Escherichia coli ST117: exploring the zoonotic hypothesis

Abstract

Extraintestinal pathogenic Escherichia coli (ExPEC) can lead to severe infections, with additional risks of increasing antimicrobial resistance rates. Genotypic similarities between ExPEC and avian pathogenic E. coli (APEC) support a possible role for a poultry meat reservoir in human disease. Some genomic studies have been done on the ST117 lineage which contaminates poultry meat, carries multidrug resistance, can be found in the human intestinal microbiota, and causes human extraintestinal disease. This study analyzed the genomes of 61 E. coli from Brazilian poultry outbreaks focusing on ST117, to further define its possible zoonotic characteristics by genotypic and phylogenomic analyses, along with 1,699 worldwide ST117 isolates originating from human, animal, and environment sources. A predominance of ST117 was detected in the Brazilian isolates (n = 20/61) frequently carrying resistance to critical antibiotics (>86%) linked to IncFII, IncI1, or IncX4 replicons. High similarities were found between IncX4 from Brazilian outbreaks and those from E. coli recovered from imported Brazilian poultry meat and human clinical cases. The ST117 phylogeny showed non-specificity according to host and continent and an AMR index score indicated the highest resistance in Asia and South America, with the latter statistically more resistant and overrepresented with resistance to extended-spectrum beta-lactamases (ESBL). Most ST117 human isolates were predicted to have a poultry origin (93%, 138/148). In conclusion, poultry is a likely source for zoonotic ExPEC strains, particularly the ST117 lineage which can also serve as a reservoir for resistance determinants against critical antibiotics encoded on highly transmissible plasmids.

Importance: Certain extraintestinal pathogenic Escherichia coli (ExPEC) are particularly important as they affect humans and animals. Lineages, such as ST117, are predominant in poultry and frequent carriers of antibiotic resistance, presenting a risk to humans handling or ingesting poultry products. We analyzed ExPEC isolates causing outbreaks in Brazilian poultry, focusing on the ST117 as the most detected lineage. Genomic comparisons with international isolates from humans and animals were performed describing the potential zoonotic profile. The Brazilian ST117 isolates carried resistance determinants against critical antibiotics, mainly on plasmids, in some cases identical to those carried by international isolates. South American ST117 isolates from all sources generally exhibit more resistance, including to critical antibiotics, and worldwide, the vast majority of human isolates belonging to this lineage have a predicted poultry origin. As the world's largest poultry exporter, Brazil has an important role in developing strategies to prevent the dissemination of multidrug-resistant zoonotic ExPEC strains.

Keywords: Escherichia coli; ExPEC; FZEC; ST117; poultry.

Fig 1

(A, B, and C) Comparison of the genetic environment surrounding high-priority AMR genes with the highest similarity (BLASTn) isolate(s). The genes of interest are in bold, and the arrows indicate the position and orientation of open reading frames. (D, E, and F): BLAST atlas comparison. The isolates of this study are highlighted in bold. The inner ring indicates one of the plasmids of this study as the reference, compared with the additional plasmids and highest identity draft ST117 sequences (outer rings). The colors represent each corresponding continent, with the host colored by different shades: darker shades identify human isolates, and lighter indicate animal isolates.

Fig 2

Midpoint rooted core genome phylogeny of 1,719 ST117 isolates connecting to the available metadata for host, continent, and the added overall score for each AMR class based on the index weighing score for each antibiotic class, from the inner to the outer ring, respectively. The phylogeny was built on SNP calling in 55% (2,85Mb) of the reference genome. The Brazilian poultry isolates of this study are shown with a red circle at the tip of the respective branch.

Fig 3

(A) Heat map indicating the added index weighting scores for antimicrobial classes identified in ST117 isolates according to each country. (B) Heat map showing the percentages of isolates from the different continents carrying genes conferring resistance to the antimicrobial class reported in the ST117 isolates. The colors in A and B indicate the lowest score/percentage (lighter) to the highest added scores (darker).

Fig 4

PCA biplot illustrating the clustering of putative zoonotic ST117 isolates (N = 126) based on the presence of resistance to antimicrobial classes. Isolates are colored based on the continent of origin. The large dots indicate the mean point within each group (continent) and the ellipses indicate the 95% confidence levels of the mean, while the arrows indicate the percentage of explained variance of each antibiotic class (top three shown). * not ESBL or carbapenemase.