Gut microbiota regulates stress responsivity via the circadian system
Stress and circadian systems are interconnected through the hypothalamic-pituitary-adrenal (HPA) axis to maintain responses to external stimuli. Yet, the mechanisms of how such signals are orchestrated remain unknown. Here, we uncover the gut microbiota as a regulator of HPA-axis rhythmicity. Microbial depletion disturbs the brain transcriptome and metabolome in stress-responding pathways in the hippocampus and amygdala across the day. This is coupled with a dysregulation of the circadian pacemaker in the brain that results in perturbed glucocorticoid rhythmicity. The resulting hyper-activation of the HPA axis at the sleep/wake transition drives time-of-day-specific impairments of the stress response and stress-sensitive behaviors. Finally, microbiota transplantation confirmed that diurnal oscillations of gut microbes underlie altered glucocorticoid secretion and that L. reuteri is a candidate strain for such effects. Our data offer compelling evidence that the microbiota regulates stress responsiveness in a circadian manner and is necessary to respond adaptively to stressors throughout the day.
Authors
- Gerard Clarke (ORCID: https://orcid.org/0000-0001-9771-3979)
- Lars Wilmes (ORCID: https://orcid.org/0000-0002-7259-0084)
- Thomaz F. S. Bastiaanssen (ORCID: https://orcid.org/0000-0001-6891-734X)
- Cassandra Elise Gheorghe (ORCID: https://orcid.org/0000-0002-2749-1335)
- Sarah‐Jane Leigh (ORCID: https://orcid.org/0000-0002-6776-6487)
- Paromita Sen (ORCID: https://orcid.org/0000-0001-9862-6914)
- G. Tofani
- John F. Cryan (ORCID: https://orcid.org/0000-0001-5887-2723)
Institutions
- University College Cork (IE)
- APC Microbiome Institute (IE)
Publication Details
- Journal
- Cell Metabolism
- Published
- 2024-11-05
- DOI
- https://doi.org/10.1016/j.cmet.2024.10.003
- Citations
- 114
- Primary Topic
- Circadian rhythm and melatonin
- Type
- article
- Field-Weighted Citation Impact
- 31.23
Funders
- DuPont
- Ian's Friends Foundation
- Saks-Kavanaugh Foundation
- Science Foundation Ireland