The immune response modulated by inoculation of commensal bacteria at birth impacts the gut microbiota and prevents Salmonella colonization
Super- and low-shedding phenomena have been observed in genetically homogeneous hosts infected by a single bacterial strain. To decipher the mechanisms underlying these phenotypes, we conducted an experiment with chicks infected with Salmonella Enteritidis in a non-sterile isolator, which prevents b...
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| Language: | English |
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Taylor & Francis Group
2025-12-01
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| Series: | Gut Microbes |
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| Online Access: | https://www.tandfonline.com/doi/10.1080/19490976.2025.2474151 |
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| author | Florent Kempf Rosanna Drumo Anne Marie Chaussé Pierrette Menanteau Tereza Kubasova Sylvie Roche Anne Christine Lalmanach Rodrigo Guabiraba Thierry Chaumeil Guillaume Larivière-Gauthier Ignacio Caballero-Posadas Béatrice Laroche Ivan Rychlík Isabelle Virlogeux-Payant Philippe Velge |
| author_facet | Florent Kempf Rosanna Drumo Anne Marie Chaussé Pierrette Menanteau Tereza Kubasova Sylvie Roche Anne Christine Lalmanach Rodrigo Guabiraba Thierry Chaumeil Guillaume Larivière-Gauthier Ignacio Caballero-Posadas Béatrice Laroche Ivan Rychlík Isabelle Virlogeux-Payant Philippe Velge |
| author_sort | Florent Kempf |
| collection | DOAJ |
| description | Super- and low-shedding phenomena have been observed in genetically homogeneous hosts infected by a single bacterial strain. To decipher the mechanisms underlying these phenotypes, we conducted an experiment with chicks infected with Salmonella Enteritidis in a non-sterile isolator, which prevents bacterial transmission between animals while allowing the development of the gut microbiota. We investigated the impact of four commensal bacteria called Mix4, inoculated at hatching, on chicken systemic immune response and intestinal microbiota composition and functions, before and after Salmonella infection. Our results revealed that these phenotypes were not linked to changes in cell invasion capacity of bacteria during infection. Mix4 inoculation had both short- and long-term effects on immune response and microbiota and promoted the low-shedder phenotype. Kinetic analysis revealed that Mix4 activated immune response from day 4, which modified the microbiota on day 6. This change promotes a more fermentative microbiota, using the aromatic compounds degradation pathway, which inhibited Salmonella colonization by day 11 and beyond. In contrast, control animals exhibited a delayed TNF-driven pro-inflammatory response and developed a microbiota using anaerobic respiration, which facilitates Salmonella colonization and growth. This strategy offers promising opportunities to strengthen the barrier effect against Salmonella and possibly other pathogens. |
| format | Article |
| id | doaj-art-2c616d0abc0d4233ab5aa72c08b6378e |
| institution | DOAJ |
| issn | 1949-0976 1949-0984 |
| language | English |
| publishDate | 2025-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Gut Microbes |
| spelling | doaj-art-2c616d0abc0d4233ab5aa72c08b6378e2025-08-20T03:12:47ZengTaylor & Francis GroupGut Microbes1949-09761949-09842025-12-0117110.1080/19490976.2025.2474151The immune response modulated by inoculation of commensal bacteria at birth impacts the gut microbiota and prevents Salmonella colonizationFlorent Kempf0Rosanna Drumo1Anne Marie Chaussé2Pierrette Menanteau3Tereza Kubasova4Sylvie Roche5Anne Christine Lalmanach6Rodrigo Guabiraba7Thierry Chaumeil8Guillaume Larivière-Gauthier9Ignacio Caballero-Posadas10Béatrice Laroche11Ivan Rychlík12Isabelle Virlogeux-Payant13Philippe Velge14ISP, INRAE, Université François Rabelais de Tours, Nouzilly, FranceISP, INRAE, Université François Rabelais de Tours, Nouzilly, FranceISP, INRAE, Université François Rabelais de Tours, Nouzilly, FranceISP, INRAE, Université François Rabelais de