Ecological niche adaptation of Salmonella Typhimurium U288 is associated with altered pathogenicity and reduced zoonotic potential

Mark Kirkwood,Hannah Pye,Robert A Kingsley,Gaëtan Thilliez,Mark P Stevens,Timothy Dallman,Priscilla Branchu,Neil Hall,Prerna Vohra,Matt Bawn,Cosmin Chintoan-Uta,Liljana Petrovska,Jennifer Tanner

doi:10.1038/s42003-021-02013-4

Abstract

The emergence of new bacterial pathogens is a continuing challenge for agriculture and food safety. Salmonella Typhimurium is a major cause of foodborne illness worldwide, with pigs a major zoonotic reservoir. Two phylogenetically distinct variants, U288 and ST34, emerged in UK pigs around the same time but present different risk to food safety. Here we show using genomic epidemiology that ST34 accounts for over half of all S. Typhimurium infections in people while U288 less than 2%. That the U288 clade evolved in the recent past by acquiring AMR genes, indels in the virulence plasmid pU288-1, and accumulation of loss-of-function polymorphisms in coding sequences. U288 replicates more slowly and is more sensitive to desiccation than ST34 isolates and exhibited distinct pathogenicity in the murine model of colitis and in pigs. U288 infection was more disseminated in the lymph nodes while ST34 were recovered in greater numbers in the intestinal contents. These data are consistent with the evolution of S. Typhimurium U288 adaptation to pigs that may determine their reduced zoonotic potential.

Highlights

The emergence of new bacterial pathogens is a continuing challenge for agriculture and food safety
Typhimurium sequence type 34 (ST34) emerged around seven years later in UK pigs, and these two variants have co-existed in pig populations since
Emergence of ST34 coincided with a decrease in number of U288 isolates, both variants were present throughout this time

Summary

Introduction

The emergence of new bacterial pathogens is a continuing challenge for agriculture and food safety. Salmonella Typhimurium is a major cause of foodborne illness worldwide, with pigs a major zoonotic reservoir. U288 infection was more disseminated in the lymph nodes while ST34 were recovered in greater numbers in the intestinal contents. Non-typhoidal Salmonella alone has the greatest impact on health with 4 million disability adjusted life years lost, the greatest burden on human health among foodborne diseases.[5] Pigs are one of the major zoonotic reservoirs, with 10–20% of human salmonellosis in Europe attributable to them.[6,7] An understanding of the evolutionary processes leading to the emergence of new infectious diseases has the potential to improve pathogen diagnostics and surveillance, and guide policy and interventions aimed at decreasing the burden of human and animal infection

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Results

Conclusion