Abstract

BackgroundA total of 179 Shiga toxin-producing Escherichia coli (STEC) complete genomes were analyzed in terms of serotypes, prophage coding regions, and stx gene variants and their distribution. We further examined the genetic diversity of Stx-converting phage genomes (Stx phages), focusing on the lysis-lysogeny decision and lytic cassettes.ResultsWe show that most STEC isolates belong to non-O157 serotypes (73 %), regardless the sources and geographical regions. While the majority of STEC genomes contain a single stx gene (61 %), strains containing two (35 %), three (3 %) and four (1 %) stx genes were also found, being stx2 the most prevalent gene variant. Their location is exclusively found in intact prophage regions, indicating that they are phage-borne. We further demonstrate that Stx phages can be grouped into four clusters (A, B, C and D), three subclusters (A1, A2 and A3) and one singleton, based on their shared gene content. This cluster distribution is in good agreement with their predicted virion morphologies. Stx phage genomes are highly diverse with a vast number of 1,838 gene phamilies (phams) of related sequences (of which 677 are orphams i.e. unique genes) and, although having high mosaicism, they are generally organized into three major transcripts. While the mechanisms that guide lysis–lysogeny decision are complex, there is a strong selective pressure to maintain the stx genes location close to the lytic cassette composed of predicted SAR-endolysin and pin-holin lytic proteins. The evolution of STEC Stx phages seems to be strongly related to acquiring genetic material, probably from horizontal gene transfer events.ConclusionsThis work provides novel insights on the genetic structure of Stx phages, showing a high genetic diversity throughout the genomes, where the various lysis-lysogeny regulatory systems are in contrast with an uncommon, but conserved, lytic system always adjacent to stx genes.

Highlights

  • A total of 179 Shiga toxin-producing Escherichia coli (STEC) complete genomes were analyzed in terms of serotypes, prophage coding regions, and stx gene variants and their distribution

  • We found all stx genes within intact Stx phages, rendering them the ability to potentially excise and infect new hosts, as observed in Shigella and Aeromonas strains, which carry Stx phages homologous to the ones detected in STEC [41, 47]

  • There is a considerable diversity of STEC serotypes that do not fall into the well-known O157:H7 and the so-called top six non-O157 serotypes (O26, O45, O103, O111, O121, O145), which carry complete Stx phages with stx genes variants

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Summary

Introduction

A total of 179 Shiga toxin-producing Escherichia coli (STEC) complete genomes were analyzed in terms of serotypes, prophage coding regions, and stx gene variants and their distribution. Shiga toxin-producing Escherichia coli (STEC) are important foodborne pathogens, responsible for numerous infections worldwide. There are two known Shiga toxin types, Stx and Stx, being further divided into three (a, c, d) and nine (a to i) subtypes, respectively [3,4,5,6]. Pinto et al BMC Genomics (2021) 22:366 subtype carried by STEC strains, being believed that Stx2a is the most associated with severe forms of the disease [7,8,9,10,11]. Several STEC serotypes have been associated with disease; not all are linked with severe infections. The most relevant serotypes in health risk are O157, O26, O45, O91, O103, O104, O111, O113, O145, and O121 [12, 13]

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