hua Huang; Xiangshu Jin; Elena J Levin; Brian Kloss; Ming Zhou
Journal:  Nature       Date:  2013-04-18       Impact factor: 49.962

Review 10.  Independent origins of neurons and synapses: insights from ctenophores.

Authors:  Leonid L Moroz; Andrea B Kohn
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2016-01-05       Impact factor: 6.237

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  15 in total

1.  Liquid brains, solid brains.

Authors:  Ricard Solé; Melanie Moses; Stephanie Forrest
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2019-06-10       Impact factor: 6.237

2.  Understanding the evolution of interspecies interactions in microbial communities.

Authors:  Florien A Gorter; Michael Manhart; Martin Ackermann
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2020-03-23       Impact factor: 6.237

3.  Encoding Membrane-Potential-Based Memory within a Microbial Community.

Authors:  Chih-Yu Yang; Maja Bialecka-Fornal; Colleen Weatherwax; Joseph W Larkin; Arthur Prindle; Jintao Liu; Jordi Garcia-Ojalvo; Gürol M Süel
Journal:  Cell Syst       Date:  2020-04-27       Impact factor: 10.304

4.  Ion Transporting Proteins and Cancer: Progress and Perspectives.

Authors:  Mustafa B A Djamgoz
Journal:  Rev Physiol Biochem Pharmacol       Date:  2022       Impact factor: 5.545

5.  Technological Approach to Mind Everywhere: An Experimentally-Grounded Framework for Understanding Diverse Bodies and Minds.

Authors:  Michael Levin
Journal:  Front Syst Neurosci       Date:  2022-03-24

6.  Bringing Microbiology to Light: Toward All-Optical Electrophysiology in Bacteria.

Authors:  Giuseppe Maria Paternò; Gaia Bondelli; Guglielmo Lanzani
Journal:  Bioelectricity       Date:  2021-06-16

Review 7.  Valuing what happens: a biogenic approach to valence and (potentially) affect.

Authors:  Pamela Lyon; Franz Kuchling
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2021-01-25       Impact factor: 6.237

8.  Reframing cognition: getting down to biological basics.

Authors:  Pamela Lyon; Fred Keijzer; Detlev Arendt; Michael Levin
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2021-01-25       Impact factor: 6.237

Review 9.  IonoBiology: The functional dynamics of the intracellular metallome, with lessons from bacteria.

Authors:  Leticia Galera-Laporta; Colin J Comerci; Jordi Garcia-Ojalvo; Gürol M Süel
Journal:  Cell Syst       Date:  2021-06-16       Impact factor: 11.091

Review 10.  Evolution of glutamatergic signaling and synapses.

Authors:  Leonid L Moroz; Mikhail A Nikitin; Pavlin G Poličar; Andrea B Kohn; Daria Y Romanova
Journal:  Neuropharmacology       Date:  2021-07-31       Impact factor: 5.273

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