Inflammatory Responses Induced by the Monophasic Variant of Salmonella Typhimurium in Pigs Play a Role in the High Shedder Phenotype and Fecal Microbiota Composition
ABSTRACT Pigs infected with Salmonella may excrete large amounts of Salmonella, increasing the risk of spread of this pathogen in the food chain. Identifying Salmonella high shedder pigs is therefore required to mitigate this risk. We analyzed immune-associated markers and composition of the gut mic...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-02-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.00852-22 |
| _version_ | 1797895815622033408 |
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| author | Florent Kempf Guido Cordoni Anne-Marie Chaussé Rosanna Drumo Helen Brown Daniel L. Horton Frédéric Paboeuf Martine Denis Philippe Velge Roberto La Ragione Annaëlle Kerouanton |
| author_facet | Florent Kempf Guido Cordoni Anne-Marie Chaussé Rosanna Drumo Helen Brown Daniel L. Horton Frédéric Paboeuf Martine Denis Philippe Velge Roberto La Ragione Annaëlle Kerouanton |
| author_sort | Florent Kempf |
| collection | DOAJ |
| description | ABSTRACT Pigs infected with Salmonella may excrete large amounts of Salmonella, increasing the risk of spread of this pathogen in the food chain. Identifying Salmonella high shedder pigs is therefore required to mitigate this risk. We analyzed immune-associated markers and composition of the gut microbiota in specific-pathogen-free pigs presenting different shedding levels after an oral infection with Salmonella. Immune response was studied through total blood cell counts, production of anti-Salmonella antibodies and cytokines, and gene expression quantification. Total Salmonella shedding for each pig was estimated and hierarchical clustering was used to cluster pigs into high, intermediate, and low shedders. Gut microbiota compositions were assessed using 16S rRNA microbial community profiling. Comparisons were made between control and inoculated pigs, then between high and low shedders pigs. Prior to infection, high shedders had similar immunological profiles compared to low shedders. As soon as 1 day postinoculation (dpi), significant differences on the cytokine production level and on the expression level of several host genes related to a proinflammatory response were observed between high and low shedders. Infection with Salmonella induced an early and profound remodeling of the immune response in all pigs, but the intensity of the response was stronger in high shedders. In contrast, low shedders seroconverted earlier than high shedders. Just after induction of the proinflammatory response (at 2 dpi), some taxa of the fecal microbiota were specific to the shedding phenotypes. This was related to the enrichment of several functional pathways related to anaerobic respiration in high shedders. In conclusion, our data show that the immune response to Salmonella modifies the fecal microbiota and subsequently could be responsible for shedding phenotypes. Influencing the gut microbiota and reducing intestinal inflammation could be a strategy for preventing Salmonella high shedding in livestock. IMPORTANCE Salmonellosis remains the most frequent human foodborne zoonosis after campylobacteriosis and pork meat is considered one of the major sources of human foodborne infections. At the farm, host heterogeneity in pig infection is problematic. High Salmonella shedders contribute more significantly to the spread of this foodborne pathogen in the food chain. The identification of predictive biomarkers for high shedders could help to control Salmonella in pigs. The purpose of the present study was to investigate why some pigs become super shedders and others low shedders. We thus investigated the differences in the fecal microbial composition and the immune response in orally infected pigs presenting different Salmonella shedding patterns. Our data show that the proinflammatory response induced by S. Typhimurium at 1 dpi could be responsible for the modification of the fecal microbiota composition and functions observed mainly at 2 and 3 dpi and to the low and super shedder phenotypes. |
| first_indexed | 2024-04-10T07:31:43Z |
| format | Article |
| id | doaj.art-0cd67d4631e5403f8a7b95929447b663 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-04-10T07:31:43Z |
| publishDate | 2023-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-0cd67d4631e5403f8a7b95929447b6632023-02-23T14:01:37ZengAmerican Society for MicrobiologymSystems2379-50772023-02-018110.1128/msystems.00852-22Inflammatory Responses Induced by the Monophasic Variant of Salmonella Typhimurium in Pigs Play a Role in the High Shedder Phenotype and Fecal Microbiota CompositionFlorent Kempf0Guido Cordoni1Anne-Marie Chaussé2Rosanna Drumo3Helen Brown4Daniel L. Horton5Frédéric Paboeuf6Martine Denis7Philippe Velge8Roberto La Ragione9Annaëlle Kerouanton10ISP, INRAE, Université François Rabelais de Tours, Nouzilly, FranceDepartment of Pathology and Infectious Diseases, School of Veterinary Medicine (VSM), University of Surrey, Guildford, Surrey, UKISP, INRAE, Université François Rabelais de Tours, Nouzilly, FranceISP, INRAE, Université François Rabelais de Tours, Nouzilly, FranceDepartment of Pathology and Infectious Diseases, School of Veterinary Medicine (VSM), University of Surrey, Guildford, Surrey, UKDepartment of Pathology and Infectious