Genomic population structure associated with repeated escape of Salmonella enterica ATCC14028s from the laboratory into nature

Authors: ACHTMAN, MARK - University Of Warwick; VAN DEN BROECK, FREDERIK - University Of Leuven; COOPER, KERRY - University Of Arizona; LEMEY, PHILIPPE - University Of Leuven; Parker, Craig; ZHOU, ZHEMIN - University Of Warwick

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/10/2021
Publication Date: 9/27/2021
Citation: Achtman, M., Van den Broeck, F., Cooper, K.K., Lemey, P., Parker, C.T., Zhou, Z. 2021. Genomic population structure associated with repeated escape of Salmonella enterica ATCC14028s from the laboratory into nature. PLoS Genetics. 17(9). Article e1009820. https://doi.org/10.1371/journal.pgen.1009820.
DOI: https://doi.org/10.1371/journal.pgen.1009820

Interpretive Summary: The foodborne pathogen Salmonella enterica serovar Typhimurium is a worldwide leading cause of bacterial gastroenteritis. Salmonella enterica serovar Typhimurium strain ATCC14028s is commercially available from multiple national type culture collections and has been widely used since 1960 for quality control and laboratory evolution. ATCC14028s has been involved in multiple cross-contaminations in the laboratory, and also caused multiple laboratory and bioterrorism infections. Salmonella core gene multilocus sequence typing (cgMLST) consists of a sequence-specific allelic designation for each of 3002 core genes, and a distinct sequence type integer for each unique combination of 3002 allelic integers a core genome sequence type (cgST). Once assigned, cgSTs are assigned to multiple levels of single linkage hierarchical clustering (HierCC) based on their pairwise patristic differences in allelic contents According to hierarchical clustering of 3002 core gene sequences, ATCC14028s belongs to HierCC cluster HC20_373 in which most internal branch lengths are only one to three SNPs long. Many natural Typhimurium isolates from humans, domesticated animals and the environment also belong to HC20_373, and their core genomes are almost indistinguishable from those of the laboratory strains. These natural isolates have infected humans in Ireland and Taiwan for decades, and are common in the British Isles as well as the Americas. Epidemiological features indicate that the natural isolates do not represent recent contamination by the laboratory strain, and 10% carry plasmids or bacteriophages which have been acquired in nature by horizontal gene transfer from unrelated bacteria. We propose that ATCC14028s has repeatedly escaped from the laboratory environment into nature via laboratory accidents or infections, but the escaped micro-lineages have only a limited life span. As a result, there is a genetic gap separating HC20_373 from its closest natural relatives, representing a divergence between them in 1890 followed by repeated extinction events of escaped HC20_373.

Technical Abstract: Salmonella enterica serovar Typhimurium strain ATCC14028s is commercially available from multiple national type culture collections, and has been widely used since 1960 for quality control and laboratory evolution. ATCC14028s has been involved in multiple cross-contaminations in the laboratory, and also caused multiple laboratory and bioterrorism infections. According to hierarchical clustering of 3002 core gene sequences, ATCC14028s belongs to HierCC cluster HC20_373 in which most internal branch lengths are only one to three SNPs long. Many natural Typhimurium isolates from humans, domesticated animals and the environment also belong to HC20_373, and their core genomes are almost indistinguishable from those of the laboratory strains. These natural isolates have infected humans in Ireland and Taiwan for decades, and are common in the British Isles as well as the Americas. Epidemiological features indicate that the natural isolates do not represent recent contamination by the laboratory strain, and 10% carry plasmids or bacteriophages which have been acquired in nature by HGT from unrelated bacteria. We propose that ATCC14028s has repeatedly escaped from the laboratory environment into nature via laboratory accidents or infections, but the escaped micro-lineages have only a limited life span. As a result, there is a genetic gap separating HC20_373 from its closest natural relatives, representing a divergence between them in 1890 followed by repeated extinction events of escaped HC20_373.