Genomic Characterization of Enterococcus hirae From Beef Cattle Feedlots and Associated Environmental Continuum

Sani-E-Zehra Zaidi; Rahat Zaheer; Ruth Barbieri; Shaun R Cook; Sherry J Hannon; Calvin W Booker; Deirdre Church; Gary Van Domselaar; Athanasios Zovoilis; Tim A McAllister

doi:10.3389/fmicb.2022.859990

Genomic Characterization of Enterococcus hirae From Beef Cattle Feedlots and Associated Environmental Continuum

Front Microbiol. 2022 Jun 27:13:859990. doi: 10.3389/fmicb.2022.859990. eCollection 2022.

Authors

Affiliations

¹ Lethbridge Research and Development Centre, Agriculture and Agri-Food Canada, Lethbridge, AB, Canada.
² University of Lethbridge, Lethbridge, AB, Canada.
³ Feedlot Health Management Services, Okotoks, AB, Canada.
⁴ Cumming School of Medicine, University of Calgary, Calgary, AB, Canada.
⁵ Calgary Laboratory Services, Calgary, AB, Canada.
⁶ National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, MB, Canada.

Abstract

Enterococci are commensal bacteria of the gastrointestinal tract of humans, animals, and insects. They are also found in soil, water, and plant ecosystems. The presence of enterococci in human, animal, and environmental settings makes these bacteria ideal candidates to study antimicrobial resistance in the One-Health continuum. This study focused on Enterococcus hirae isolates (n = 4,601) predominantly isolated from beef production systems including bovine feces (n = 4,117, 89.5%), catch-basin water (n = 306, 66.5%), stockpiled bovine manure (n = 24, 0.5%), and natural water sources near feedlots (n = 145, 32%), and a few isolates from urban wastewater (n = 9, 0.2%) denoted as human-associated environmental samples. Antimicrobial susceptibility profiling of a subset (n = 1,319) of E. hirae isolates originating from beef production systems (n = 1,308) showed high resistance to tetracycline (65%) and erythromycin (57%) with 50.4% isolates harboring multi-drug resistance, whereas urban wastewater isolates (n = 9) were resistant to nitrofurantoin (44.5%) and tigecycline (44.5%) followed by linezolid (33.3%). Genes for tetracycline (tetL, M, S/M, and O/32/O) and macrolide resistance erm(B) were frequently found in beef production isolates. Antimicrobial resistance profiles of E. hirae isolates recovered from different environmental settings appeared to reflect the kind of antimicrobial usage in beef and human sectors. Comparative genomic analysis of E. hirae isolates showed an open pan-genome that consisted of 1,427 core genes, 358 soft core genes, 1701 shell genes, and 7,969 cloud genes. Across species comparative genomic analysis conducted on E. hirae, Enterococcus faecalis and Enterococcus faecium genomes revealed that E. hirae had unique genes associated with vitamin production, cellulose, and pectin degradation, traits which may support its adaptation to the bovine digestive tract. E. faecium and E. faecalis more frequently harbored virulence genes associated with biofilm formation, iron transport, and cell adhesion, suggesting niche specificity within these species.

Keywords: antimicrobial resistance; cattle production; enterococci; genomic signatures; pan-genome.

Copyright © 2022 Sherry J. Hannon, Calvin W. Booker, Deirdre Church, Gary Van Domselaar, Athanasios Zovoilis and Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada for the contribution of Tim A. McAllister, Sani-e-Zehra Zaidi , Rahat Zaheer, Ruth Barbieri and Shaun R. Cook.