Diversity of Plasmids and Genes Encoding Resistance to Extended-Spectrum ß-Lactamase in Escherichia coli from Different Animal Sources

Authors: Ibekwe, Abasiofiok - Mark; Durso, Lisa; Ducey, Thomas; Oladeinde, Adelumola - Ade; Jackson, Charlene; Frye, Jonathan; Dungan, Robert - Rob; Moorman, Thomas; Brooks, John; OBAYIUWANA, AMARACHUKWU - Augustine University Ilara; KARATHIA, HIREN - Cosmosid; FANELLI, BRIAN - Cosmosid; HASAN, NUR - Cosmosid

Submitted to: Microorganisms
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/4/2021
Publication Date: 5/13/2021
Citation: Ibekwe, A.M., Durso, L.M., Ducey, T.F., Oladeinde, A., Jackson, C.R., Frye, J.G., Dungan, R.S., Moorman, T.B., Brooks, J.P., Obayiuwana, A., Karathia, H., Fanelli, B., Hasan, N.A. 2021. Diversity of plasmids and genes encoding resistance to extended-spectrum ß-Lactamase in Escherichia coli from different animal sources. Microorganisms. 9(5). Article 1057. https://doi.org/10.3390/microorganisms9051057.
DOI: https://doi.org/10.3390/microorganisms9051057

Interpretive Summary: Antibiotic-resistant bacteria can be transferred from animals to humans by direct contact, and can spread to soil, food, and groundwater through the application of manure to agricultural fields. However, little is known about the population structure and antibiotic-resistant patterns of E. coli from different animal sources. E. coli isolates from different animal sources collected from different regions of the United States were typed into different groups, characterized by DNA method, and tested for resistant to 18 antibiotics. Furthermore, advance DNA method was used to identify genes that may easily be transferred from bacteria to bacteria. We found that swine and dairy cattle may be the main reservoirs of these bacteria. It was also determined that these bacteria are resistant to many antibiotics, and one of the isolates from swine may belong to a high-risk clone. This information will be of interest to livestock farmers, water quality agencies, government agencies, and researchers.

Technical Abstract: Antimicrobial resistance associated with the spread of plasmid-encoded extended-spectrum ß-lactamase (ESBL) genes conferring resistance to third generation cephalosporins is increasing worldwide. However, data on the population of ESBL producing E. coli in different animal sources and their antimicrobial characteristics are limited. The purpose of this study was to investigate potential reservoirs of ESBL-encoded genes in E. coli isolated from swine, beef, dairy, and poultry collected from different regions of the United States using whole-genome sequencing (WGS). Three hundred isolates were typed into different phylogroups, characterized by BOX AIR-1 PCR and tested for resistance to antimicrobials. Of the 300 isolates, 59.7% were resistant to sulfisoxazole, 49.3% to tetracycline, 32.3% to cephalothin, 22.3% to ampicillin, 20% to streptomycin, 16% to ticarcillin; resistance to the remaining 12 antimicrobials was less than 10%. Phylogroups A and B1 were most prevalent with A (n = 92, 30%) and B1 (87 = 29%). A total of nine E. coli isolates were confirmed as ESBL producers by double-disk synergy testing and multidrug resistant (MDR) to at least three antimicrobial drug classes. Using WGS, significantly higher numbers of ESBL-E. coli were detected in swine and dairy manure than from any other animal sources, suggesting that these may be the primary animal sources for ESBL producing E. coli. These isolates carry plasmids, such as IncFIA(B), IncFII, IncX1, IncX4, IncQ1, CollRNAI, Col440I, and acquired ARGs aph(6)-Id, aph(3')-Ib, aadA5, aph(3')-Ia, blaCTX-M-15, blaTEM-1B, mphA, ermB, catA1, sul1, sul2, tetB, dfrA17. One of the E. coli isolates from swine with ST 410 was resistant to nine antibiotics and carried more than 28 virulence factors, and this ST has been shown to belong to an international high-risk clone. Our data suggests that ESBL producing E. coli are widely distributed in different animal sources, but swine and dairy cattle may be their main reservoir.