Salmonella T3SS-2 virulence enhances gut-luminal colonization by enabling chemotaxis-dependent exploitation of intestinal inflammation
Summary: Salmonella Typhimurium (S.Tm) utilizes the chemotaxis receptor Tsr to exploit gut inflammation. However, the characteristics of this exploitation and the mechanism(s) employed by the pathogen to circumvent antimicrobial effects of inflammation are poorly defined. Here, using different natur...
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| Format: | Article |
| Language: | English |
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Elsevier
2024-03-01
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| Series: | Cell Reports |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124724002535 |
| _version_ | 1797267813805588480 |
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| author | Ersin Gül Jemina Huuskonen Andrew Abi Younes Luca Maurer Ursina Enz Jakob Zimmermann Mikael E. Sellin Erik Bakkeren Wolf-Dietrich Hardt |
| author_facet | Ersin Gül Jemina Huuskonen Andrew Abi Younes Luca Maurer Ursina Enz Jakob Zimmermann Mikael E. Sellin Erik Bakkeren Wolf-Dietrich Hardt |
| author_sort | Ersin Gül |
| collection | DOAJ |
| description | Summary: Salmonella Typhimurium (S.Tm) utilizes the chemotaxis receptor Tsr to exploit gut inflammation. However, the characteristics of this exploitation and the mechanism(s) employed by the pathogen to circumvent antimicrobial effects of inflammation are poorly defined. Here, using different naturally occurring S.Tm strains (SL1344 and 14028) and competitive infection experiments, we demonstrate that type-three secretion system (T3SS)-2 virulence is indispensable for the beneficial effects of Tsr-directed chemotaxis. The removal of the 14028-specific prophage Gifsy3, encoding virulence effectors, results in the loss of the Tsr-mediated fitness advantage in that strain. Surprisingly, without T3SS-2 effector secretion, chemotaxis toward the gut epithelium using Tsr becomes disadvantageous for either strain. Our findings reveal that luminal neutrophils recruited as a result of NLRC4 inflammasome activation locally counteract S.Tm cells exploiting the byproducts of the host immune response. This work highlights a mechanism by which S.Tm exploitation of gut inflammation for colonization relies on the coordinated effects of chemotaxis and T3SS activities. |
| first_indexed | 2024-04-25T01:22:33Z |
| format | Article |
| id | doaj.art-764260268a954cffa30251e5f2f0072a |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-04-25T01:22:33Z |
| publishDate | 2024-03-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-764260268a954cffa30251e5f2f0072a2024-03-09T09:24:53ZengElsevierCell Reports2211-12472024-03-01433113925Salmonella T3SS-2 virulence enhances gut-luminal colonization by enabling chemotaxis-dependent exploitation of intestinal inflammationErsin Gül0Jemina Huuskonen1Andrew Abi Younes2Luca Maurer3Ursina Enz4Jakob Zimmermann5Mikael E. Sellin6Erik Bakkeren7Wolf-Dietrich Hardt8Institute of Microbiology, Department of Biology, ETH Zurich, Zurich, Switzerland; Corresponding authorInstitute 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 Visceral Surgery and Medicine, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland; Department for Biomedical Research, University of Bern, Bern, SwitzerlandDepartment of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden; Science for Life Laboratory, Uppsala, SwedenInstitute of Microbiology, Department of Biology, ETH Zurich, Zurich, SwitzerlandInstitute of Microbiology, Department of Biology, ETH Zurich, Zurich, Switzerland; Corresponding authorSummary: Salmonella Typhimurium (S.Tm) utilizes the chemotaxis receptor Tsr to exploit gut inflammation. However, the characteristics of this exploitation and the mechanism(s) employed by the pathogen to circumvent antimicrobial effects of inflammation are poorly defined. Here, using different naturally occurring S.Tm strains (SL1344 and 14028) and competitive infection experiments, we demonstrate that type-three secretion system (T3SS)-2 virulence is indispensable for the beneficial effects of Tsr-directed chemotaxis. The removal of the 14028-specific prophage Gifsy3, encoding virulence effectors, results in the loss of the Tsr-mediated fitness advantage in that strain. Surprisingly, without T3SS-2 effector secretion, chemotaxis toward the gut epithelium using Tsr becomes disadvantageous for either strain. Our findings reveal that luminal neutrophils recruited as a result of NLRC4 inflammasome activation locally counteract S.Tm cells exploiting the byproducts of the host immune response. This work highlights a mechanism by which S.Tm exploitation of gut inflammation for colonization relies on the coordinated effects of chemotaxis and T3SS activities.http://www.sciencedirect.com/science/article/pii/S2211124724002535CP: MicrobiologyCP: Immunology |
| spellingShingle | Ersin Gül Jemina Huuskonen Andrew Abi Younes Luca Maurer Ursina Enz Jakob Zimmermann Mikael E. Sellin Erik Bakkeren Wolf-Dietrich Hardt Salmonella T3SS-2 virulence enhances gut-luminal colonization by enabling chemotaxis-dependent exploitation of intestinal inflammation Cell Reports CP: Microbiology CP: Immunology |
| title | Salmonella T3SS-2 virulence enhances gut-luminal colonization by enabling chemotaxis-dependent exploitation of intestinal inflammation |
| title_full | Salmonella T3SS-2 virulence enhances gut-luminal colonization by enabling chemotaxis-dependent exploitation of intestinal inflammation |
| title_fullStr | Salmonella T3SS-2 virulence enhances gut-luminal colonization by enabling chemotaxis-dependent exploitation of intestinal inflammation |
| title_full_unstemmed | Salmonella T3SS-2 virulence enhances gut-luminal colonization by enabling chemotaxis-dependent exploitation of intestinal inflammation |
| title_short | Salmonella T3SS-2 virulence enhances gut-luminal colonization by enabling chemotaxis-dependent exploitation of intestinal inflammation |
| title_sort | salmonella t3ss 2 virulence enhances gut luminal colonization by enabling chemotaxis dependent exploitation of intestinal inflammation |
| topic | CP: Microbiology CP: Immunology |
| url | http://www.sciencedirect.com/science/article/pii/S2211124724002535 |
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