Emergence and divergence of major lineages of Shiga-toxin-producing Escherichia coli in Australia

Abstract

Shiga-toxin-producing Escherichia coli (STEC) infection is an important global cause of foodborne disease. To date however, genomics-based studies of STEC have been predominately focused upon STEC collected in the Northern Hemisphere. Here, we demonstrate the population structure of 485 STEC isolates in Australia, and show that several clonal groups (CGs) common to Australia were infrequently detected in a representative selection of contemporary STEC genomes from around the globe. Further, phylogenetic analysis demonstrated that lineage II of the global O157:H7 STEC was most prevalent in Australia, and was characterized by a frameshift mutation in flgF, resulting in the H-non-motile phenotype. Strong concordance between in silico and phenotypic serotyping was observed, along with concordance between in silico and conventional detection of stx genes. These data represent the most comprehensive STEC analysis from the Southern Hemisphere, and provide a framework for future national genomics-based surveillance of STEC in Australia.

Keywords: STEC; enteric pathogens; epidemiology; evolution; genomic epidemiology.

Fig. 1.

Overview of STEC population structure in Australia. The inferred core phylogeny of 558 STEC genomes produced from 235 746 informative SNPs. The reference genome was O157:H7 Sakai (NCBI accession number: NC_002695.2). Identified CGs are delineated by the most common ST in the CG. The eight major CGs are identified by different colours.

Fig. 2.

Summary of the features of the eight most common STEC CGs in this study. Data indicates the source (geography or animal or historic Australian) of the genomes included in the CGs. The N (Aus) indicates the number of isolates from humans between 2007–2016. The ‘O-group’ indicates the distinct O-antigen genes detected in the isolates. The ‘H-type’ indicates the distinct H-antigen genes detected in the isolates. Where no O-group or H-type was detected in silico, this is given by O- and H-, respectively. ‘AMR profiles’ indicates the proportion of AMR determinants acquired by horizontal gene transfer grouped by drug class detected in the STEC isolates.

Fig. 3.

Phylogeny of CG11 suggests emergence of local Australian STEC. (a) Maximum clade credibility phylogeny of 311 isolates belonging to the CG11 lineage, including the reference Sakai genome. Tips are coloured by Manning clade membership [20] determined in silico. The scale is in years and nodes of posterior support ≥95 are indicated in the phylogeny by black circles at the node. Isolates from the 2013 STEC outbreak associated with cattle are indicated to the right of the phylogeny [18]. (b) Geographic location of strain collection site (AUS: Australia, UK: United Kingdom and USA: United States of America). (c) The presence of stx subtypes is shown to the right of the phylogeny. (d) H-type phenotype data (where available) is shown, together with detection of an insertion of a cytosine base in position 125 in flgF associated with a non-motile flagellar phenotype. (e) Isolates that were ten pairwise SNPs from another isolate are shown in black.