Comparing Campylobacter jejuni to three other enteric pathogens in OligoMM12 mice reveals pathogen-specific host and microbiota responses

Campylobacter jejuni, non-typhoidal Salmonella spp., Listeria monocytogenes and enteropathogenic/enterohemorrhagic Escherichia coli (EPEC/EHEC) are leading causes of food-borne illness worldwide. Citrobacter rodentium has been used to model EPEC and EHEC infection in mice. The gut microbiome is well...

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Main Authors: Mathias K.-M. Herzog, Audrey Peters, Nizar Shayya, Monica Cazzaniga, Kardokh Kaka Bra, Trisha Arora, Manja Barthel, Ersin Gül, Luca Maurer, Patrick Kiefer, Philipp Christen, Katharina Endhardt, Julia A. Vorholt, Gad Frankel, Markus M. Heimesaat, Stefan Bereswill, Cormac G. M. Gahan, Marcus J. Claesson, Xavier Domingo-Almenara, Wolf-Dietrich Hardt
Format: Article
Language:English
Published: Taylor & Francis Group 2025-12-01
Series:Gut Microbes
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Online Access:https://www.tandfonline.com/doi/10.1080/19490976.2024.2447832
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author Mathias K.-M. Herzog
Audrey Peters
Nizar Shayya
Monica Cazzaniga
Kardokh Kaka Bra
Trisha Arora
Manja Barthel
Ersin Gül
Luca Maurer
Patrick Kiefer
Philipp Christen
Katharina Endhardt
Julia A. Vorholt
Gad Frankel
Markus M. Heimesaat
Stefan Bereswill
Cormac G. M. Gahan
Marcus J. Claesson
Xavier Domingo-Almenara
Wolf-Dietrich Hardt
author_facet Mathias K.-M. Herzog
Audrey Peters
Nizar Shayya
Monica Cazzaniga
Kardokh Kaka Bra
Trisha Arora
Manja Barthel
Ersin Gül
Luca Maurer
Patrick Kiefer
Philipp Christen
Katharina Endhardt
Julia A. Vorholt
Gad Frankel
Markus M. Heimesaat
Stefan Bereswill
Cormac G. M. Gahan
Marcus J. Claesson
Xavier Domingo-Almenara
Wolf-Dietrich Hardt
author_sort Mathias K.-M. Herzog
collection DOAJ
description Campylobacter jejuni, non-typhoidal Salmonella spp., Listeria monocytogenes and enteropathogenic/enterohemorrhagic Escherichia coli (EPEC/EHEC) are leading causes of food-borne illness worldwide. Citrobacter rodentium has been used to model EPEC and EHEC infection in mice. The gut microbiome is well-known to affect gut colonization and host responses to many food-borne pathogens. Recent progress has established gnotobiotic mice as valuable models to study how microbiota affect the enteric infections by S. Typhimurium, C. rodentium and L. monocytogenes. However, for C. jejuni, we are still lacking a suitable gnotobiotic mouse model. Moreover, the limited comparability of data across laboratories is often negatively affected by variations between different research facilities or murine microbiotas. In this study, we applied the standardized gnotobiotic OligoMM12 microbiota mouse model and compared the infections in the same facility. We provide evidence of robust colonization and significant pathological changes in OligoMM12 mice following infection with these pathogens. Moreover, we offer insights into pathogen-specific host responses and metabolite signatures, highlighting the advantages of a standardized mouse model for direct comparisons of factors influencing the pathogenesis of major food-borne pathogens. Notably, we reveal for the first time that C. jejuni stably colonizes OligoMM12 mice, triggering inflammation. Additionally, our comparative approach successfully identifies pathogen-specific responses, including the detection of genes uniquely associated with C. jejuni infection in humans. These findings underscore the potential of the OligoMM12 model as a versatile tool for advancing our understanding of food-borne pathogen interactions.