Tours, Nouzilly, FranceDepartment of Microbiology and antimicrobial resistance, Veterinary Research Institute, Brno, Czech RepublicISP, INRAE, Université François Rabelais de Tours, Nouzilly, FranceISP, INRAE, Université François Rabelais de Tours, Nouzilly, FranceISP, INRAE, Université François Rabelais de Tours, Nouzilly, FrancePlate-Forme d’Infectiologie Expérimentale, INRAE, Nouzilly, FranceISP, INRAE, Université François Rabelais de Tours, Nouzilly, FranceISP, INRAE, Université François Rabelais de Tours, Nouzilly, FranceMaIAGE, INRAE, Jouy-en-Josas, FranceDepartment of Microbiology and antimicrobial resistance, Veterinary Research Institute, Brno, Czech RepublicISP, INRAE, Université François Rabelais de Tours, Nouzilly, FranceISP, INRAE, Université François Rabelais de Tours, Nouzilly, FranceSuper- and low-shedding phenomena have been observed in genetically homogeneous hosts infected by a single bacterial strain. To decipher the mechanisms underlying these phenotypes, we conducted an experiment with chicks infected with Salmonella Enteritidis in a non-sterile isolator, which prevents bacterial transmission between animals while allowing the development of the gut microbiota. We investigated the impact of four commensal bacteria called Mix4, inoculated at hatching, on chicken systemic immune response and intestinal microbiota composition and functions, before and after Salmonella infection. Our results revealed that these phenotypes were not linked to changes in cell invasion capacity of bacteria during infection. Mix4 inoculation had both short- and long-term effects on immune response and microbiota and promoted the low-shedder phenotype. Kinetic analysis revealed that Mix4 activated immune response from day 4, which modified the microbiota on day 6. This change promotes a more fermentative microbiota, using the aromatic compounds degradation pathway, which inhibited Salmonella colonization by day 11 and beyond. In contrast, control animals exhibited a delayed TNF-driven pro-inflammatory response and developed a microbiota using anaerobic respiration, which facilitates Salmonella colonization and growth. This strategy offers promising opportunities to strengthen the barrier effect against Salmonella and possibly other pathogens.https://www.tandfonline.com/doi/10.1080/19490976.2025.2474151Salmonellacarrier-stateexcretionchickensuper-shedderimmune response |
| spellingShingle | Florent Kempf Rosanna Drumo Anne Marie Chaussé Pierrette Menanteau Tereza Kubasova Sylvie Roche Anne Christine Lalmanach Rodrigo Guabiraba Thierry Chaumeil Guillaume Larivière-Gauthier Ignacio Caballero-Posadas Béatrice Laroche Ivan Rychlík Isabelle Virlogeux-Payant Philippe Velge The immune response modulated by inoculation of commensal bacteria at birth impacts the gut microbiota and prevents Salmonella colonization Gut Microbes Salmonella carrier-state excretion chicken super-shedder immune response |
| title | The immune response modulated by inoculation of commensal bacteria at birth impacts the gut microbiota and prevents Salmonella colonization |
| title_full | The immune response modulated by inoculation of commensal bacteria at birth impacts the gut microbiota and prevents Salmonella colonization |
| title_fullStr | The immune response modulated by inoculation of commensal bacteria at birth impacts the gut microbiota and prevents Salmonella colonization |
| title_full_unstemmed | The immune response modulated by inoculation of commensal bacteria at birth impacts the gut microbiota and prevents Salmonella colonization |
| title_short | The immune response modulated by inoculation of commensal bacteria at birth impacts the gut microbiota and prevents Salmonella colonization |
| title_sort | immune response modulated by inoculation of commensal bacteria at birth impacts the gut microbiota and prevents salmonella colonization |
| topic | Salmonella carrier-state excretion chicken super-shedder immune response |
| url | https://www.tandfonline.com/doi/10.1080/19490976.2025.2474151 |
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