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

Abasiofiok Ibekwe; Lisa Durso; Thomas F Ducey; Adelumola Oladeinde; Charlene R Jackson; Jonathan G Frye; Robert Dungan; Tom Moorman; John P Brooks; Amarachukwu Obayiuwana; Hiren Karathia; Brian Fanelli; Nur Hasan

doi:10.3390/microorganisms9051057

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

Microorganisms. 2021 May 13;9(5):1057. doi: 10.3390/microorganisms9051057.

Authors

Affiliations

¹ US Salinity Laboratory, Agricultural Research Service, United States Department of Agriculture, Riverside, CA 92507, USA.
² Agricultural Research Service, United States Department of Agriculture, Lincoln, NE 68583, USA.
³ Agricultural Research Service, United States Department of Agriculture, Florence, SC 29501, USA.
⁴ Agricultural Research Service, United States Department of Agriculture, Athens, GA 30605, USA.
⁵ Agricultural Research Service, United States Department of Agriculture, Kimberly, ID 83341, USA.
⁶ Agricultural Research Service, United States Department of Agriculture, Ames, IA 50011, USA.
⁷ Agricultural Research Service, United States Department of Agriculture, Mississippi State, MS 39762, USA.
⁸ Department of Biological Sciences (Microbiology Option), Augustine University Ilara (AUI), Epe 106101, Lagos State, Nigeria.
⁹ CosmosID Inc., Rockville, MD 20850, USA.
¹⁰ Center for Bioinformatics and Computational Biology, University of Maryland, College Park, MD 20878, USA.

Abstract

Antimicrobial resistance associated with the spread of plasmid-encoded extended-spectrum β-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, bla_CTX-M-15, bla_TEM-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.

Keywords: animal sources; antimicrobial resistance; extended-spectrum β-lactamase; multi-locus sequence typing; whole-genome sequencing.

Abstract

Grants and funding