Salmonella enterica Serovar Typhimurium Exploits Inflammation to Modify Swine Intestinal Microbiota.

Rosanna Drumo,Valerio Napolioni,Giovanni Pezzotti,Barbara Chirullo,Matteo Picciolini,Gianfranco Gabai,Andrea Battistoni,Silvia Pavone,Elisabetta Manuali,Nicola Martinelli,Michela Tarantino,Serena Ammendola,Paola Petrucci,Jessica Ruggeri,Claudia Pistoia,Michele Pesciaroli,Livia Moscati,Paolo Pasquali,G L Alborali ,Chiara Francesca Magistrali

doi:10.3389/fcimb.2015.00106

Abstract

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.

Highlights

Nontyphoidal salmonellae (NTS) as Salmonella enterica serovar Typhimurium are a leading cause of acute food-borne zoonoses worldwide being responsible for hundreds of millions of cases of gastroenteritis and bacteremia annually (Hohmann, 2001)
Piglets infected with STM znuABC and STMwt had a transient increase in body temperature at 1 dpi compared with naïve controls
To further assess the inflammatory response induced by STMwt and STM znuABC, piglets were bled at different time points and haptoglobin, C-reactive Protein (CRP), IL1-α, and TNF-α levels were measured in sera

Summary

Introduction

Nontyphoidal salmonellae (NTS) as Salmonella enterica serovar Typhimurium are a leading cause of acute food-borne zoonoses worldwide being responsible for hundreds of millions of cases of gastroenteritis and bacteremia annually (Hohmann, 2001). Microbiota contributes to the digestion of dietary substances and to the synthesis of essential food supplements such as vitamins, and to the development or maintenance of the mucosal immune system (Littman and Pamer, 2011) It acts as a barrier against invading bacteria both physically, blocking pathogen access to the epithelial layer, and by outcompeting for nutrients reducing the survival and invasiveness of enteric pathogens (Hallstrom and McCormick, 2011; Sassone-Corsi and Raffatellu, 2015). It has been shown that Salmonella can alter the normal composition of the gut microbiota, and this influence is associated with Salmonella virulence factors that induce inflammatory mucosal host responses (Barman et al, 2008). Salmonella could overcome colonization resistance through the reduction of microbiota members normally involved in the intestinal homeostasis and in the inhibition of pathogen growth

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Results

Conclusion