Muc2-dependent microbial colonization of the jejunal mucus layer is diet sensitive and confers local resistance to enteric pathogen infection
Summary: Intestinal mucus barriers normally prevent microbial infections but are sensitive to diet-dependent changes in the luminal environment. Here we demonstrate that mice fed a Western-style diet (WSD) suffer regiospecific failure of the mucus barrier in the small intestinal jejunum caused by di...
| Main Authors: | , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2023-02-01
|
| Series: | Cell Reports |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124723000955 |
| _version_ | 1811169505462714368 |
|---|---|
| author | George M.H. Birchenough Bjoern O. Schroeder Sinan Sharba Liisa Arike Christian V. Recktenwald Fabiola Puértolas-Balint Mahadevan V. Subramani Karl T. Hansson Bahtiyar Yilmaz Sara K. Lindén Fredrik Bäckhed Gunnar C. Hansson |
| author_facet | George M.H. Birchenough Bjoern O. Schroeder Sinan Sharba Liisa Arike Christian V. Recktenwald Fabiola Puértolas-Balint Mahadevan V. Subramani Karl T. Hansson Bahtiyar Yilmaz Sara K. Lindén Fredrik Bäckhed Gunnar C. Hansson |
| author_sort | George M.H. Birchenough |
| collection | DOAJ |
| description | Summary: Intestinal mucus barriers normally prevent microbial infections but are sensitive to diet-dependent changes in the luminal environment. Here we demonstrate that mice fed a Western-style diet (WSD) suffer regiospecific failure of the mucus barrier in the small intestinal jejunum caused by diet-induced mucus aggregation. Mucus barrier disruption due to either WSD exposure or chromosomal Muc2 deletion results in collapse of the commensal jejunal microbiota, which in turn sensitizes mice to atypical jejunal colonization by the enteric pathogen Citrobacter rodentium. We illustrate the jejunal mucus layer as a microbial habitat, and link the regiospecific mucus dependency of the microbiota to distinctive properties of the jejunal niche. Together, our data demonstrate a symbiotic mucus-microbiota relationship that normally prevents jejunal pathogen colonization, but is highly sensitive to disruption by exposure to a WSD. |
| first_indexed | 2024-04-10T16:43:31Z |
| format | Article |
| id | doaj.art-a96200ad06eb4e86aa3f1f03dd90aee0 |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-04-10T16:43:31Z |
| publishDate | 2023-02-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-a96200ad06eb4e86aa3f1f03dd90aee02023-02-08T04:16:45ZengElsevierCell Reports2211-12472023-02-01422112084Muc2-dependent microbial colonization of the jejunal mucus layer is diet sensitive and confers local resistance to enteric pathogen infectionGeorge M.H. Birchenough0Bjoern O. Schroeder1Sinan Sharba2Liisa Arike3Christian V. Recktenwald4Fabiola Puértolas-Balint5Mahadevan V. Subramani6Karl T. Hansson7Bahtiyar Yilmaz8Sara K. Lindén9Fredrik Bäckhed10Gunnar C. Hansson11Department of Medical Biochemistry & Cell Biology, Institute of Biomedicine, University of Gothenburg, Gothenburg, Sweden; Wallenberg Centre for Molecular & Translational Medicine, University of Gothenburg, Gothenburg, Sweden; Corresponding authorDepartment of Molecular Biology and Laboratory for Molecular Infection Medicine Sweden (MIMS), Umeå University, Umeå, Sweden; Wallenberg Laboratory, Department of Molecular and Clinical Medicine, Institute of Medicine, University of Gothenburg, Gothenburg, SwedenDepartment of Medical Biochemistry & Cell Biology, Institute of Biomedicine, University of Gothenburg, Gothenburg, SwedenDepartment of Medical Biochemistry & Cell Biology, Institute of Biomedicine, University of Gothenburg, Gothenburg, SwedenDepartment of Medical Biochemistry & Cell Biology, Institute of Biomedicine, University of Gothenburg, Gothenburg, SwedenDepartment of Molecular Biology and Laboratory for Molecular Infection Medicine Sweden (MIMS), Umeå University, Umeå, SwedenDepartment of Medical Biochemistry & Cell Biology, Institute of Biomedicine, University of Gothenburg, Gothenburg, Sweden; Wallenberg Centre for Molecular & Translational Medicine, University of Gothenburg, Gothenburg, SwedenDepartment of Medical Biochemistry & Cell Biology, Institute of Biomedicine, University of Gothenburg, Gothenburg, Sweden; Wallenberg Centre for Molecular & Translational Medicine, University of Gothenburg, Gothenburg, SwedenDepartment for BioMedical Research, University of Bern, Bern, SwitzerlandDepartment of Medical Biochemistry & Cell Biology, Institute of Biomedicine, University of Gothenburg, Gothenburg, SwedenWallenberg