Investigating the dispersal of antibiotic resistance associated genes from manure application to soil and drainage waters in simulated agricultural farmland systems

Authors: SMITH, SCHUYLER - Iowa State University; COLGAN, PHIL - Iowa State University; YANG, FAN - Iowa State University; RIEKE, ELIZABETH - Iowa State University; SOUPIR, MICHELLE - Iowa State University; Moorman, Thomas; Allen, Heather; HOWE, ADINA - Iowa State University

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/10/2019
Publication Date: 9/17/2019
Citation: Smith, S.D., Colgan, P., Yang, F., Rieke, E.L., Soupir, M.L., Moorman, T.B., Allen, H.K., Howe, A. 2019. Investigating the dispersal of antibiotic resistance associated genes from manure application to soil and drainage waters in simulated agricultural farmland systems. PLoS One. 14(9):e0222470. https://doi.org/10.1371/journal.pone.0222470.
DOI: https://doi.org/10.1371/journal.pone.0222470

Interpretive Summary: Manure from animals that have been treated with antibiotics is often used to fertilize agricultural soils and its application has previously been shown to enrich for genes associated with antibiotic resistance (ARG) in agroecosystems. To investigate the magnitude of this effect, we designed a column experiment simulating manure-treated agricultural soil that utilizes artificial subsurface drainage to determine the duration and extent which this type of manure fertilization impacts the set of genes associated with antibiotic resistance in drainage water. We classified ARGs in manure-treated drainage water by its source, manure, or soil. Overall, we found that 61% and 7% of the total abundance of ARGs found in drainage water could be attributed to growth of soil bacteria caused by manure addition and bacteria added in the manure itself, respectively. Among these ARGs, we identified 75 genes unique to manure that persisted in both soil and drainage water throughout a drainage season typical of the Upper Midwestern United States. While most of these genes gradually decreased in abundance over time, a gene for resistance to tetracycline (tet33) increased. These results demonstrate the influence of manure applications on the composition of the ARG in agricultural drainage water. The research informs scientists, advocacy groups, and agricultural commodity organizations and concerned citizens about swine manure application and fate of ARGs in the farm environment.

Technical Abstract: Manure from animals that have been treated with antibiotics is often used to fertilize agricultural soils and its application has previously been shown to enrich for genes associated with antibiotic resistance (ARG) in agroecosystems. To investigate the magnitude of this effect, we designed a column experiment simulating manure-treated agricultural soil that utilizes artificial subsurface drainage to determine the duration and extent which this type of manure fertilization impacts the set of genes associated with antibiotic resistance in drainage water. We classified ARGs in manure-treated drainage effluent water by its source of origin. Overall, we found that 61% and 7% of the total abundance of ARGs found in drainage water samples could be attributed to manure enrichment and manure addition, respectively. Among these ARGs, we identified 75 genes unique to manure that persisted in both soil and drainage water throughout a drainage season typical of the Upper Midwestern United States. While most of these genes gradually decreased in abundance over time, the IS6100-associated tet(33) gene accrued. These results demonstrate the influence of manure applications on the composition of the resistome observed in agricultural drainage water and highlight the importance of anthropogenic ARGs in the environment.