Acute stress triggers sex-dependent rapid alterations in the human small intestine microbiota composition
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...
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2025-01-01
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| author | Bruno K. Rodiño-Janeiro Bruno K. Rodiño-Janeiro Olfat Khannous-Lleiffe Olfat Khannous-Lleiffe Marc Pigrau Marc Pigrau Marc Pigrau Jesse R. Willis Jesse R. Willis Eloísa Salvo-Romero Eloísa Salvo-Romero Eloísa Salvo-Romero Adoración Nieto Adoración Nieto Elba Expósito Elba Expósito Elba Expósito Marina Fortea Marina Fortea Cristina Pardo-Camacho Cristina Pardo-Camacho Cristina Pardo-Camacho Mercé Albert-Bayo Mercé Albert-Bayo Ana María González-Castro Ana María González-Castro Ana María González-Castro Ana María González-Castro Danila Guagnozzi Danila Guagnozzi Danila Guagnozzi Danila Guagnozzi Cristina Martínez Cristina Martínez Cristina Martínez Beatriz Lobo Beatriz Lobo Beatriz Lobo Beatriz Lobo María Vicario María Vicario Javier Santos Javier Santos Javier Santos Javier Santos Toni Gabaldón Toni Gabaldón Toni Gabaldón Toni Gabaldón Carmen Alonso-Cotoner Carmen Alonso-Cotoner Carmen Alonso-Cotoner Carmen Alonso-Cotoner |
| author_facet | Bruno K. Rodiño-Janeiro Bruno K. Rodiño-Janeiro Olfat Khannous-Lleiffe Olfat Khannous-Lleiffe Marc Pigrau Marc Pigrau Marc Pigrau Jesse R. Willis Jesse R. Willis Eloísa Salvo-Romero Eloísa Salvo-Romero Eloísa Salvo-Romero Adoración Nieto Adoración Nieto Elba Expósito Elba Expósito Elba Expósito Marina Fortea Marina Fortea Cristina Pardo-Camacho Cristina Pardo-Camacho Cristina Pardo-Camacho Mercé Albert-Bayo Mercé Albert-Bayo Ana María González-Castro Ana María González-Castro Ana María González-Castro Ana María González-Castro Danila Guagnozzi Danila Guagnozzi Danila Guagnozzi Danila Guagnozzi Cristina Martínez Cristina Martínez Cristina Martínez Beatriz Lobo Beatriz Lobo Beatriz Lobo Beatriz Lobo María Vicario María Vicario Javier Santos Javier Santos Javier Santos Javier Santos Toni Gabaldón Toni Gabaldón Toni Gabaldón Toni Gabaldón Carmen Alonso-Cotoner Carmen Alonso-Cotoner Carmen Alonso-Cotoner Carmen Alonso-Cotoner |
| author_sort | Bruno K. Rodiño-Janeiro |
| collection | DOAJ |
| description | 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. |
| format | Article |
| id | doaj-art-1f22c7642ac749128a9e1be2cc35c85c |
| institution | Kabale University |
| issn | 1664-302X |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Frontiers Media S.A. |
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| spelling | doaj-art-1f22c7642ac749128a9e1be2cc35c85c2025-01-15T19:24:24ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-01-011510.3389/fmicb.2024.14411261441126Acute stress triggers sex-dependent rapid alterations in the human small intestine microbiota compositionBruno K. Rodiño-Janeiro0Bruno K. Rodiño-Janeiro1Olfat Khannous-Lleiffe2Olfat Khannous-Lleiffe3Marc Pigrau4Marc Pigrau5Marc Pigrau6Jesse R. Willis7Jesse R. Willis8Eloísa Salvo-Romero9Eloísa Salvo-Romero10Eloísa Salvo-Romero11Adoración Nieto12Adoración Nieto13Elba Expósito14Elba Expósito15Elba Expósito16Marina Fortea17Marina Fortea18Cristina Pardo-Camacho19Cristina Pardo-Camacho20Cristina Pardo-Camacho21Mercé Albert-Bayo22Mercé Albert-Bayo23Ana María González-Castro24Ana María González-Castro25Ana María González-Castro26Ana María González-Castro27Danila Guagnozzi28Danila Guagnozzi29Danila Guagnozzi30Danila Guagnozzi31Cristina Martínez32Cristina Martínez33Cristina Martínez34Beatriz Lobo35Beatriz Lobo36Beatriz Lobo37Beatriz Lobo38María Vicario39María Vicario40Javier Santos41Javier Santos42Javier Santos43Javier Santos44Toni Gabaldón45Toni Gabaldón46Toni Gabaldón47Toni Gabaldón48Carmen Alonso-Cotoner49Carmen Alonso-Cotoner50Carmen Alonso-Cotoner51Carmen Alonso-Cotoner52Laboratory 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, SpainDepartment of Gastroenterology, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainBarcelona Supercomputing Centre (BSC-CNS), Barcelona, SpainInstitute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology, Barcelona, SpainLaboratory 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, SpainDepartment of Gastroenterology, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainFacultat de Medicina, Universitat Autònoma de Barcelona, Bellaterra, SpainBarcelona Supercomputing Centre (BSC-CNS), Barcelona, SpainInstitute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology, Barcelona, SpainLaboratory 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, SpainDepartment of Gastroenterology, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainLaboratory of Translational Mucosal Immunology, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainLaboratory 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, SpainDepartment of Gastroenterology, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainLaboratory 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, SpainDepartment of Gastroenterology, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainLaboratory of Translational Mucosal Immunology, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainDepartment of Gastroenterology, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainLaboratory of Translational Mucosal Immunology, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainLaboratory 