Indole, a signaling molecule produced by the gut microbiota, negatively impacts emotional behaviors in rats
Open accessAbstract
Gut microbiota produces a wide and diverse array of metabolites that are an integral part of the host metabolome. The emergence of the gut microbiome-brain axis concept has prompted investigations on the role of gut microbiota dysbioses in the pathophysiology of brain diseases. Specifically, the search for microbe-related metabolomic signatures in human patients and animal models of psychiatric disorders has pointed out the importance of the microbial metabolism of aromatic amino acids. Here, we investigated the effect of indole on brain and behavior in rats. Indole is produced by gut microbiota from tryptophan, through the tryptophanase enzyme encoded by the tnaA gene. First, we mimicked an acute and high overproduction of indole by injecting this compound in the cecum of conventional rats. This treatment led to a dramatic decrease of motor activity. The neurodepressant oxidized derivatives of indole, oxindole and isatin, accumulated in the brain. In addition, increase in eye blinking frequency and in c-Fos protein expression in the dorsal vagal complex denoted a vagus nerve activation. Second, we mimicked a chronic and moderate overproduction of indole by colonizing germ-free rats with the indole-producing bacterial species Escherichia coli. We compared emotional behaviors of these rats with those of germ-free rats colonized with a genetically-engineered counterpart strain unable to produce indole. Rats overproducing indole displayed higher helplessness in the tail suspension test, and enhanced anxiety-like behavior in the novelty, elevated plus maze and open-field tests. Vagus nerve activation was suggested by an increase in eye blinking frequency. However, unlike the conventional rats dosed with a high amount of indole, the motor activity was not altered and neither oxindole nor isatin could be detected in the brain. Further studies are required for a comprehensive understanding of the mechanisms supporting indole effects on emotional behaviors. As our findings suggest that people whose gut microbiota is highly prone to produce indole could be more likely to develop anxiety and mood disorders, we addressed the issue of the inter-individual variability of indole producing potential in humans. An in silico investigation of metagenomic data focused on the tnaA gene products definitively proved this inter-individual variability.
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Overproduction of indoles resulted in anxiety- and depression-like behavior in animals.
“Although many important beneficial functions (e.g., antioxidative effect) have been linked to indoles, overproduction of these metabolites resulted in anxiety-and depression-like behavior in animals (404).”
From Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health (2021) · cites this paper as [404]
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- Authors
- Jaglin, M., Rhimi, M., Philippe, C., Pons, N., Bruneau, A., Goustard, B., Daugé, V., Maguin, E., Naudon, L., & Rabot, S.
- Affiliations
- AgroParisTech (FR)
- Université Paris-Saclay (FR)
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Naudon, Laurent
- Rabot, Sylvie
- ORCID
- Venue
- Frontiers in Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2018-04-09
- Volume
- 12
- Pages
- 216-216
- ISSN
- 1662-453X (ISSN-L)
- PMC
- PMC5900047
- OpenAlex
- W2793407886
- Cited by
- 269
- References
- 66
- Citations by year
- 2026: 17 · 2025: 33 · 2024: 52 · 2023: 37 · 2022: 42 · 2021: 33 · 2020: 34 · 2019: 17 · 2018: 4
- FWCI
- 7.83
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Frontiers in Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- HAL (submittedVersion, cc-by)
- HAL (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Institut National de la Recherche Agronomique
- Centre National de la Recherche Scientifique
- Ministère de l'Education Nationale, de l'Enseignement Supérieur et de la Recherche
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- indole, gut microbiota, gut-brain axis, tryptophan metabolism, tryptophanase, germ-free rats, Escherichia coli, anxiety-like behavior, helplessness, dorsal vagal complex, blinking, oxindoles, isatin, interindividual variability, metagenomics, emotional behavior
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