Phylogenetic Characterization of Salmonella enterica Serovar Typhimurium and Its Monophasic Variant Isolated from Food Animals in Japan Revealed Replacement of Major Epidemic Clones in the Last 4 Decades

J Clin Microbiol. 2018 Apr 25;56(5):e01758-17. doi: 10.1128/JCM.01758-17. Print 2018 May.

Abstract

Salmonella enterica serovar Typhimurium (Salmonella Typhimurium) and its monophasic variant (Salmonella 4,[5],12:i:-) are the major causes of gastroenteritis in both humans and animals. Pulsed-field gel electrophoresis and multilocus variable-number tandem-repeat analysis have been used widely as subtyping methods for these pathogens in molecular epidemiological analyses, but the results do not precisely reflect phylogenetic information. In this study, we performed a phylogenetic analysis of these serovars using whole-genome sequencing data and identified nine distinct genotypic clades. Then, we established an allele-specific PCR-based genotyping method detecting a clade-specific single nucleotide polymorphism to rapidly identify the clade of each isolate. Among a total of 815 isolates obtained from cattle in Japan between 1977 and 2017, clades 1, 7, and 9 contained 77% of isolates. Obvious replacement of the dominant clone was observed five times in this period, and clade 9, which mostly contains Salmonella 4,[5],12:i:-, is currently dominant. Among 140 isolates obtained from swine in Japan between 1976 and 2017, clades 3 and 9 contained 64% of isolates. Clade 9 is the latest clone as is the case in cattle isolates. Clade 9 is similar to an epidemic clone from Europe, which is characterized by sequence type 34 (ST34), chromosomal Salmonella genomic island 3, and a composite transposon containing antimicrobial resistance genes. The increased prevalence of clade 9 among food animals in Japan might be a part of the pandemic of the European Salmonella 4,[5],12:i:- clone.

Keywords: Japan; Salmonella enterica; Typhimurium; food animal; monophasic variant; pandemic; phylogeny.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cattle
  • DNA, Bacterial / genetics
  • Genome, Bacterial / genetics
  • Genotype
  • Japan / epidemiology
  • Meat / microbiology*
  • Molecular Epidemiology
  • Phylogeny*
  • Polymorphism, Single Nucleotide / genetics
  • Prevalence
  • Salmonella Infections, Animal / epidemiology*
  • Salmonella Infections, Animal / microbiology*
  • Salmonella typhimurium / classification*
  • Salmonella typhimurium / genetics
  • Salmonella typhimurium / isolation & purification
  • Sequence Analysis, DNA
  • Swine
  • Whole Genome Sequencing

Substances

  • DNA, Bacterial