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Drumo, Rosanna (2016) Study of host-pathogen-microbiota interactions on a Salmonella enterica serovar Typhimurium piglet model. [Ph.D. thesis]

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Abstract (english)

Salmonella enterica serovar Typhimurium is a Gram negative gastrointestinal pathogen responsible for food poisoning worldwide. Upon entry into the host, Salmonella must overcome the robust line of defense provided by the innate immune system and by microbiota-mediated colonization resistance. It is a fascinating example of pathogen able not only to evade immune response, but also to exploit multiple aspects of it to colonize intestine. S. Typhimurium has evolved strategies allowing to thrive in the inflamed gut at the expense of the resident microbiota, taking advantage of the dramatic environmental conditions induced by inflammation. To understand the complex dynamics of interaction among S. Typhimurium-host-microbiota, is extremely important for the possible implications in the development strategies resulting in the reduction of colonization and/or frequency of salmonellosis. This thesis aimed at investigating the contribution of virulence, inflammation and microbiota to S. Typhimurium infection using piglet as model for salmonellosis. Firstly, we evaluated the capability of S. Typhimurium to exploit inflammation to promote its own colonization in vivo and in vitro. Our findings have shown that lipopolysaccharide (LPS) treatment-induced inflammation enhances the progression of S. Typhimurium, making the pathogen more capable to colonize at higher numbers both piglets and porcine enterocytes (IPEC-J2) and monocytes/macrophages cells. Secondly, we investigated the impact of Salmonella virulence on the porcine intestinal microbiota. To this end, we compared the effects on the microbiota induced by two different strains of Salmonella, a wild type strain and its isogenic attenuated mutant. We observed the existence of a link among virulence, inflammation and microbiota composition. S. Typhimurium wild type induces a strong inflammation which results in the reduction of some members of microbiota (i.e. SCFA-producing bacteria), normally involved in the maintaining of intestinal homeostasis and in the inhibition of pathogen growth. On the contrary, S. Typhimurium attenuated strain determines a milder inflammation and is correlated to an increase of protective species of microbiota which could shift the competition between the pathogen and microbiota in favour of the latter explaining the reduced ability of the attenuated strain to colonize host.
Finally, we focused on the physiological alterations of porcine cecum caused by wild type and attenuated S. Typhimurium strains. Our results suggest that host could adopt a “nutriprive mechanism” in which deprives environment of nutrients and energy sources, creating intestinal conditions that are detrimental for Salmonella growth. Moreover, the minor reduction of metabolic and energetic status of the host upon infection with Salmonella wild type in comparison with the attenuated strain could indicate that Salmonella wild type is more capable to oppose to the nutriprive mechanism.
Overall, by investigating the interaction dynamics among S. Typhimurium-host-microbiota, we have provided insights that the three factors are strictly interrelated and multiple aspects of each of them contribute to determine the outcome of infection.

Abstract (italian)

Salmonella enterica serovar Typhimurium è un batterio Gram negativo, patogeno enterico responsabile di una tossinfezione alimentare a diffusione mondiale. In seguito alla penetrazione nell’ospite, Salmonella deve superare la robusta linea di difesa rappresentata dal sistema dell’immunità innata e dalla resistenza alla colonizzazione mediata dal microbiota. Salmonella è un affascinante esempio di patogeno capace oltre che di eludere la risposta immunitaria, anche di sfruttarne i molteplici aspetti per colonizzare l’intestino. Ha sviluppato, infatti, strategie di virulenza che gli consentono di prosperare nell’intestino infiammato a discapito del microbiota residente, traendo vantaggio dalle condizioni ambientali fortemente alterate indotte dall’infiammazione.
Comprendere le complesse dinamiche di interazione tra S. Typhimurium-ospite-microbiota, è estremamente importante per le possibili implicazioni nello sviluppo di strategie vòlte a ridurre la colonizzazione e/o la frequenza della salmonellosi. Scopo di questa tesi è stato caratterizzare il contributo della virulenza, dell’infiammazione e del microbiota all’infezione da Salmonella, utilizzando il suino come modello sperimentale per la salmonellosi.
In primo luogo, abbiamo valutato l’abilità di S. Typhimurium di trarre vantaggio dall’infiammazione per favorire la propria colonizzazione, in vivo e in vitro. I nostri risultati hanno mostrato che l’infiammazione indotta dal trattamento con lipopolisaccaride (LPS) migliora la progressione dell’infezione, rendendo il patogeno capace di colonizzare con una carica più elevata sia i suinetti sia gli enterociti (IPEC-J2) e i monociti/macrofagi di origine suina.
Successivamente, abbiamo valutato l’impatto che la virulenza del patogeno ha sul microbiota intestinale suino. A tale scopo, abbiamo comparato gli effetti causati da due differenti ceppi di Salmonella, un ceppo wild type e il suo mutante isogenico attenuato, sulla composizione del microbiota. Abbiamo osservato l’esistenza di un collegamento diretto tra virulenza, infiammazione e composizione del microbiota. S. Typhimurium wild type induce una forte risposta infiammatoria che determina la riduzione di membri del microbiota (ad es. i batteri che producono SCFA) normalmente implicati nel mantenimento dell’omeostasi intestinale e nell’inibizione della crescita dei patogeni. Al contrario, il ceppo attenuato di S. Typhimurium causa una debole infiammazione che è invece associata ad un aumento di specie protettive del microbiota e ciò potrebbe spostare la competizione tra patogeno e microbiota in favore di quest’ ultimo, spiegando così la ridotta abilità di questo ceppo a colonizzare l’ospite.
Infine, la nostra attenzione si è focalizzata sulla risposta dell’ospite ed in particolare sulle modificazioni pato-fisiologiche che verificano a livello del cieco in seguito ad infezione con i due ceppi di S. Typhimurium, wild type e attenuato. I nostri risultati suggeriscono l’induzione di un “meccanismo nutriprivo” attraverso il quale l’ospite riduce la disponibilità di nutrienti e di fonti di energia per creare condizioni intestinali che risultano svantaggiose per la crescita di Salmonella. Inoltre, è stata osservata una minore riduzione dello stato metabolico ed energetico dell’ospite dopo infezione con S. Typhimurium wild type rispetto a quella indotta dal ceppo attenuato che potrebbe indicare una maggiore capacità del ceppo wild type a contrastare il meccanismo nutriprivo.
In conclusione, studiando le dinamiche di interazione tra S. Typhimurium-ospite-microbiota, abbiamo fornito ulteriori evidenze del fatto che i tre fattori sono strettamente correlati e che l’esito dell’infezione è il risultato del contributo fornito dai molti aspetti che li caratterizzano.

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EPrint type:Ph.D. thesis
Tutor:Pasquali, Paolo
Ph.D. course:Ciclo 28 > Scuole 28 > SCIENZE VETERINARIE
Data di deposito della tesi:22 July 2016
Anno di Pubblicazione:22 July 2016
Key Words:Salmonella Typhimurium, microbiota, inflammation, proteome, pig, infiammazione
Settori scientifico-disciplinari MIUR:Area 07 - Scienze agrarie e veterinarie > VET/05 Malattie infettive degli animali domestici
Struttura di riferimento:Dipartimenti > Dipartimento di Biomedicina Comparata ed Alimentazione
Codice ID:9672
Depositato il:03 Nov 2017 08:40
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