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, SpainDepartment of Gastroenterology, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainLaboratory of Translational Mucosal Immunology, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainDepartment of Gastroenterology, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainLaboratory of Translational Mucosal Immunology, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainLaboratory 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, SpainDepartment of Gastroenterology, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainLaboratory of Translational Mucosal Immunology, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainCentro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), Instituto de Salud Carlos III, Madrid, SpainLaboratory 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, SpainDepartment of Gastroenterology, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainLaboratory of Translational Mucosal Immunology, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainCentro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), Instituto de Salud Carlos III, Madrid, SpainLaboratory 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, SpainDepartment of Gastroenterology, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainRenal Physiopathology Group, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainLaboratory 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, SpainDepartment of Gastroenterology, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainFacultat de Medicina, Universitat Autònoma de Barcelona, Bellaterra, SpainCentro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), Instituto de Salud Carlos III, Madrid, SpainDepartment of Gastroenterology, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainLaboratory of Translational Mucosal Immunology, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainLaboratory 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, SpainDepartment of Gastroenterology, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainFacultat de Medicina, Universitat Autònoma de Barcelona, Bellaterra, SpainCentro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), Instituto de Salud Carlos III, Madrid, SpainBarcelona Supercomputing Centre (BSC-CNS), Barcelona, SpainInstitute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology, Barcelona, SpainCatalan Institution for Research and Advanced Studies (ICREA), Barcelona, Spain0Centro de Investigación Biomédica En Red de Enfermedades Infecciosas (CIBERINFEC), Instituto de Salud Carlos III, Madrid, SpainLaboratory 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, SpainDepartment of Gastroenterology, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, SpainFacultat de Medicina, Universitat Autònoma de Barcelona, Bellaterra, SpainCentro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), Instituto de Salud Carlos III, Madrid, SpainBackground/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.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1441126/fullstressfunctional dyspepsiadisorders of gut-brain interactionirritable bowel syndromesmall intestine microbiota |
| spellingShingle | Bruno K. Rodiño-Janeiro Bruno K. Rodiño-Janeiro Olfat Khannous-Lleiffe Olfat Khannous-Lleiffe Marc Pigrau Marc Pigrau Marc Pigrau Jesse R. Willis Jesse R. Willis Eloísa Salvo-Romero Eloísa Salvo-Romero Eloísa Salvo-Romero Adoración Nieto Adoración Nieto Elba Expósito Elba Expósito Elba Expósito Marina Fortea Marina Fortea Cristina Pardo-Camacho Cristina Pardo-Camacho Cristina Pardo-Camacho Mercé Albert-Bayo Mercé Albert-Bayo Ana María González-Castro Ana María González-Castro Ana María González-Castro Ana María González-Castro Danila Guagnozzi Danila Guagnozzi Danila Guagnozzi Danila Guagnozzi Cristina Martínez Cristina Martínez Cristina Martínez Beatriz Lobo Beatriz Lobo Beatriz Lobo Beatriz Lobo María Vicario María Vicario Javier Santos Javier Santos Javier Santos Javier Santos Toni Gabaldón Toni Gabaldón Toni Gabaldón Toni Gabaldón Carmen Alonso-Cotoner Carmen Alonso-Cotoner Carmen Alonso-Cotoner Carmen Alonso-Cotoner Acute stress triggers sex-dependent rapid alterations in the human small intestine microbiota composition Frontiers in Microbiology stress functional dyspepsia disorders of gut-brain interaction irritable bowel syndrome small intestine microbiota |
| title | Acute stress triggers sex-dependent rapid alterations in the human small intestine microbiota composition |
| title_full | Acute stress triggers sex-dependent rapid alterations in the human small intestine microbiota composition |
| title_fullStr | Acute stress triggers sex-dependent rapid alterations in the human small intestine microbiota composition |
| title_full_unstemmed | Acute stress triggers sex-dependent rapid alterations in the human small intestine microbiota composition |
| title_short | Acute stress triggers sex-dependent rapid alterations in the human small intestine microbiota composition |
| title_sort | acute stress triggers sex dependent rapid alterations in the human small intestine microbiota composition |
| topic | stress functional dyspepsia disorders of gut-brain interaction irritable bowel syndrome small intestine microbiota |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2024.1441126/full |
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