Laboratory, Department of Molecular and Clinical Medicine, Institute of Medicine, University of Gothenburg, Gothenburg, SwedenDepartment of Medical Biochemistry & Cell Biology, Institute of Biomedicine, University of Gothenburg, Gothenburg, SwedenSummary: Intestinal mucus barriers normally prevent microbial infections but are sensitive to diet-dependent changes in the luminal environment. Here we demonstrate that mice fed a Western-style diet (WSD) suffer regiospecific failure of the mucus barrier in the small intestinal jejunum caused by diet-induced mucus aggregation. Mucus barrier disruption due to either WSD exposure or chromosomal Muc2 deletion results in collapse of the commensal jejunal microbiota, which in turn sensitizes mice to atypical jejunal colonization by the enteric pathogen Citrobacter rodentium. We illustrate the jejunal mucus layer as a microbial habitat, and link the regiospecific mucus dependency of the microbiota to distinctive properties of the jejunal niche. Together, our data demonstrate a symbiotic mucus-microbiota relationship that normally prevents jejunal pathogen colonization, but is highly sensitive to disruption by exposure to a WSD.http://www.sciencedirect.com/science/article/pii/S2211124723000955CP: MicrobiologyCP: Immunology |
| spellingShingle | George M.H. Birchenough Bjoern O. Schroeder Sinan Sharba Liisa Arike Christian V. Recktenwald Fabiola Puértolas-Balint Mahadevan V. Subramani Karl T. Hansson Bahtiyar Yilmaz Sara K. Lindén Fredrik Bäckhed Gunnar C. Hansson Muc2-dependent microbial colonization of the jejunal mucus layer is diet sensitive and confers local resistance to enteric pathogen infection Cell Reports CP: Microbiology CP: Immunology |
| title | Muc2-dependent microbial colonization of the jejunal mucus layer is diet sensitive and confers local resistance to enteric pathogen infection |
| title_full | Muc2-dependent microbial colonization of the jejunal mucus layer is diet sensitive and confers local resistance to enteric pathogen infection |
| title_fullStr | Muc2-dependent microbial colonization of the jejunal mucus layer is diet sensitive and confers local resistance to enteric pathogen infection |
| title_full_unstemmed | Muc2-dependent microbial colonization of the jejunal mucus layer is diet sensitive and confers local resistance to enteric pathogen infection |
| title_short | Muc2-dependent microbial colonization of the jejunal mucus layer is diet sensitive and confers local resistance to enteric pathogen infection |
| title_sort | muc2 dependent microbial colonization of the jejunal mucus layer is diet sensitive and confers local resistance to enteric pathogen infection |
| topic | CP: Microbiology CP: Immunology |
| url | http://www.sciencedirect.com/science/article/pii/S2211124723000955 |
| work_keys_str_mv | AT georgemhbirchenough muc2dependentmicrobialcolonizationofthejejunalmucuslayerisdietsensitiveandconferslocalresistancetoentericpathogeninfection AT bjoernoschroeder muc2dependentmicrobialcolonizationofthejejunalmucuslayerisdietsensitiveandconferslocalresistancetoentericpathogeninfection AT sinansharba muc2dependentmicrobialcolonizationofthejejunalmucuslayerisdietsensitiveandconferslocalresistancetoentericpathogeninfection AT liisaarike muc2dependentmicrobialcolonizationofthejejunalmucuslayerisdietsensitiveandconferslocalresistancetoentericpathogeninfection AT christianvrecktenwald muc2dependentmicrobialcolonizationofthejejunalmucuslayerisdietsensitiveandconferslocalresistancetoentericpathogeninfection AT fabiolapuertolasbalint muc2dependentmicrobialcolonizationofthejejunalmucuslayerisdietsensitiveandconferslocalresistancetoentericpathogeninfection AT mahadevanvsubramani muc2dependentmicrobialcolonizationofthejejunalmucuslayerisdietsensitiveandconferslocalresistancetoentericpathogeninfection AT karlthansson muc2dependentmicrobialcolonizationofthejejunalmucuslayerisdietsensitiveandconferslocalresistancetoentericpathogeninfection AT bahtiyaryilmaz muc2dependentmicrobialcolonizationofthejejunalmucuslayerisdietsensitiveandconferslocalresistancetoentericpathogeninfection AT saraklinden muc2dependentmicrobialcolonizationofthejejunalmucuslayerisdietsensitiveandconferslocalresistancetoentericpathogeninfection AT fredrikbackhed muc2dependentmicrobialcolonizationofthejejunalmucuslayerisdietsensitiveandconferslocalresistancetoentericpathogeninfection AT gunnarchansson muc2dependentmicrobialcolonizationofthejejunalmucuslayerisdietsensitiveandconferslocalresistancetoentericpathogeninfection |