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Bioelectrical State of Bacteria Is Linked to Growth Dynamics and Response to Neurotransmitters: Perspectives for the Investigation of the Microbiota–Brain Axis

Inter-cellular communication is mediated by a sum of biochemical, biophysical, and bioelectrical signals. This might occur not only between cells belonging to the same tissue and/or animal species but also between cells that are, from an evolutionary point of view, far away. The possibility that bio...

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Autores principales: Muñoz-Rodríguez, David, Bourqqia-Ramzi, Marwane, García-Esteban, Maria Teresa, Murciano-Cespedosa, Antonio, Vian, Alejandro, Lombardo-Hernández, Juan, García-Pérez, Pablo, Conejero, Francisco, Mateos González, Álvaro, Geuna, Stefano, Herrera-Rincon, Celia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10488255/
https://www.ncbi.nlm.nih.gov/pubmed/37686197
http://dx.doi.org/10.3390/ijms241713394
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author Muñoz-Rodríguez, David
Bourqqia-Ramzi, Marwane
García-Esteban, Maria Teresa
Murciano-Cespedosa, Antonio
Vian, Alejandro
Lombardo-Hernández, Juan
García-Pérez, Pablo
Conejero, Francisco
Mateos González, Álvaro
Geuna, Stefano
Herrera-Rincon, Celia
author_facet Muñoz-Rodríguez, David
Bourqqia-Ramzi, Marwane
García-Esteban, Maria Teresa
Murciano-Cespedosa, Antonio
Vian, Alejandro
Lombardo-Hernández, Juan
García-Pérez, Pablo
Conejero, Francisco
Mateos González, Álvaro
Geuna, Stefano
Herrera-Rincon, Celia
author_sort Muñoz-Rodríguez, David
collection PubMed
description Inter-cellular communication is mediated by a sum of biochemical, biophysical, and bioelectrical signals. This might occur not only between cells belonging to the same tissue and/or animal species but also between cells that are, from an evolutionary point of view, far away. The possibility that bioelectrical communication takes place between bacteria and nerve cells has opened exciting perspectives in the study of the gut microbiota–brain axis. The aim of this paper is (i) to establish a reliable method for the assessment of the bioelectrical state of two bacterial strains: Bacillus subtilis (B. subtilis) and Limosilactobacillus reuteri (L. reuteri); (ii) to monitor the bacterial bioelectrical profile throughout its growth dynamics; and (iii) to evaluate the effects of two neurotransmitters (glutamate and γ-aminobutyric acid-GABA) on the bioelectrical signature of bacteria. Our results show that membrane potential (Vmem) and the proliferative capacity of the population are functionally linked in B. subtilis in each phase of the cell cycle. Remarkably, we demonstrate that bacteria respond to neural signals by changing Vmem properties. Finally, we show that Vmem changes in response to neural stimuli are present also in a microbiota-related strain L. reuteri. Our proof-of-principle data reveal a new methodological approach for the better understanding of the relation between bacteria and the brain, with a special focus on gut microbiota. Likewise, this approach will open exciting perspectives in the study of the inter-cellular mechanisms which regulate the bi-directional communication between bacteria and neurons and, ultimately, for designing gut microbiota–brain axis-targeted treatments for neuropsychiatric diseases.
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spelling pubmed-104882552023-09-09 Bioelectrical State of Bacteria Is Linked to Growth Dynamics and Response to Neurotransmitters: Perspectives for the Investigation of the Microbiota–Brain Axis Muñoz-Rodríguez, David Bourqqia-Ramzi, Marwane García-Esteban, Maria Teresa Murciano-Cespedosa, Antonio Vian, Alejandro Lombardo-Hernández, Juan García-Pérez, Pablo Conejero, Francisco Mateos González, Álvaro Geuna, Stefano Herrera-Rincon, Celia Int J Mol Sci Article Inter-cellular communication is mediated by a sum of biochemical, biophysical, and bioelectrical signals. This might occur not only between cells belonging to the same tissue and/or animal species but also between cells that are, from an evolutionary point of view, far away. The possibility that bioelectrical communication takes place between bacteria and nerve cells has opened exciting perspectives in the study of the gut microbiota–brain axis. The aim of this paper is (i) to establish a reliable method for the assessment of the bioelectrical state of two bacterial strains: Bacillus subtilis (B. subtilis) and Limosilactobacillus reuteri (L. reuteri); (ii) to monitor the bacterial bioelectrical profile throughout its growth dynamics; and (iii) to evaluate the effects of two neurotransmitters (glutamate and γ-aminobutyric acid-GABA) on the bioelectrical signature of bacteria. Our results show that membrane potential (Vmem) and the proliferative capacity of the population are functionally linked in B. subtilis in each phase of the cell cycle. Remarkably, we demonstrate that bacteria respond to neural signals by changing Vmem properties. Finally, we show that Vmem changes in response to neural stimuli are present also in a microbiota-related strain L. reuteri. Our proof-of-principle data reveal a new methodological approach for the better understanding of the relation between bacteria and the brain, with a special focus on gut microbiota. Likewise, this approach will open exciting perspectives in the study of the inter-cellular mechanisms which regulate the bi-directional communication between bacteria and neurons and, ultimately, for designing gut microbiota–brain axis-targeted treatments for neuropsychiatric diseases. MDPI 2023-08-29 /pmc/articles/PMC10488255/ /pubmed/37686197 http://dx.doi.org/10.3390/ijms241713394 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Muñoz-Rodríguez, David
Bourqqia-Ramzi, Marwane
García-Esteban, Maria Teresa
Murciano-Cespedosa, Antonio
Vian, Alejandro
Lombardo-Hernández, Juan
García-Pérez, Pablo
Conejero, Francisco
Mateos González, Álvaro
Geuna, Stefano
Herrera-Rincon, Celia
Bioelectrical State of Bacteria Is Linked to Growth Dynamics and Response to Neurotransmitters: Perspectives for the Investigation of the Microbiota–Brain Axis
title Bioelectrical State of Bacteria Is Linked to Growth Dynamics and Response to Neurotransmitters: Perspectives for the Investigation of the Microbiota–Brain Axis
title_full Bioelectrical State of Bacteria Is Linked to Growth Dynamics and Response to Neurotransmitters: Perspectives for the Investigation of the Microbiota–Brain Axis
title_fullStr Bioelectrical State of Bacteria Is Linked to Growth Dynamics and Response to Neurotransmitters: Perspectives for the Investigation of the Microbiota–Brain Axis
title_full_unstemmed Bioelectrical State of Bacteria Is Linked to Growth Dynamics and Response to Neurotransmitters: Perspectives for the Investigation of the Microbiota–Brain Axis
title_short Bioelectrical State of Bacteria Is Linked to Growth Dynamics and Response to Neurotransmitters: Perspectives for the Investigation of the Microbiota–Brain Axis
title_sort bioelectrical state of bacteria is linked to growth dynamics and response to neurotransmitters: perspectives for the investigation of the microbiota–brain axis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10488255/
https://www.ncbi.nlm.nih.gov/pubmed/37686197
http://dx.doi.org/10.3390/ijms241713394
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