From the Microbiome to the Electrome: Implications for the Microbiota–Gut–Brain Axis

Author:

Bourqqia-Ramzi Marwane12ORCID,Mansilla-Guardiola Jesús13ORCID,Muñoz-Rodriguez David1,Quarta Elisa14ORCID,Lombardo-Hernandez Juan1,Murciano-Cespedosa Antonio15,Conejero-Meca Francisco José1,Mateos González Álvaro16,Geuna Stefano7ORCID,Garcia-Esteban María Teresa3ORCID,Herrera-Rincon Celia1ORCID

Affiliation:

1. Modeling, Data Analysis &Computational Tools for Biology Research Group, Biomathematics Unit, Department of Biodiversity, Ecology & Evolution, Faculty of Biological Sciences, Complutense University of Madrid, 28040 Madrid, Spain

2. Department of Neurosciences “Rita Levi Montalcini”, University of Turin, 10126 Turin, Italy

3. Unit of Microbiology, Department of Genetic, Physiology and Microbiology, Faculty of Biological Sciences, Complutense University of Madrid, 28040 Madrid, Spain

4. Department of Molecular Biotechnology and Health Sciences, Molecular Biotechnology Center “Guido Tarone”, University of Torino, 10126 Turin, Italy

5. Neuro-Computing and Neuro-Robotics Research Group, Neural Plasticity Research Group Instituto Investigación Sanitaria Hospital Clínico San Carlos (IdISSC), Complutense University of Madrid, 28040 Madrid, Spain

6. University of Michigan-Shanghai Jiao Tong University Joint Institute, Shanghai Jiao Tong University, Shanghai 200240, China

7. Department of Clinical and Biological Sciences, Cavalieri Ottolenghi Neuroscience Institute, University of Turin, Ospedale San Luigi, 10043 Turin, Italy

Abstract

The gut microbiome plays a fundamental role in metabolism, as well as the immune and nervous systems. Microbial imbalance (dysbiosis) can contribute to subsequent physical and mental pathologies. As such, interest has been growing in the microbiota–gut–brain brain axis and the bioelectrical communication that could exist between bacterial and nervous cells. The aim of this study was to investigate the bioelectrical profile (electrome) of two bacterial species characteristic of the gut microbiome: a Proteobacteria Gram-negative bacillus Escherichia coli (E. coli), and a Firmicutes Gram-positive coccus Enterococcus faecalis (E. faecalis). We analyzed both bacterial strains to (i) validate the fluorescent probe bis-(1,3-dibutylbarbituric acid) trimethine oxonol, DiBAC4(3), as a reliable reporter of the changes in membrane potential (Vmem) for both bacteria; (ii) assess the evolution of the bioelectric profile throughout the growth of both strains; (iii) investigate the effects of two neural-type stimuli on Vmem changes: the excitatory neurotransmitter glutamate (Glu) and the inhibitory neurotransmitter γ-aminobutyric acid (GABA); (iv) examine the impact of the bioelectrical changes induced by neurotransmitters on bacterial growth, viability, and cultivability using absorbance, live/dead fluorescent probes, and viable counts, respectively. Our findings reveal distinct bioelectrical profiles characteristic of each bacterial species and growth phase. Importantly, neural-type stimuli induce Vmem changes without affecting bacterial growth, viability, or cultivability, suggesting a specific bioelectrical response in bacterial cells to neurotransmitter cues. These results contribute to understanding the bacterial response to external stimuli, with potential implications for modulating bacterial bioelectricity as a novel therapeutic target.

Funder

Ramon y Cajal program through the Spanish Ministry of Science, Research Agency

Computense University of Madrid

Publisher

MDPI AG

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