Genomic epidemiology and carbon metabolism of Escherichia coli serogroup O145 reflect contrasting phylogenies

PLoS One. 2020 Jun 25;15(6):e0235066. doi: 10.1371/journal.pone.0235066. eCollection 2020.

Abstract

Shiga toxin-producing Escherichia coli (STEC) are a leading cause of foodborne outbreaks of human disease, but they reside harmlessly as an asymptomatic commensal in the ruminant gut. STEC serogroup O145 are difficult to isolate as routine diagnostic methods are unable to distinguish non-O157 serogroups due to their heterogeneous metabolic characteristics, resulting in under-reporting which is likely to conceal their true prevalence. In light of these deficiencies, the purpose of this study was a twofold approach to investigate enhanced STEC O145 diagnostic culture-based methods: firstly, to use a genomic epidemiology approach to understand the genetic diversity and population structure of serogroup O145 at both a local (New Zealand) (n = 47) and global scale (n = 75) and, secondly, to identify metabolic characteristics that will help the development of a differential media for this serogroup. Analysis of a subset of E. coli serogroup O145 strains demonstrated considerable diversity in carbon utilisation, which varied in association with eae subtype and sequence type. Several carbon substrates, such as D-serine and D-malic acid, were utilised by the majority of serogroup O145 strains, which, when coupled with current molecular and culture-based methods, could aid in the identification of presumptive E. coli serogroup O145 isolates. These carbon substrates warrant subsequent testing with additional serogroup O145 strains and non-O145 strains. Serogroup O145 strains displayed extensive genetic heterogeneity that was correlated with sequence type and eae subtype, suggesting these genetic markers are good indicators for distinct E. coli phylogenetic lineages. Pangenome analysis identified a core of 3,036 genes and an open pangenome of >14,000 genes, which is consistent with the identification of distinct phylogenetic lineages. Overall, this study highlighted the phenotypic and genotypic heterogeneity within E. coli serogroup O145, suggesting that the development of a differential media targeting this serogroup will be challenging.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carbon / metabolism*
  • Escherichia coli Infections* / epidemiology
  • Escherichia coli Infections* / genetics
  • Escherichia coli Infections* / metabolism
  • Genotype*
  • Humans
  • Malates / metabolism
  • New Zealand / epidemiology
  • Phylogeny*
  • Serine / genetics
  • Serine / metabolism
  • Serogroup*
  • Shiga-Toxigenic Escherichia coli* / genetics
  • Shiga-Toxigenic Escherichia coli* / isolation & purification
  • Shiga-Toxigenic Escherichia coli* / metabolism

Substances

  • Malates
  • Serine
  • Carbon
  • malic acid

Grants and funding

This research was supported by the AgResearch Food Provenance and Assurance Strategic Science Investment (SSI) Fund programme awarded to GB, the Massey University School of Veterinary Science post-graduate research fund Massey University awarded to RMC and the Palmerston North Medical Research Foundation awarded to ALC. The funder AgResearch Ltd provided support in the form of salaries for the authors ALC and GB, but AgResearch Ltd and other Funders did not have any additional role in the study design, data collection, and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section.