Cumulative acquisition of pathogenicity islands has shaped virulence potential and contributed to the emergence of LEE-negative Shiga toxin-producing Escherichia coli strains

Emerg Microbes Infect. 2019;8(1):486-502. doi: 10.1080/22221751.2019.1595985.

Abstract

Shiga toxin-producing Escherichia coli (STEC) are foodborne pathogens causing severe gastroenteritis, which may lead to hemolytic uremic syndrome. The Locus of Enterocyte Effacement (LEE), a Pathogenicity Island (PAI), is a major determinant of intestinal epithelium attachment of a group of STEC strains; however, the virulence repertoire of STEC strains lacking LEE, has not been fully characterized. The incidence of LEE-negative STEC strains has increased in several countries, highlighting the relevance of their study. In order to gain insights into the basis for the emergence of LEE-negative STEC strains, we performed a large-scale genomic analysis of 367 strains isolated worldwide from humans, animals, food and the environment. We identified uncharacterized genomic islands, including two PAIs and one Integrative Conjugative Element. Additionally, the Locus of Adhesion and Autoaggregation (LAA) was the most prevalent PAI among LEE-negative strains and we found that it contributes to colonization of the mice intestine. Our comprehensive and rigorous comparative genomic and phylogenetic analyses suggest that the accumulative acquisition of PAIs has played an important, but currently unappreciated role, in the evolution of virulence in these strains. This study provides new knowledge on the pathogenicity of LEE-negative STEC strains and identifies molecular markers for their epidemiological surveillance.

Keywords: Integrative Conjugative Element; LEE-negative STEC; Locus of Adhesion and Autoaggregation; Pathogenicity Island; comparative genomics.

MeSH terms

  • Animals
  • Disease Models, Animal
  • Environmental Microbiology
  • Escherichia coli Infections / microbiology
  • Escherichia coli Infections / veterinary
  • Escherichia coli Proteins
  • Evolution, Molecular*
  • Food Microbiology
  • Genomic Islands*
  • Genotype
  • Incidence
  • Interspersed Repetitive Sequences
  • Intestines / microbiology
  • Mice
  • Phosphoproteins / deficiency*
  • Phylogeny
  • Shiga-Toxigenic Escherichia coli / genetics
  • Shiga-Toxigenic Escherichia coli / isolation & purification*
  • Shiga-Toxigenic Escherichia coli / pathogenicity*
  • Virulence
  • Virulence Factors / genetics*

Substances

  • Escherichia coli Proteins
  • LEE protein, E coli
  • Phosphoproteins
  • Virulence Factors

Grants and funding

This study was supported by FONDECYT grant 1161161 to R. Vidal and CONICYT-PCHA/2014-63140238 fellowship to D. Montero. Work at USC-LREC was supported by Project PI16/01477 from Plan Estatal de I+D+I 2013-2016, Instituto de Salud Carlos III, Subdirección General de Evaluación y Fomento de la Investigación and FEDER, Ministerio de Economia, Industria y Competitividad, Gobierno de España and Project ED431C 2017/57 from the Consellería de Cultura, Educación e Ordenación Universitaria, Xunta de Galicia and FEDER. Fondecyt 11150966 to Felipe Del Canto. Consejo Nacional de Ciencia y Tecnología; [Fondo Nacional de Desarrollo Científico y Tecnológico].