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Salmonella enterica Serovar Typhimurium Exploits Inflammation to Modify Swine Intestinal Microbiota

Salmonella enterica serovar Typhimurium is an important zoonotic gastrointestinal pathogen responsible for foodborne disease worldwide. It is a successful enteric pathogen because it has developed virulence strategies allowing it to survive in a highly inflamed intestinal environment exploiting infl...

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Autores principales: Drumo, Rosanna, Pesciaroli, Michele, Ruggeri, Jessica, Tarantino, Michela, Chirullo, Barbara, Pistoia, Claudia, Petrucci, Paola, Martinelli, Nicola, Moscati, Livia, Manuali, Elisabetta, Pavone, Silvia, Picciolini, Matteo, Ammendola, Serena, Gabai, Gianfranco, Battistoni, Andrea, Pezzotti, Giovanni, Alborali, Giovanni L., Napolioni, Valerio, Pasquali, Paolo, Magistrali, Chiara F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4722131/
https://www.ncbi.nlm.nih.gov/pubmed/26835435
http://dx.doi.org/10.3389/fcimb.2015.00106
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author Drumo, Rosanna
Pesciaroli, Michele
Ruggeri, Jessica
Tarantino, Michela
Chirullo, Barbara
Pistoia, Claudia
Petrucci, Paola
Martinelli, Nicola
Moscati, Livia
Manuali, Elisabetta
Pavone, Silvia
Picciolini, Matteo
Ammendola, Serena
Gabai, Gianfranco
Battistoni, Andrea
Pezzotti, Giovanni
Alborali, Giovanni L.
Napolioni, Valerio
Pasquali, Paolo
Magistrali, Chiara F.
author_facet Drumo, Rosanna
Pesciaroli, Michele
Ruggeri, Jessica
Tarantino, Michela
Chirullo, Barbara
Pistoia, Claudia
Petrucci, Paola
Martinelli, Nicola
Moscati, Livia
Manuali, Elisabetta
Pavone, Silvia
Picciolini, Matteo
Ammendola, Serena
Gabai, Gianfranco
Battistoni, Andrea
Pezzotti, Giovanni
Alborali, Giovanni L.
Napolioni, Valerio
Pasquali, Paolo
Magistrali, Chiara F.
author_sort Drumo, Rosanna
collection PubMed
description Salmonella enterica serovar Typhimurium is an important zoonotic gastrointestinal pathogen responsible for foodborne disease worldwide. It is a successful enteric pathogen because it has developed virulence strategies allowing it to survive in a highly inflamed intestinal environment exploiting inflammation to overcome colonization resistance provided by intestinal microbiota. In this study, we used piglets featuring an intact microbiota, which naturally develop gastroenteritis, as model for salmonellosis. We compared the effects on the intestinal microbiota induced by a wild type and an attenuated S. Typhimurium in order to evaluate whether the modifications are correlated with the virulence of the strain. This study showed that Salmonella alters microbiota in a virulence-dependent manner. We found that the wild type S. Typhimurium induced inflammation and a reduction of specific protecting microbiota species (SCFA-producing bacteria) normally involved in providing a barrier against pathogens. Both these effects could contribute to impair colonization resistance, increasing the host susceptibility to wild type S. Typhimurium colonization. In contrast, the attenuated S. Typhimurium, which is characterized by a reduced ability to colonize the intestine, and by a very mild inflammatory response, was unable to successfully sustain competition with the microbiota.
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spelling pubmed-47221312016-01-29 Salmonella enterica Serovar Typhimurium Exploits Inflammation to Modify Swine Intestinal Microbiota Drumo, Rosanna Pesciaroli, Michele Ruggeri, Jessica Tarantino, Michela Chirullo, Barbara Pistoia, Claudia Petrucci, Paola Martinelli, Nicola Moscati, Livia Manuali, Elisabetta Pavone, Silvia Picciolini, Matteo Ammendola, Serena Gabai, Gianfranco Battistoni, Andrea Pezzotti, Giovanni Alborali, Giovanni L. Napolioni, Valerio Pasquali, Paolo Magistrali, Chiara F. Front Cell Infect Microbiol Microbiology Salmonella enterica serovar Typhimurium is an important zoonotic gastrointestinal pathogen responsible for foodborne disease worldwide. It is a successful enteric pathogen because it has developed virulence strategies allowing it to survive in a highly inflamed intestinal environment exploiting inflammation to overcome colonization resistance provided by intestinal microbiota. In this study, we used piglets featuring an intact microbiota, which naturally develop gastroenteritis, as model for salmonellosis. We compared the effects on the intestinal microbiota induced by a wild type and an attenuated S. Typhimurium in order to evaluate whether the modifications are correlated with the virulence of the strain. This study showed that Salmonella alters microbiota in a virulence-dependent manner. We found that the wild type S. Typhimurium induced inflammation and a reduction of specific protecting microbiota species (SCFA-producing bacteria) normally involved in providing a barrier against pathogens. Both these effects could contribute to impair colonization resistance, increasing the host susceptibility to wild type S. Typhimurium colonization. In contrast, the attenuated S. Typhimurium, which is characterized by a reduced ability to colonize the intestine, and by a very mild inflammatory response, was unable to successfully sustain competition with the microbiota. Frontiers Media S.A. 2016-01-22 /pmc/articles/PMC4722131/ /pubmed/26835435 http://dx.doi.org/10.3389/fcimb.2015.00106 Text en Copyright © 2016 Drumo, Pesciaroli, Ruggeri, Tarantino, Chirullo, Pistoia, Petrucci, Martinelli, Moscati, Manuali, Pavone, Picciolini, Ammendola, Gabai, Battistoni, Pezzotti, Alborali, Napolioni, Pasquali and Magistrali. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Drumo, Rosanna
Pesciaroli, Michele
Ruggeri, Jessica
Tarantino, Michela
Chirullo, Barbara
Pistoia, Claudia
Petrucci, Paola
Martinelli, Nicola
Moscati, Livia
Manuali, Elisabetta
Pavone, Silvia
Picciolini, Matteo
Ammendola, Serena
Gabai, Gianfranco
Battistoni, Andrea
Pezzotti, Giovanni
Alborali, Giovanni L.
Napolioni, Valerio
Pasquali, Paolo
Magistrali, Chiara F.
Salmonella enterica Serovar Typhimurium Exploits Inflammation to Modify Swine Intestinal Microbiota
title Salmonella enterica Serovar Typhimurium Exploits Inflammation to Modify Swine Intestinal Microbiota
title_full Salmonella enterica Serovar Typhimurium Exploits Inflammation to Modify Swine Intestinal Microbiota
title_fullStr Salmonella enterica Serovar Typhimurium Exploits Inflammation to Modify Swine Intestinal Microbiota
title_full_unstemmed Salmonella enterica Serovar Typhimurium Exploits Inflammation to Modify Swine Intestinal Microbiota
title_short Salmonella enterica Serovar Typhimurium Exploits Inflammation to Modify Swine Intestinal Microbiota
title_sort salmonella enterica serovar typhimurium exploits inflammation to modify swine intestinal microbiota
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4722131/
https://www.ncbi.nlm.nih.gov/pubmed/26835435
http://dx.doi.org/10.3389/fcimb.2015.00106
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