Diseases, School of Veterinary Medicine (VSM), University of Surrey, Guildford, Surrey, UKANSES, SPF Pig Production and Experimental Unit, Ploufragan, FranceANSES, Hygiene and Quality of Poultry and Pig Products Unit, Ploufragan, FranceISP, INRAE, Université François Rabelais de Tours, Nouzilly, FranceDepartment of Pathology and Infectious Diseases, School of Veterinary Medicine (VSM), University of Surrey, Guildford, Surrey, UKANSES, Hygiene and Quality of Poultry and Pig Products Unit, Ploufragan, FranceABSTRACT Pigs infected with Salmonella may excrete large amounts of Salmonella, increasing the risk of spread of this pathogen in the food chain. Identifying Salmonella high shedder pigs is therefore required to mitigate this risk. We analyzed immune-associated markers and composition of the gut microbiota in specific-pathogen-free pigs presenting different shedding levels after an oral infection with Salmonella. Immune response was studied through total blood cell counts, production of anti-Salmonella antibodies and cytokines, and gene expression quantification. Total Salmonella shedding for each pig was estimated and hierarchical clustering was used to cluster pigs into high, intermediate, and low shedders. Gut microbiota compositions were assessed using 16S rRNA microbial community profiling. Comparisons were made between control and inoculated pigs, then between high and low shedders pigs. Prior to infection, high shedders had similar immunological profiles compared to low shedders. As soon as 1 day postinoculation (dpi), significant differences on the cytokine production level and on the expression level of several host genes related to a proinflammatory response were observed between high and low shedders. Infection with Salmonella induced an early and profound remodeling of the immune response in all pigs, but the intensity of the response was stronger in high shedders. In contrast, low shedders seroconverted earlier than high shedders. Just after induction of the proinflammatory response (at 2 dpi), some taxa of the fecal microbiota were specific to the shedding phenotypes. This was related to the enrichment of several functional pathways related to anaerobic respiration in high shedders. In conclusion, our data show that the immune response to Salmonella modifies the fecal microbiota and subsequently could be responsible for shedding phenotypes. Influencing the gut microbiota and reducing intestinal inflammation could be a strategy for preventing Salmonella high shedding in livestock. IMPORTANCE Salmonellosis remains the most frequent human foodborne zoonosis after campylobacteriosis and pork meat is considered one of the major sources of human foodborne infections. At the farm, host heterogeneity in pig infection is problematic. High Salmonella shedders contribute more significantly to the spread of this foodborne pathogen in the food chain. The identification of predictive biomarkers for high shedders could help to control Salmonella in pigs. The purpose of the present study was to investigate why some pigs become super shedders and others low shedders. We thus investigated the differences in the fecal microbial composition and the immune response in orally infected pigs presenting different Salmonella shedding patterns. Our data show that the proinflammatory response induced by S. Typhimurium at 1 dpi could be responsible for the modification of the fecal microbiota composition and functions observed mainly at 2 and 3 dpi and to the low and super shedder phenotypes.https://journals.asm.org/doi/10.1128/msystems.00852-22Salmonellapiggut microbiotaimmunityhigh shedderinflammation |
| spellingShingle | Florent Kempf Guido Cordoni Anne-Marie Chaussé Rosanna Drumo Helen Brown Daniel L. Horton Frédéric Paboeuf Martine Denis Philippe Velge Roberto La Ragione Annaëlle Kerouanton Inflammatory Responses Induced by the Monophasic Variant of Salmonella Typhimurium in Pigs Play a Role in the High Shedder Phenotype and Fecal Microbiota Composition mSystems Salmonella pig gut microbiota immunity high shedder inflammation |
| title | Inflammatory Responses Induced by the Monophasic Variant of Salmonella Typhimurium in Pigs Play a Role in the High Shedder Phenotype and Fecal Microbiota Composition |
| title_full | Inflammatory Responses Induced by the Monophasic Variant of Salmonella Typhimurium in Pigs Play a Role in the High Shedder Phenotype and Fecal Microbiota Composition |
| title_fullStr | Inflammatory Responses Induced by the Monophasic Variant of Salmonella Typhimurium in Pigs Play a Role in the High Shedder Phenotype and Fecal Microbiota Composition |
| title_full_unstemmed | Inflammatory Responses Induced by the Monophasic Variant of Salmonella Typhimurium in Pigs Play a Role in the High Shedder Phenotype and Fecal Microbiota Composition |
| title_short | Inflammatory Responses Induced by the Monophasic Variant of Salmonella Typhimurium in Pigs Play a Role in the High Shedder Phenotype and Fecal Microbiota Composition |
| title_sort | inflammatory responses induced by the monophasic variant of salmonella typhimurium in pigs play a role in the high shedder phenotype and fecal microbiota composition |
| topic | Salmonella pig gut microbiota immunity high shedder inflammation |
| url | https://journals.asm.org/doi/10.1128/msystems.00852-22 |
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