Chicken Production and Human Clinical Escherichia coli Isolates Differ in Their Carriage of Antimicrobial Resistance and Virulence Factors

Appl Environ Microbiol. 2023 Feb 28;89(2):e0116722. doi: 10.1128/aem.01167-22. Epub 2023 Jan 18.

Abstract

Contamination of food animal products by Escherichia coli is a leading cause of foodborne disease outbreaks, hospitalizations, and deaths in humans. Chicken is the most consumed meat both in the United States and across the globe according to the U.S. Department of Agriculture. Although E. coli is a ubiquitous commensal bacterium of the guts of humans and animals, its ability to acquire antimicrobial resistance (AMR) genes and virulence factors (VFs) can lead to the emergence of pathogenic strains that are resistant to critically important antibiotics. Thus, it is important to identify the genetic factors that contribute to the virulence and AMR of E. coli. In this study, we performed in-depth genomic evaluation of AMR genes and VFs of E. coli genomes available through the National Antimicrobial Resistance Monitoring System GenomeTrackr database. Our objective was to determine the genetic relatedness of chicken production isolates and human clinical isolates. To achieve this aim, we first developed a massively parallel analytical pipeline (Reads2Resistome) to accurately characterize the resistome of each E. coli genome, including the AMR genes and VFs harbored. We used random forests and hierarchical clustering to show that AMR genes and VFs are sufficient to classify isolates into different pathogenic phylogroups and host origin. We found that the presence of key type III secretion system and AMR genes differentiated human clinical isolates from chicken production isolates. These results further improve our understanding of the interconnected role AMR genes and VFs play in shaping the evolution of pathogenic E. coli strains. IMPORTANCE Pathogenic Escherichia coli causes disease in both humans and food-producing animals. E. coli pathogenesis is dependent on a repertoire of virulence factors and antimicrobial resistance genes. Food-borne outbreaks are highly associated with the consumption of undercooked and contaminated food products. This association highlights the need to understand the genetic factors that make E. coli virulent and pathogenic in humans and poultry. This research shows that E. coli isolates originating from human clinical settings and chicken production harbor different antimicrobial resistance genes and virulence factors that can be used to classify them into phylogroups and host origins. In addition, to aid in the repeatability and reproducibility of the results presented in this study, we have made a public repository of the Reads2Resistome pipeline and have provided the accession numbers associated with the E. coli genomes analyzed.

Keywords: Escherichia coli; antimicrobial resistance; poultry production; random forests; virulence factors.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Anti-Bacterial Agents / pharmacology
  • Anti-Infective Agents*
  • Chickens / microbiology
  • Drug Resistance, Bacterial / genetics
  • Escherichia coli
  • Escherichia coli Infections* / microbiology
  • Escherichia coli Infections* / veterinary
  • Humans
  • Reproducibility of Results
  • Virulence Factors / genetics

Substances

  • Virulence Factors
  • Anti-Bacterial Agents
  • Anti-Infective Agents