Acute stress triggers sex-dependent rapid alterations in the human small intestine microbiota composition

Digestive disorders of gut-brain interaction (DGBI) are very common, predominant in females, and usually associated with intestinal barrier dysfunction, dysbiosis, and stress. We previously found that females have increased susceptibility to intestinal barrier dysfunction in response to acute stress...

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Published inFrontiers in microbiology Vol. 15; p. 1441126
Main Authors Rodiño-Janeiro, Bruno K., Khannous-Lleiffe, Olfat, Pigrau, Marc, Willis, Jesse R., Salvo-Romero, Eloísa, Nieto, Adoración, Expósito, Elba, Fortea, Marina, Pardo-Camacho, Cristina, Albert-Bayo, Mercé, González-Castro, Ana María, Guagnozzi, Danila, Martínez, Cristina, Lobo, Beatriz, Vicario, María, Santos, Javier, Gabaldón, Toni, Alonso-Cotoner, Carmen
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 15.01.2025
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ISSN1664-302X
1664-302X
DOI10.3389/fmicb.2024.1441126

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Summary:Digestive disorders of gut-brain interaction (DGBI) are very common, predominant in females, and usually associated with intestinal barrier dysfunction, dysbiosis, and stress. We previously found that females have increased susceptibility to intestinal barrier dysfunction in response to acute stress. However, whether this is associated with changes in the small bowel microbiota remains unknown. We have evaluated changes in the small intestinal microbiota in response to acute stress to better understand stress-induced intestinal barrier dysfunction. Jejunal biopsies were obtained at baseline and 90 min after cold pain or sham stress. Autonomic (blood pressure and heart rate), hormonal (plasma cortisol and adrenocorticotropic hormone) and psychological (Subjective Stress Rating Scale) responses to cold pain and sham stress were monitored. Microbial DNA from the biopsies was analyzed using a 16S metabarcoding approach before and after cold pain stress and sham stress. Differences in diversity and relative abundance of microbial taxa were examined. Cold pain stress was associated with a significant decrease in alpha diversity ( = 0.015), which was more pronounced in females, along with significant sex differences in the abundance of specific taxa and the overall microbiota composition. Microbiota alterations significantly correlated with changes in psychological responses, hormones, and gene expression in the intestinal mucosal. Cold pain stress was also associated with activation of autonomic, hormonal and psychological response, with no differences between sexes. Acute stress elicits rapid alterations in bacterial composition in the jejunum of healthy subjects and these changes are more pronounced in females. Our results may contribute to the understanding of female predominance in DGBI.
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Edited by: Valeria D'Argenio, University of Naples Federico II, Italy
These authors share last authorship
Lorella Tripodi, Dipartimento di Medicina Molecolare e Biotecnologie Mediche (MMBM) Università Federico II di Napoli, Italy
These authors have contributed equally to this work and share first authorship
Present addresses: Bruno K. Rodiño-Janeiro, BFlow, Edificio Emprendia, Santiago de Compostela, Spain
Reviewed by: Muriel Larauche, University of California, Los Angeles, United States
María Vicario, Nestlé Institute of Health Sciences, Société des Produits Nestlé S.A., Lausanne, Switzerland
ISSN:1664-302X
1664-302X
DOI:10.3389/fmicb.2024.1441126