Virulome analysis of Escherichia coli ST117 from bovine sources identifies similarities and differences with strains isolated from other food animals

Authors: Haley, Bradd; SALAHEEN, SERAJUS - US Department Of Agriculture (USDA); Kim, Seonwoo; Van Kessel, Jo Ann

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/14/2023
Publication Date: 1/4/2024
Citation: Haley, B.J., Salaheen, S., Kim, S., Van Kessel, J.S. 2024. Virulome analysis of Escherichia coli ST117 from bovine sources identifies similarities and differences with strains isolated from other food animals. PLOS ONE. 10:e0296514. https://doi.org/10.1371/journal.pone.0296514.
DOI: https://doi.org/10.1371/journal.pone.0296514

Interpretive Summary: Extraintestinal infections are a significant human health concern and Escherichia coli sequence type 117 (ST117) is globally known as a human pathogen that causes extraintestinal infections, such as urinary tract infections. The primary reservoir of this pathogen is thought to be poultry, and strains from these animals have been well-characterized. However, E. coli ST117 strains from other food animals have not been adequately evaluated. Here we analyzed the genomes of 40 E. coli ST117 along with over 1000 ST117 genomes from poultry, swine, and humans. Results of this study demonstrated that bovine-associated genomes encode virulence factors (VFs) known to be involved in extraintestinal infections, but also occasionally encode the Shiga toxin, a VF known to be involved in severe gastrointestinal infections, and more frequently identified in E. coli from ruminants than other animals. The majority of the E. coli ST117 genomes from cows were multidrug-resistant, and some encoded genes that conferred resistance to antibiotics of human health significance. Results of this study demonstrate cattle as a reservoir of ST117 strains, some of which are highly similar to those isolated from other food animals and some of which have unique bovine-specific characteristics, such as the Shiga toxin. This information can be used by scientists to further understand the distribution of pathogenic bacteria that cause extraintestinal infections in humans.

Technical Abstract: Escherichia coli ST117 is a pandemic extraintestinal pathogenic E. coli (ExPEC) causing significant morbidity globally. Poultry are a known reservoir of this pathogen, but the characteristics of ST117 strains from other animal sources have not been adequately investigated. Here we characterize the genomes of 40 ST117 strains recovered primarily from preweaned dairy calves, but also from older postweaned and lactating cows, in the context of other bovine-associated strains and strains from poultry, swine, and humans. Results of this study demonstrate that bovine-associated genomes encoded virulence factors (VFs) known to be involved in extraintestinal infections, but also occasionally encode the Shiga toxin, a VF known to be involved in severe gastrointestinal infections and more frequently identified in E. coli from ruminants than other animals. Bovine-associated genomes were also more likely to encode afa-VIII (adhesins), pap (P-fimbriae), cdt (cytolethal distending toxin), and stx (Shiga toxins) than were poultry and swine-associated genomes. All of the genomes were grouped into seven virulence clusters, with bovine-associated genomes grouping into Clusters 1, 2, 4, 5, but not 3, 6, or 7. Major differences in the presence of virulence factors between clusters were observed as well. Antimicrobial resistance genes were detected in 112 of 122 (91%) bovine-associated isolates, with 103 of these being multidrug-resistant. Inclusion of genomes that differed by one multi-locus sequence type allele identified 31 STs, four of these among the bovine-associated genomes. These non-ST117 genomes clustered with the ST117 genomes suggesting that they may cause similar disease as ST117. Results of this study identify cattle as a reservoir of ST117 strains, some of which are highly similar to those isolated from other food animals and some of which have unique bovine-specific characteristics.