Short-chain fatty acids: microbial metabolites that alleviate stress-induced brain–gut axis alterations
Open accessAbstract
KEY POINTS: Chronic (psychosocial) stress changes gut microbiota composition, as well as inducing behavioural and physiological deficits. The microbial metabolites short-chain fatty acids (SCFAs) have been implicated in gastrointestinal functional, (neuro)immune regulation and host metabolism, but their role in stress-induced behavioural and physiological alterations is poorly understood. Administration of SCFAs to mice undergoing psychosocial stress alleviates enduring alterations in anhedonia and heightened stress-responsiveness, as well as stress-induced increases in intestinal permeability. In contrast, chronic stress-induced alterations in body weight gain, faecal SCFAs and the gene expression of the SCFA receptors FFAR2 and FFAR3 remained unaffected by SCFA supplementation. These results present novel insights into mechanisms underpinning the influence of the gut microbiota on brain homeostasis, behaviour and host metabolism, informing the development of microbiota-targeted therapies for stress-related disorders. ABSTRACT: There is a growing recognition of the involvement of the gastrointestinal microbiota in the regulation of physiology and behaviour. Microbiota-derived metabolites play a central role in the communication between microbes and their host, with short-chain fatty acids (SCFAs) being perhaps the most studied. SCFAs are primarily derived from fermentation of dietary fibres and play a pivotal role in host gut, metabolic and immune function. All these factors have previously been demonstrated to be adversely affected by stress. Therefore, we sought to assess whether SCFA supplementation could counteract the enduring effects of chronic psychosocial stress. C57BL/6J male mice received oral supplementation of a mixture of the three principle SCFAs (acetate, propionate and butyrate). One week later, mice underwent 3 weeks of repeated psychosocial stress, followed by a comprehensive behavioural analysis. Finally, plasma corticosterone, faecal SCFAs and caecal microbiota composition were assessed. SCFA treatment alleviated psychosocial stress-induced alterations in reward-seeking behaviour, and increased responsiveness to an acute stressor and in vivo intestinal permeability. In addition, SCFAs exhibited behavioural test-specific antidepressant and anxiolytic effects, which were not present when mice had also undergone psychosocial stress. Stress-induced increases in body weight gain, faecal SCFAs and the colonic gene expression of the SCFA receptors free fatty acid receptors 2 and 3 remained unaffected by SCFA supplementation. Moreover, there were no collateral effects on caecal microbiota composition. Taken together, these data show that SCFA supplementation alleviates selective and enduring alterations induced by repeated psychosocial stress and these data may inform future research into microbiota-targeted therapies for stress-related disorders.
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The influence of the gut microbiota is not restricted to the gastrointestinal tract; it plays a major role in bidirectional communication between the gastrointestinal tract and the central nervous system.
“it plays a major role in the bidirectional communication between the GI tract and the central nervous system (CNS).”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [8]
SCFAs decreased anxiety- and depressive-like behavior in selective behavioral tests, which was not present when mice had previously undergone psychosocial stress.
“Also, SCFAs decreased anxietyand depressive-like behavior in selective behavioral tests, which was not present when mice had previously undergone psychosocial stress.”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as van de Wouw et al., 2018
In stressed mice, SCFA administration reduces HPA axis hyperactivity and intestinal permeability.
“In stressed mice, SCFA administration reduced HPA axis hyperactivity and intestinal permeability (291).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [291]
SCFAs produced by the gut microbiome have anti-inflammatory properties and can work to regulate the immune response.
“The SCFAs produced by the gut microbiome have anti-inflammatory properties and can work to regulate the immune response [54].”
From Effect of fecal microbiota transplant on symptoms of psychiatric disorders: a systematic review (2020) · cites this paper as [54]
In an animal model, administration of SCFAs reduced depressive-like behavior, stress responsiveness, and intestinal permeability associated with psychosocial stress.
“In an animal model, administration of SCFAs reduced behavioral deficits (depressive-like behavior), stress responsiveness and intestinal permeability associated with psychosocial stress (354)”
From Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health (2021) · cites this paper as [354]
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Self-citation
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“Studies on chronic psychosocial stress have also shown a possible application for prebiotics (154) and SCFAs (8) in reverting sociability impairment while also reducing stressinduced corticosterone release.”
BackgroundThe gut microbiota–brain axis in behaviour and brain disorders
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- Authors
- van de Wouw, M., Boehme, M., Lyte, J. M., Wiley, N., Strain, C., O'Sullivan, O., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F.
- Affiliations
- Department of Anatomy and Neuroscience University College Cork Cork Ireland
- University College Cork (IE)
- Teagasc - The Irish Agriculture and Food Development Authority (IE)
- APC Microbiome Ireland University College Cork Cork Ireland
- Corresponding author
- Cryan, John F.
- ORCID
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2018-08-28
- Volume
- 596
- Issue
- 20
- Pages
- 4923-4944
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- PMC
- PMC6187046
- OpenAlex
- W2891851874
- Cited by
- 789
- References
- 100
- Citations by year
- 2026: 87 · 2025: 121 · 2024: 140 · 2023: 98 · 2022: 116 · 2021: 87 · 2020: 79 · 2019: 51 · 2018: 8 · 2017: 1
- FWCI
- 20.01
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Arrow@dit (Dublin Institute of Technology) (submittedVersion)
- T-Stór (Teagasc) (submittedVersion, cc-by-nc-sa)
- Funders
- Science Foundation Ireland (15/JP‐HDHL/3270)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Keywords
- short-chain fatty acids, psychosocial stress, gut-brain axis, gut microbiota, anhedonia, stress responsiveness, intestinal permeability, corticosterone, free fatty acid receptors, FFAR2, FFAR3, cecal microbiota, antidepressant effects, anxiolytic effects, weight gain, butyrate, propionate, acetate
- MeSH terms
- Gastrointestinal Microbiome, Animals, Fatty Acids, Volatile, Intestinal Absorption, Male, Mice, Inbred C57BL, Social Behavior, Stress, Psychological, Maze Learning, Mice
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