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

• Published in: International journal of molecular sciences Vol. 25; no. 11; p. 6233
• Main Authors: Bourqqia-Ramzi, Marwane, Mansilla-Guardiola, Jesús, Muñoz-Rodriguez, David, Quarta, Elisa, Lombardo-Hernandez, Juan, Murciano-Cespedosa, Antonio, Conejero-Meca, Francisco José, Mateos González, Álvaro, Geuna, Stefano, Garcia-Esteban, María Teresa, Herrera-Rincon, Celia
• Format: Journal Article
• Language: English
• Published: Switzerland MDPI AG 01-06-2024; MDPI
• Subjects: Bacteria; Biofilms; bis-(1,3-dibutylbarbituric acid) trimethine oxonol-DiBAC; Brain-Gut Axis - physiology; Cell division; Communication; E coli; Enterococcus faecalis - physiology; Escherichia coli; Ethylenediaminetetraacetic acid; GABA; gamma-Aminobutyric Acid - metabolism; Gastrointestinal Microbiome; Glutamate; Glutamic Acid - metabolism; Gram-positive; growth phase; Humans; membrane potential; Membrane Potentials; Metabolism; Metabolites; Microbiota; Microbiota (Symbiotic organisms); microbiota–gut–brain axis; Nervous system; neurotransmitters; Physiology; Probiotics; Scientific equipment and supplies industry; Statistical analysis; United States; Spain; bis-(1,3-dibutylbarbituric acid) trimethine oxonol-DiBAC; Gram-negative; Gram-positive; neurotransmitters; membrane potential; microbiota–gut–brain axis; growth phase
• ISSN: 1422-0067; 1661-6596; 1422-0067
• DOI: 10.3390/ijms25116233

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
(
), and a Firmicutes Gram-positive coccus
(
). 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.