The global population structure and evolutionary history of the acquisition of major virulence factor-encoding genetic elements in Shiga toxin-producing Escherichia coli O121:H19.

Ruriko Nishida,Junko Isobe,Tetsuya Harada,Hiroshi Narimatsu,Kazuhiko Ishikawa,Tetsuya Hayashi,Yuhki Nagai,Atsushi Toyoda,Koichi Akashi,Kazunori Murase,Itsuki Taniguchi,Makoto Ohnishi,Tadasuke Ooka,Kazuko Seto,Yoshitoshi Ogura,Dongchon Kang,Mitsuhiro Hamasaki,Mitsuhiro Kameyama,Eiji Yokoyama,Jun Kawase,Yoshiki Etoh,Sunao Iyoda,Keiji Nakamura,Yuko Matsumoto,Takehiko Itoh,Jun Yatsuyanagi,Keiko Kimata,Kenichi Lee ,Jacques Mainil ,Takayuki Shiomoto ,Denis Piérard ,Yasuhiro Gotoh

doi:10.1099/mgen.0.000716

Abstract

Shiga toxin (Stx)-producing Escherichia coli (STEC) are foodborne pathogens causing serious diseases, such as haemorrhagic colitis and haemolytic uraemic syndrome. Although O157:H7 STEC strains have been the most prevalent, incidences of STEC infections by several other serotypes have recently increased. O121:H19 STEC is one of these major non-O157 STECs, but systematic whole genome sequence (WGS) analyses have not yet been conducted on this STEC. Here, we performed a global WGS analysis of 638 O121:H19 strains, including 143 sequenced in this study, and a detailed comparison of 11 complete genomes, including four obtained in this study. By serotype-wide WGS analysis, we found that O121:H19 strains were divided into four lineages, including major and second major lineages (named L1 and L3, respectively), and that the locus of enterocyte effacement (LEE) encoding a type III secretion system (T3SS) was acquired by the common ancestor of O121:H19. Analyses of 11 complete genomes belonging to L1 or L3 revealed remarkable interlineage differences in the prophage pool and prophage-encoded T3SS effector repertoire, independent acquisition of virulence plasmids by the two lineages, and high conservation in the prophage repertoire, including that for Stx2a phages in lineage L1. Further sequence determination of complete Stx2a phage genomes of 49 strains confirmed that Stx2a phages in lineage L1 are highly conserved short-tailed phages, while those in lineage L3 are long-tailed lambda-like phages with notable genomic diversity, suggesting that an Stx2a phage was acquired by the common ancestor of L1 and has been stably maintained. Consistent with these genomic features of Stx2a phages, most lineage L1 strains produced much higher levels of Stx2a than lineage L3 strains. Altogether, this study provides a global phylogenetic overview of O121:H19 STEC and shows the interlineage genomic differences and the highly conserved genomic features of the major lineage within this serotype of STEC.

Highlights

Shiga toxin (Stx)-producing Escherichia coli (STEC) are foodborne pathogens that cause a range of diseases, from mild enteritis to severe haemorrhagic enteritis, and sometimes life-threatening complications such as haemolytic uraemic syndrome (HUS) [1]
By serotype-wide whole genome sequence (WGS) analysis, we found that O121:H19 strains were divided into four lineages, including major and second major lineages, and that the locus of enterocyte effacement (LEE) encoding a type III secretion system (T3SS) was acquired by the common ancestor of O121:H19
Through a global WGS analysis of O121:H19 STEC, we identified four lineages

Summary

Introduction

Shiga toxin (Stx)-producing Escherichia coli (STEC) are foodborne pathogens that cause a range of diseases, from mild enteritis to severe haemorrhagic enteritis, and sometimes life-threatening complications such as haemolytic uraemic syndrome (HUS) [1]. While there are STEC strains with various serotypes, those with O157:H7 serotype STEC infections by STEC strains with non-O157:H7 serotypes (non-O 157 STEC) have increased in recent years. In the United States and Europe, the total number of reported non-O 157 STEC infections has exceeded that of O157 since 2013 and 2007, respectively, and many outbreaks of non-O 157 STEC infections have been reported [2, 3]. The major virulence factors of typical STECs are Stxs encoded by prophages and the type III secretion system (T3SS) encoded by the locus of enterocyte effacement (LEE). Several T3SS- secreted effectors are encoded by the LEE, many additional effectors are encoded by prophages [6,7,8].

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Results

Conclusion