Persistence of antibiotic resistance genes in beef cattle backgrounding environment over two years after cessation of operation

Authors: Agga, Getahun; Cook, Kimberly - Kim; NETTHISINGHE, ANNESLY - Western Kentucky University; GILFILLEN, REBECCA - Western Kentucky University; WOOSLEY, PAUL - Western Kentucky University; Sistani, Karamat

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/6/2019
Publication Date: 2/15/2019
Publication URL: https://handle.nal.usda.gov/10113/6471073
Citation: Agga, G.E., Cook, K.L., Netthisinghe, A.M., Gilfillen, R.A., Woosley, P.B., Sistani, K.R. 2019. Persistence of antibiotic resistance genes in beef cattle backgrounding environment over two years after cessation of operation. PLoS One. 12(2):1-19. https://doi.org/10.1371/journal.pone.0212510.
DOI: https://doi.org/10.1371/journal.pone.0212510

Interpretive Summary: Confinement of cattle at feedlot can facilitate the spread of antibiotic resistance genes. To understand for how long the genes persist in beef cattle production environment we monitored a beef cattle backgrounding environment for two years after removal of cattle from the operation. Soil samples were collected from specifically georeferenced locations at cattle removal, and then one year and two years after cattle were removed. Concentrations of total bacteria, Enterococcus bacteria and the antibiotic resistance genes were higher in and around the feeding area with a gradual decline in the grazing area. Although significantly lowered two years after cattle removal, their concentrations were still higher than that observed in the grazing area of the backgrounding environment. These results indicate that antibiotic resistant bacteria and the genes associated with resistance can persist longer after cessation of operation, and in the absence of antibiotic use.

Technical Abstract: Confined animal feeding operations can facilitate the spread of genes associated with antibiotic resistance. It is not known how cattle removal from beef cattle backgrounding operation affects the persistence of antibiotic resistance genes (ARGs) in the environment. We investigated the effect of cessation of beef cattle backgrounding operation on the persistence and distribution of ARGs in the beef cattle backgrounding environment. The study was conducted at a pasture-feedlot type beef cattle backgrounding operation which consisted of feeding and grazing areas that were separated by a fence with an access gate. Backgrounding occurred for seven years before cattle were removed from the facility. Soil samples (n=78) from 26 georeferenced locations were collected at the baseline before cattle were removed, and then one year and two years after cattle were removed. Total community DNA was extracted from the soil samples and total bacterial population (16S rRNA), total Enterococcus species and class 1 integrons (intI1), and erythromycin (ermB and ermF), sulfonamide (sul1 and sul2) and tetracycline (tetO, tetW and tetQ) resistance genes were quantified. Concentrations of total bacteria, Enterococcus spp., class 1 integrons, and ARGs were higher in the feeding area and its immediate vicinity (around the fence and the gate) followed by a gradient decline along the grazing area. Although the concentrations of total bacteria, Enterococcus spp., class 1 integrons and ARGs in the feeding area significantly decreased two years after cattle removal, their concentrations were still higher than that observed in the grazing area. Higher concentrations over a two year period in the feeding area when compared to the grazing area suggest a lasting effect of confined beef cattle production system on the persistence of bacteria and ARGs in the soil.