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

• Published in: Communications biology 2021-04, Vol.4 (1), p.498-15, Article 498
• Main Authors: Kirkwood, Mark, Vohra, Prerna, Bawn, Matt, Thilliez, Gaëtan, Pye, Hannah, Tanner, Jennifer, Chintoan-Uta, Cosmin, Branchu, Priscilla, Petrovska, Liljana, Dallman, Timothy, Hall, Neil, Stevens, Mark P., Kingsley, Robert A.
• Format: Article
• Language: English
• Subjects: 13; 13/106; 45; 45/22; 45/23; 45/70; 631/181/757; 631/326/421; 64; 64/60; Adaptation, Biological; Animal models; Animals; Bacterial Zoonoses; Bacterial Zoonoses - epidemiology; Bacterial Zoonoses - microbiology; Biology; Biomedical and Life Sciences; Colitis; Desiccation; Ecosystem; England; England - epidemiology; Epidemiology; Food safety; Foodborne diseases; Genomics; Intestine; Life Sciences; Livestock; Lymph nodes; Molecular evolution; Pathogenicity; Phylogeny; Salmonella; Salmonella Infections; Salmonella Infections - epidemiology; Salmonella Infections - microbiology; Salmonella Infections, Animal; Salmonella Infections, Animal - epidemiology; Salmonella Infections, Animal - microbiology; Salmonella Typhimurium; Salmonella typhimurium - pathogenicity; Salmonella typhimurium - physiology; Virulence; Wales; Wales - epidemiology; Zoonoses
• ISSN: 2399-3642; 2399-3642
• DOI: 10.1038/s42003-021-02013-4

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. Mark Kirkwood et al. take an epidemiological, genomic, phylogenetic, and experimental approach to assess the evolutionary origins and virulence of the U288 and ST34 isolates of Salmonella enterica in affecting livestock and potentially humans. Their results indicate that the molecular evolution of these isolates is associated with altered pathogenicity in pigs and reduced zoonotic potential of U288.