Genome-wide analysis of Escherichia coli isolated from dairy animals identifies virulence factors and genes enriched in multidrug-resistant strains

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

Submitted to: Antibiotics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/16/2023
Publication Date: 10/17/2023
Citation: Haley, B.J., Kim, S., Salaheen, S., Hovingh, E., Van Kessel, J.S. 2023. Genome-wide analysis of Escherichia coli isolated from dairy animals identifies virulence factors and genes enriched in multidrug-resistant strains. Antibiotics. 12(10): e1559. https://doi.org/10.3390/antibiotics12101559.
DOI: https://doi.org/10.3390/antibiotics12101559

Interpretive Summary: Antimicrobial resistance is a growing global concern that affects the health of both humans and animals. Dairy cows are reservoirs of antimicrobial-resistant bacteria some of which are potential human pathogens such as Escherichia coli (E. coli). This species of bacteria has been characterized from lactating cows, but there is limited information on the antimicrobial resistance and virulence characteristics from dry cows, postweaned calves, and preweaned calves. In this study, the genomes of 264 multidrug-resistant (MDR), antimicrobial-resistant, and antimicrobial-susceptible E. coli were sequenced and analyzed to determine their gene contents, including their resistance gene and virulence gene contents. Results of this study demonstrated that an appreciable number of E. coli carried genes conferring resistance to antibiotics of human health significance and can be considered potential human pathogens based on the presence of specific virulence genes. Some genes were more prevalent in MDR isolate genomes than in the genomes of sensitive isolates. The types of genes that were found more often in MDR isolates provide potential clues for understanding the mechanisms that lead to colonization of the calf gut by MDR bacteria. Results of this study yield important information on the virulence potential of E. coli from dairy animals of all ages as well as potential targets to reduce the carriage of MDR bacteria through simple dietary interventions. This information will guide researchers to develop and test interventions for reducing the levels of antimicrobial-resistant bacteria found in farm animals.

Technical Abstract: The gastrointestinal tracts of dairy calves and cows is a reservoir of antimicrobial-resistant bacteria (ARB) which are present regardless of previous antimicrobial therapy. Young calves harbor a greater abundance of resistant bacteria than older cows, but the factors driving this high abundance are unknown. Here we sequenced the genomes of 264 Escherichia coli isolates (105 multidrug resistant [MDR], 39 resistant, and 120 pansusceptible) from preweaned calves, postweaned calves, dry cows, and lactating cows on 80 commercial dairy operations to evaluate the genomic diversity, virulence and fitness factors (VFFs), and accessory gene content among the resistant and susceptible populations. Results indicated that both susceptible and resistant E. coli isolates recovered from animals on commercial dairy operations were highly diverse and encoded a large pool of virulence factors. In total, 838 transferrable antimicrobial resistance genes (ARGs) were detected, with genes conferring resistance to aminoglycosides being the most frequently detected. Multiple sequence types (STs) associated with mild to severe human gastrointestinal and extraintestinal infections were identified. In total 24,691 genes (non-ARGs and ARGs) were identified in the pangenome of susceptible and MDR strains. Of these, 619 were significantly enriched in MDR isolates, while 147 were enriched in susceptible isolates (Fisher test, Padj < 0.05). Significantly enriched genes in MDR isolates included the iron scavenging aerobactin synthesis and receptor genes (iucABCD-iutA) and the sitABCD system, as well as the P fimbriae pap genes, myo-inositol catabolism (iolABCDEG-iatA), and ascorbate transport genes (ulaABC). Results of this study demonstrate a highly diverse population of E. coli in commercial dairy operations, some of which encode virulence genes responsible for human infections. Further, the enriched accessory genes in MDR isolates (aerobactin, sit, P fimbriae, and myo-inositol catabolism and ascorbate transport genes) represent potential targets for reducing colonization of antimicrobial-resistant bacteria in the calf gut.