Evolution of Salmonella enterica serotype Typhimurium driven by anthropogenic selection and niche adaptation

Abstract

Salmonella enterica serotype Typhimurium (S. Typhimurium) is a leading cause of gastroenteritis and disseminated disease worldwide, and a model organism for host pathogen interactions. Genotypic variation of S. Typhimurium results in strains with diverse host range, pathogenicity and risk to food safety. A robust fully parsimonious phylogenetic tree constructed from recombination purged variation in the whole genome sequence of 131 diverse strains of S. Typhimurium revealed population structure composed of two high order clades (α and β) and multiple subclades on extended internal branches, that exhibited distinct signatures of host adaptation and anthropogenic selection. Clade α contained a number of subclades composed of strains from well characterized epidemics in domesticated animals, while clade β predominantly contained subclades associated with wild avian species, with the notable exception of a subclade containing the DT204/49 complex. The contrasting epidemiology of α and β strains was reflected in distinct distribution of antimicrobial resistance (AMR) genes, accumulation of hypothetically disrupted coding sequences (HDCS), and signatures of functional diversification associated with invasiveness of host adapted serotypes. Gene flux was predominantly driven by acquisition, loss or recombination of prophage, awhile acquisition of large genetic islands (SGI-1 and 4) was restricted to two recent pandemic clones (DT104 and monophasic S. Typhimurium ST34) in clade α.Together, our data are consistent with the view that a broad host range common ancestor of S.Typhimurium diversified with clade α lineages remained largely associated with multiple domesticated animal species, while clade β spawned multiple lineages that underwent diversifying selection associated with adaptation to various niches, predominantly in wild avian species.

ProkEvo: an automated, reproducible, and scalable framework for high-throughput bacterial population genomics analyses

“…5A ). This partitioning matches the known clonality of the S. Typhimurium Monophasic populations and their association with the ST34 complex [65]. As for the Biphasic population, it is predominantly associated with ST19 and likely contains the ancestor of the other ST clonal complexes.…”

“…Therefore, we designed the studies described below to provide a practical example of how to link the distribution of known AMR genes to the population structure of the organism using serovars and STs in the case of S. enterica lineage I serovars, and STs for C. jejuni and S. aureus . We chose to use known AMR loci and evaluate their association with STs and epidemiological clones worldwide, as in the case of Salmonella [65], C. jejuni [66], and S. aureus [67].…”

Whole-genome epidemiology links phage-mediated acquisition of a virulence gene to the clonal expansion of a pandemic Salmonella enterica serovar Typhimurium clone

“…In S . Typhimurium strains NCTC 13348 (DT104), D23580 (ST313) and SO7676-03 (DT56), mTmV displaced the TmVII prophage integrated in thrW [23], as indicated by the PCR amplification of the mTmV junctions with specific primers.…”

“…LITE libraries with the DNA of 49 monophasic S .Typhimurium ST34 (Table S3) were generated and sequenced at the Earlham Institute using a HiSeq 2500 system (Illumina), as described previously [31]. Long-read whole-genome sequencing of strain S01569-10 [9] was performed using a PacBio RS system (Pacific Biosciences) at the Earlham Institute and long-read sequence assembled, as previously described [23].…”

“…Temperate bacteriophages represent an important source of HGT that can modify the characteristics of bacteria through cargo genes [22], and account for a greater proportion of the lineage-specific accessory genome in S . Typhimurium than either plasmids or non-phage chromosomal genes [23]. Monophasic S .…”