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 in | Frontiers in microbiology Vol. 15; p. 1441126 |
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Main Authors | , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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15.01.2025
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ISSN | 1664-302X 1664-302X |
DOI | 10.3389/fmicb.2024.1441126 |
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Abstract | 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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AbstractList | Background/aimsDigestive 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.MethodsJejunal 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.ResultsCold pain stress was associated with a significant decrease in alpha diversity (P = 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.ConclusionsAcute 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. 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. 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.Background/aimsDigestive 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.MethodsJejunal 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 (P = 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.ResultsCold pain stress was associated with a significant decrease in alpha diversity (P = 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.ConclusionsAcute 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. |
Author | Alonso-Cotoner, Carmen Guagnozzi, Danila Pardo-Camacho, Cristina Salvo-Romero, Eloísa Expósito, Elba Gabaldón, Toni Nieto, Adoración Santos, Javier Martínez, Cristina Khannous-Lleiffe, Olfat Albert-Bayo, Mercé Vicario, María Pigrau, Marc González-Castro, Ana María Rodiño-Janeiro, Bruno K. Lobo, Beatriz Willis, Jesse R. Fortea, Marina |
AuthorAffiliation | 4 Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology , Barcelona , Spain 8 Renal Physiopathology Group, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus , Barcelona , Spain 6 Laboratory of Translational Mucosal Immunology, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus , Barcelona , Spain 1 Laboratory of Neuro-Immuno-Gastroenterology, Digestive System Research Unit, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus , Barcelona , Spain 5 Facultat de Medicina, Universitat Autònoma de Barcelona , Bellaterra , Spain 2 Department of Gastroenterology, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus , Barcelona , Spain 9 Catalan Institution for Research and Advanced Studies (ICREA) , Barcelona , Spain 3 Barcelo |
AuthorAffiliation_xml | – name: 5 Facultat de Medicina, Universitat Autònoma de Barcelona , Bellaterra , Spain – name: 3 Barcelona Supercomputing Centre (BSC-CNS) , Barcelona , Spain – name: 8 Renal Physiopathology Group, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus , Barcelona , Spain – name: 6 Laboratory of Translational Mucosal Immunology, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus , Barcelona , Spain – name: 1 Laboratory of Neuro-Immuno-Gastroenterology, Digestive System Research Unit, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus , Barcelona , Spain – name: 10 Centro de Investigación Biomédica En Red de Enfermedades Infecciosas (CIBERINFEC), Instituto de Salud Carlos III , Madrid , Spain – name: 9 Catalan Institution for Research and Advanced Studies (ICREA) , Barcelona , Spain – name: 2 Department of Gastroenterology, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus , Barcelona , Spain – name: 4 Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology , Barcelona , Spain – name: 7 Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), Instituto de Salud Carlos III , Madrid , Spain |
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Copyright | Copyright © 2025 Rodiño-Janeiro, Khannous-Lleiffe, Pigrau, Willis, Salvo-Romero, Nieto, Expósito, Fortea, Pardo-Camacho, Albert-Bayo, González-Castro, Guagnozzi, Martínez, Lobo, Vicario, Santos, Gabaldón and Alonso-Cotoner. Copyright © 2025 Rodiño-Janeiro, Khannous-Lleiffe, Pigrau, Willis, Salvo-Romero, Nieto, Expósito, Fortea, Pardo-Camacho, Albert-Bayo, González-Castro, Guagnozzi, Martínez, Lobo, Vicario, Santos, Gabaldón and Alonso-Cotoner. 2025 Rodiño-Janeiro, Khannous-Lleiffe, Pigrau, Willis, Salvo-Romero, Nieto, Expósito, Fortea, Pardo-Camacho, Albert-Bayo, González-Castro, Guagnozzi, Martínez, Lobo, Vicario, Santos, Gabaldón and Alonso-Cotoner |
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Keywords | small intestine microbiota stress functional dyspepsia irritable bowel syndrome disorders of gut-brain interaction |
Language | English |
License | Copyright © 2025 Rodiño-Janeiro, Khannous-Lleiffe, Pigrau, Willis, Salvo-Romero, Nieto, Expósito, Fortea, Pardo-Camacho, Albert-Bayo, González-Castro, Guagnozzi, Martínez, Lobo, Vicario, Santos, Gabaldón and Alonso-Cotoner. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 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 |
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SubjectTerms | disorders of gut-brain interaction functional dyspepsia irritable bowel syndrome Microbiology small intestine microbiota stress |
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Title | Acute stress triggers sex-dependent rapid alterations in the human small intestine microbiota composition |
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