Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota.

2.50
Hdl Handle:
http://hdl.handle.net/10033/19178
Title:
Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota.
Authors:
Stecher, Bärbel; Robbiani, Riccardo; Walker, Alan W; Westendorf, Astrid M; Barthel, Manja; Kremer, Marcus; Chaffron, Samuel; Macpherson, Andrew J; Buer, Jan; Parkhill, Julian; Dougan, Gordon; von Mering, Christian; Hardt, Wolf-Dietrich
Abstract:
Most mucosal surfaces of the mammalian body are colonized by microbial communities ("microbiota"). A high density of commensal microbiota inhabits the intestine and shields from infection ("colonization resistance"). The virulence strategies allowing enteropathogenic bacteria to successfully compete with the microbiota and overcome colonization resistance are poorly understood. Here, we investigated manipulation of the intestinal microbiota by the enteropathogenic bacterium Salmonella enterica subspecies 1 serovar Typhimurium (S. Tm) in a mouse colitis model: we found that inflammatory host responses induced by S. Tm changed microbiota composition and suppressed its growth. In contrast to wild-type S. Tm, an avirulent invGsseD mutant failing to trigger colitis was outcompeted by the microbiota. This competitive defect was reverted if inflammation was provided concomitantly by mixed infection with wild-type S. Tm or in mice (IL10(-/-), VILLIN-HA(CL4-CD8)) with inflammatory bowel disease. Thus, inflammation is necessary and sufficient for overcoming colonization resistance. This reveals a new concept in infectious disease: in contrast to current thinking, inflammation is not always detrimental for the pathogen. Triggering the host's immune defence can shift the balance between the protective microbiota and the pathogen in favour of the pathogen.
Affiliation:
Institute of Microbiology, Swiss Institute of Technology Zurich, Zurich, Switzerland.
Citation:
Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. 2007, 5 (10):2177-89 PLoS Biol.
Journal:
PLoS biology
Issue Date:
Oct-2007
URI:
http://hdl.handle.net/10033/19178
DOI:
10.1371/journal.pbio.0050244
PubMed ID:
17760501
Additional Links:
http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pubmed&pubmedid=17760501
Type:
Article
Language:
en
ISSN:
1545-7885
Appears in Collections:
Publications of RG Mucosal Immunity (MI)

Full metadata record

DC FieldValue Language
dc.contributor.authorStecher, Bärbel-
dc.contributor.authorRobbiani, Riccardo-
dc.contributor.authorWalker, Alan W-
dc.contributor.authorWestendorf, Astrid M-
dc.contributor.authorBarthel, Manja-
dc.contributor.authorKremer, Marcus-
dc.contributor.authorChaffron, Samuel-
dc.contributor.authorMacpherson, Andrew J-
dc.contributor.authorBuer, Jan-
dc.contributor.authorParkhill, Julian-
dc.contributor.authorDougan, Gordon-
dc.contributor.authorvon Mering, Christian-
dc.contributor.authorHardt, Wolf-Dietrich-
dc.date.accessioned2008-02-26T14:00:54Z-
dc.date.available2008-02-26T14:00:54Z-
dc.date.issued2007-10-
dc.identifier.citationSalmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. 2007, 5 (10):2177-89 PLoS Biol.en
dc.identifier.issn1545-7885-
dc.identifier.pmid17760501-
dc.identifier.doi10.1371/journal.pbio.0050244-
dc.identifier.urihttp://hdl.handle.net/10033/19178-
dc.description.abstractMost mucosal surfaces of the mammalian body are colonized by microbial communities ("microbiota"). A high density of commensal microbiota inhabits the intestine and shields from infection ("colonization resistance"). The virulence strategies allowing enteropathogenic bacteria to successfully compete with the microbiota and overcome colonization resistance are poorly understood. Here, we investigated manipulation of the intestinal microbiota by the enteropathogenic bacterium Salmonella enterica subspecies 1 serovar Typhimurium (S. Tm) in a mouse colitis model: we found that inflammatory host responses induced by S. Tm changed microbiota composition and suppressed its growth. In contrast to wild-type S. Tm, an avirulent invGsseD mutant failing to trigger colitis was outcompeted by the microbiota. This competitive defect was reverted if inflammation was provided concomitantly by mixed infection with wild-type S. Tm or in mice (IL10(-/-), VILLIN-HA(CL4-CD8)) with inflammatory bowel disease. Thus, inflammation is necessary and sufficient for overcoming colonization resistance. This reveals a new concept in infectious disease: in contrast to current thinking, inflammation is not always detrimental for the pathogen. Triggering the host's immune defence can shift the balance between the protective microbiota and the pathogen in favour of the pathogen.en
dc.language.isoenen
dc.relation.urlhttp://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pubmed&pubmedid=17760501en
dc.subject.meshAnimalsen
dc.subject.meshBacteriaen
dc.subject.meshColitisen
dc.subject.meshFemaleen
dc.subject.meshGenotypeen
dc.subject.meshIn Situ Hybridization, Fluorescenceen
dc.subject.meshIntestinesen
dc.subject.meshMaleen
dc.subject.meshMiceen
dc.subject.meshMice, Inbred C3Hen
dc.subject.meshMice, Inbred C57BLen
dc.subject.meshMice, Inbred Strainsen
dc.subject.meshMicroscopy, Fluorescenceen
dc.subject.meshModels, Animalen
dc.subject.meshMolecular Sequence Dataen
dc.subject.meshMutationen
dc.subject.meshPhylogenyen
dc.subject.meshRNA, Ribosomal, 16Sen
dc.subject.meshSalmonella Infectionsen
dc.subject.meshSalmonella typhimuriumen
dc.subject.meshSequence Analysis, DNAen
dc.titleSalmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota.en
dc.typeArticleen
dc.contributor.departmentInstitute of Microbiology, Swiss Institute of Technology Zurich, Zurich, Switzerland.en
dc.identifier.journalPLoS biologyen

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