Sources and Drivers of ARGs in Urban Streams in Atlanta, Georgia, USA

The spread of antibiotic resistance genes (ARGs) in the aquatic environment is an emerging concern in the interest of protecting public health. Stemming the environmental dissemination of ARGs will require a better understanding of the sources and drivers of ARGs in the water environment. In this st...

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Main Authors: Robert A. Sowah, Marirosa Molina, Ourania Georgacopoulos, Blake Snyder, Mike Cyterski
Format: Article
Language:English
Published: MDPI AG 2022-09-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/10/9/1804
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author Robert A. Sowah
Marirosa Molina
Ourania Georgacopoulos
Blake Snyder
Mike Cyterski
author_facet Robert A. Sowah
Marirosa Molina
Ourania Georgacopoulos
Blake Snyder
Mike Cyterski
author_sort Robert A. Sowah
collection DOAJ
description The spread of antibiotic resistance genes (ARGs) in the aquatic environment is an emerging concern in the interest of protecting public health. Stemming the environmental dissemination of ARGs will require a better understanding of the sources and drivers of ARGs in the water environment. In this study, we used direct measurement of sewage-associated molecular markers, the class 1 integron gene, standard water quality parameters, and watershed characteristics to evaluate the sources and drivers of ARGs in an urban watershed impacted by a gradient of human activities. Quantitative polymerase chain reaction (qPCR) was used to quantify the abundance of the sewage-associated HF183, the <i>E</i>. <i>coli</i> fecal indicator, class 1 integron gene (<i>int</i>1), and the ARGs <i>sulI</i>, <i>sulII</i>, <i>tet</i>W, <i>tet</i>M, <i>ampC,</i> and <i>bla</i>SHV in stream water samples collected from the Proctor Creek watershed in Atlanta, Georgia. Our findings show that ARGs were widely distributed, with detection frequencies of 96% (<i>sulI</i> and <i>sulII</i>), 82% (<i>tet</i>W and <i>tet</i>M), and 49% (<i>ampC</i> and <i>bla</i>SHV). All the ARGs were positively and significantly correlated (<i>r</i> > 0.5) with the HF183 and <i>E</i>. <i>coli</i> markers. Non-linear machine learning models developed using generalized boosting show that more than 70% of the variation in ARG loads in the watershed could be explained by fecal source loading, with other factors such as class 1 integron, which is associated with acquired antibiotic resistance, and environmental factors contributing < 30% to ARG variation. These results suggest that input from fecal sources is a more critical driver of ARG dissemination than environmental stressors or horizontal gene transfer in aquatic environments highly impacted by anthropogenic pollution. Finally, our results provide local watershed managers and stakeholders with information to mitigate the burden of ARGs and fecal bacteria in urban streams.
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spelling doaj.art-a5f2a5c587df42b58dcb91cfad4b1d8a2023-11-23T17:53:30ZengMDPI AGMicroorganisms2076-26072022-09-01109180410.3390/microorganisms10091804Sources and Drivers of ARGs in Urban Streams in Atlanta, Georgia, USARobert A. Sowah0Marirosa Molina1Ourania Georgacopoulos2Blake Snyder3Mike Cyterski4Oak Ridge Institute for Science and Education, Oak Ridge, TN 37831, USAU.S. EPA, Office of Research and Development, Center for Environmental Measurement and Modeling, 109 T. W. Alexander Drive, Durham, NC 27709, USAStudent Services Contractor to the U.S. EPA, Office of Research and Development, Center for Environmental Measurement and Modeling, 960 College Station Rd., Athens, GA 30605, USAU.S. EPA, Laboratory of Services & Applied Sciences Division, 980 College Station Rd., Athens, GA 30605, USAU.S. EPA, Office of Research and Development, Center for Environmental Measurement and Modeling, 960 College Station Rd., Athens, GA 30605, USAThe spread of antibiotic resistance genes (ARGs) in the aquatic environment is an emerging concern in the interest of protecting public health. Stemming the environmental dissemination of ARGs will require a better understanding of the sources and drivers of ARGs in the water environment. In this study, we used direct measurement of sewage-associated molecular markers, the class 1 integron gene, standard water quality parameters, and watershed characteristics to evaluate the sources and drivers of ARGs in an urban watershed impacted by a gradient of human activities. Quantitative polymerase chain reaction (qPCR) was used to quantify the abundance of the sewage-associated HF183, the <i>E</i>. <i>coli</i> fecal indicator, class 1 integron gene (<i>int</i>1), and the ARGs <i>sulI</i>, <i>sulII</i>, <i>tet</i>W, <i>tet</i>M, <i>ampC,</i> and <i>bla</i>SHV in stream water samples collected from the Proctor Creek watershed in Atlanta, Georgia. Our findings show that ARGs were widely distributed, with detection frequencies of 96% (<i>sulI</i> and <i>sulII</i>), 82% (<i>tet</i>W and <i>tet</i>M), and 49% (<i>ampC</i> and <i>bla</i>SHV). All the ARGs were positively and significantly correlated (<i>r</i> > 0.5) with the HF183 and <i>E</i>. <i>coli</i> markers. Non-linear machine learning models developed using generalized boosting show that more than 70% of the variation in ARG loads in the watershed could be explained by fecal source loading, with other factors such as class 1 integron, which is associated with acquired antibiotic resistance, and environmental factors contributing < 30% to ARG variation. These results suggest that input from fecal sources is a more critical driver of ARG dissemination than environmental stressors or horizontal gene transfer in aquatic environments highly impacted by anthropogenic pollution. Finally, our results provide local watershed managers and stakeholders with information to mitigate the burden of ARGs and fecal bacteria in urban streams.https://www.mdpi.com/2076-2607/10/9/1804antibiotic resistanceurban streamswaterborne pathogensfecal indicator bacteria
spellingShingle Robert A. Sowah
Marirosa Molina
Ourania Georgacopoulos
Blake Snyder
Mike Cyterski
Sources and Drivers of ARGs in Urban Streams in Atlanta, Georgia, USA
Microorganisms
antibiotic resistance
urban streams
waterborne pathogens
fecal indicator bacteria
title Sources and Drivers of ARGs in Urban Streams in Atlanta, Georgia, USA
title_full Sources and Drivers of ARGs in Urban Streams in Atlanta, Georgia, USA
title_fullStr Sources and Drivers of ARGs in Urban Streams in Atlanta, Georgia, USA
title_full_unstemmed Sources and Drivers of ARGs in Urban Streams in Atlanta, Georgia, USA
title_short Sources and Drivers of ARGs in Urban Streams in Atlanta, Georgia, USA
title_sort sources and drivers of args in urban streams in atlanta georgia usa
topic antibiotic resistance
urban streams
waterborne pathogens
fecal indicator bacteria
url https://www.mdpi.com/2076-2607/10/9/1804
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