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spelling doaj-art-b4e924c93ba04bef8a60c6b5b7af8d962025-01-21T09:27:00ZengTaylor & Francis GroupGut Microbes1949-09761949-09842025-12-0117110.1080/19490976.2024.2447832Comparing Campylobacter jejuni to three other enteric pathogens in OligoMM12 mice reveals pathogen-specific host and microbiota responsesMathias K.-M. Herzog0Audrey Peters1Nizar Shayya2Monica Cazzaniga3Kardokh Kaka Bra4Trisha Arora5Manja Barthel6Ersin Gül7Luca Maurer8Patrick Kiefer9Philipp Christen10Katharina Endhardt11Julia A. Vorholt12Gad Frankel13Markus M. Heimesaat14Stefan Bereswill15Cormac G. M. Gahan16Marcus J. Claesson17Xavier Domingo-Almenara18Wolf-Dietrich Hardt19Institute of Microbiology, Department of Biology, ETH Zurich, Zurich, SwitzerlandDepartment of Life Sciences, MRC Centre for Bacterial Resistance Biology, Imperial College London, London, UKGastrointestinal Microbiology Research Group, Institute of Microbiology, Infectious Diseases and Immunology, Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, GermanyAPC Microbiome Ireland, University College Cork, Cork, IrelandAPC Microbiome Ireland, University College Cork, Cork, IrelandOmic Sciences Unit, EURECAT – Technology Centre of Catalonia, Reus, SpainInstitute of Microbiology, Department of Biology, ETH Zurich, Zurich, SwitzerlandInstitute of Microbiology, Department of Biology, ETH Zurich, Zurich, SwitzerlandInstitute of Microbiology, Department of Biology, ETH Zurich, Zurich, SwitzerlandInstitute of Microbiology, Department of Biology, ETH Zurich, Zurich, SwitzerlandInstitute of Microbiology, Department of Biology, ETH Zurich, Zurich, SwitzerlandDepartment of Pathology and Molecular Pathology, University Hospital Zurich, Zurich, SwitzerlandInstitute of Microbiology, Department of Biology, ETH Zurich, Zurich, SwitzerlandDepartment of Life Sciences, MRC Centre for Bacterial Resistance Biology, Imperial College London, London, UKGastrointestinal Microbiology Research Group, Institute of Microbiology, Infectious Diseases and Immunology, Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, GermanyGastrointestinal Microbiology Research Group, Institute of Microbiology, Infectious Diseases and Immunology, Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, GermanyAPC Microbiome Ireland, University College Cork, Cork, IrelandAPC Microbiome Ireland, University College Cork, Cork, IrelandOmic Sciences Unit, EURECAT – Technology Centre of Catalonia, Reus, SpainInstitute of Microbiology, Department of Biology, ETH Zurich, Zurich, SwitzerlandCampylobacter jejuni, non-typhoidal Salmonella spp., Listeria monocytogenes and enteropathogenic/enterohemorrhagic Escherichia coli (EPEC/EHEC) are leading causes of food-borne illness worldwide. Citrobacter rodentium has been used to model EPEC and EHEC infection in mice. The gut microbiome is well-known to affect gut colonization and host responses to many food-borne pathogens. Recent progress has established gnotobiotic mice as valuable models to study how microbiota affect the enteric infections by S. Typhimurium, C. rodentium and L. monocytogenes. However, for C. jejuni, we are still lacking a suitable gnotobiotic mouse model. Moreover, the limited comparability of data across laboratories is often negatively affected by variations between different research facilities or murine microbiotas. In this study, we applied the standardized gnotobiotic OligoMM12 microbiota mouse model and compared the infections in the same facility. We provide evidence of robust colonization and significant pathological changes in OligoMM12 mice following infection with these pathogens. Moreover, we offer insights into pathogen-specific host responses and metabolite signatures, highlighting the advantages of a standardized mouse model for direct comparisons of factors influencing the pathogenesis of major food-borne pathogens. Notably, we reveal for the first time that C. jejuni stably colonizes OligoMM12 mice, triggering inflammation. Additionally, our comparative approach successfully identifies pathogen-specific responses, including the detection of genes uniquely associated with C. jejuni infection in humans. These findings underscore the potential of the OligoMM12 model as a versatile tool for advancing our understanding of food-borne pathogen interactions.https://www.tandfonline.com/doi/10.1080/19490976.2024.2447832Infectious diseasesmouse modelmicrobiotaCampylobacter jejuniListeria monocytogenesCitrobacter rodentium
spellingShingle Mathias K.-M. Herzog
Audrey Peters
Nizar Shayya
Monica Cazzaniga
Kardokh Kaka Bra
Trisha Arora
Manja Barthel
Ersin Gül
Luca Maurer
Patrick Kiefer
Philipp Christen
Katharina Endhardt
Julia A. Vorholt
Gad Frankel
Markus M. Heimesaat
Stefan Bereswill
Cormac G. M. Gahan
Marcus J. Claesson
Xavier Domingo-Almenara
Wolf-Dietrich Hardt
Comparing Campylobacter jejuni to three other enteric pathogens in OligoMM12 mice reveals pathogen-specific host and microbiota responses
Gut Microbes
Infectious diseases
mouse model
microbiota
Campylobacter jejuni
Listeria monocytogenes
Citrobacter rodentium
title Comparing Campylobacter jejuni to three other enteric pathogens in OligoMM12 mice reveals pathogen-specific host and microbiota responses
title_full Comparing Campylobacter jejuni to three other enteric pathogens in OligoMM12 mice reveals pathogen-specific host and microbiota responses
title_fullStr Comparing Campylobacter jejuni to three other enteric pathogens in OligoMM12 mice reveals pathogen-specific host and microbiota responses
title_full_unstemmed Comparing Campylobacter jejuni to three other enteric pathogens in OligoMM12 mice reveals pathogen-specific host and microbiota responses
title_short Comparing Campylobacter jejuni to three other enteric pathogens in OligoMM12 mice reveals pathogen-specific host and microbiota responses
title_sort comparing campylobacter jejuni to three other enteric pathogens in oligomm12 mice reveals pathogen specific host and microbiota responses
topic Infectious diseases
mouse model
microbiota
Campylobacter jejuni
Listeria monocytogenes
Citrobacter rodentium
url https://www.tandfonline.com/doi/10.1080/19490976.2024.2447832
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