{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,12]],"date-time":"2026-09-12T06:28:01Z","timestamp":1789194481824,"version":"build-2803163510"},"reference-count":40,"publisher":"MDPI AG","issue":"19","license":[{"start":{"date-parts":[[2019,10,7]],"date-time":"2019-10-07T00:00:00Z","timestamp":1570406400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100007917","name":"Agricultural Research Service","doi-asserted-by":"publisher","award":["6040-32000-009-00-D"],"award-info":[{"award-number":["6040-32000-009-00-D"]}],"id":[{"id":"10.13039\/100007917","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000030","name":"Centers for Disease Control and Prevention","doi-asserted-by":"publisher","award":["Broad Agency Announcement to address antibiotic resistance, Agricultural Research Service Sub-Project Number: 6040-32000-009-08-R"],"award-info":[{"award-number":["Broad Agency Announcement to address antibiotic resistance, Agricultural Research Service Sub-Project Number: 6040-32000-009-08-R"]}],"id":[{"id":"10.13039\/100000030","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>In order to determine the role of surface water in the development and spread of antibiotic-resistant (AR) bacteria, water samples were collected quarterly from 2015 to 2016 from a mixed-use watershed in Georgia. In our previous study, 496 Escherichia coli were isolated from surface water, out of which, 34 isolates were resistant to antimicrobials. For the current study, these 34 AR E. coli were characterized using pulsed-field gel electrophoresis, AR gene detection, plasmid replicon typing, class I integron detection, and multi-locus sequence typing. Genes were identified as conferring resistance to azithromycin (mph(A)); \u03b2-lactams (blaCMY, blaCTX, blaTEM); chloramphenicol (floR); streptomycin (strA, strB); sulfisoxazole (sul1, sul2); tetracycline (tetA, tetB, tetC); and trimethoprim\/sulfamethoxazole (dhfr5, dhfr12). Five ciprofloxacin- and\/or nalidixic-resistant isolates contained point mutations in gyrA and\/or parC. Most of the isolates (n = 28) carried plasmids and three were positive for class I integrons. Twenty-nine sequence types (ST) were detected, including three epidemic urinary-tract-infection-associated ST131 isolates. One of the ST131 E. coli isolates exhibited an extended-spectrum \u03b2-lactamase (ESBL) phenotype and carried blaCTX-M-15 and blaTEM-1. To our knowledge, this is the first study on the emergence of an ESBL-producing E. coli ST131 from environmental water in the USA, which poses a potential risk to human health through the recreational, agricultural, or municipal use of this natural resource. This study identified E. coli with AR mechanisms to commonly used antimicrobials and carrying mobile genetic elements, which could transfer AR genes to other bacteria in the aquatic environment.<\/jats:p>","DOI":"10.3390\/ijerph16193761","type":"journal-article","created":{"date-parts":[[2019,10,7]],"date-time":"2019-10-07T10:05:12Z","timestamp":1570442712000},"page":"3761","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":25,"title":["Genetic Characterization of Antimicrobial-Resistant Escherichia coli Isolated from a Mixed-Use Watershed in Northeast Georgia, USA"],"prefix":"10.3390","volume":"16","author":[{"given":"Sohyun","family":"Cho","sequence":"first","affiliation":[{"name":"Department of Microbiology, University of Georgia, Athens, GA 30602, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hoang Anh Thi","family":"Nguyen","sequence":"additional","affiliation":[{"name":"Department of Microbiology, University of Georgia, Athens, GA 30602, USA"},{"name":"(Present) Houston Methodist Research Institute, Houston, TX 77030, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jacob M.","family":"McDonald","sequence":"additional","affiliation":[{"name":"Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA"},{"name":"Southeast Coast Network, National Park Service, Athens, GA 30605, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tiffanie A.","family":"Woodley","sequence":"additional","affiliation":[{"name":"Bacterial Epidemiology and Antimicrobial Resistance Research Unit, United States Department of Agriculture, Agricultural Research Service, U.S. National Poultry Research Center, Athens, GA 30605, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lari M.","family":"Hiott","sequence":"additional","affiliation":[{"name":"Bacterial Epidemiology and Antimicrobial Resistance Research Unit, United States Department of Agriculture, Agricultural Research Service, U.S. National Poultry Research Center, Athens, GA 30605, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John B.","family":"Barrett","sequence":"additional","affiliation":[{"name":"Bacterial Epidemiology and Antimicrobial Resistance Research Unit, United States Department of Agriculture, Agricultural Research Service, U.S. National Poultry Research Center, Athens, GA 30605, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Charlene R.","family":"Jackson","sequence":"additional","affiliation":[{"name":"Bacterial Epidemiology and Antimicrobial Resistance Research Unit, United States Department of Agriculture, Agricultural Research Service, U.S. National Poultry Research Center, Athens, GA 30605, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8500-3395","authenticated-orcid":false,"given":"Jonathan G.","family":"Frye","sequence":"additional","affiliation":[{"name":"Bacterial Epidemiology and Antimicrobial Resistance Research Unit, United States Department of Agriculture, Agricultural Research Service, U.S. National Poultry Research Center, Athens, GA 30605, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,10,7]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1177\/2042098614554919","article-title":"Antimicrobial resistance: Risk associated with antibiotic overuse and initiatives to reduce the problem","volume":"5","author":"Llor","year":"2014","journal-title":"Adv. Drug Saf."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1016\/j.ijmm.2005.07.002","article-title":"Antimicrobial resistance of Escherichia coli and therapeutic implications","volume":"295","author":"Marre","year":"2005","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1093\/trstmh\/trw048","article-title":"Antibiotic resistance is the quintessential One Health issue","volume":"110","author":"Robinson","year":"2016","journal-title":"Trans. R Soc. Trop. Med. Hyg."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"704","DOI":"10.1093\/cid\/cit355","article-title":"The scourge of antibiotic resistance: The important role of the environment","volume":"57","author":"Finley","year":"2013","journal-title":"Clin. Infect. Dis."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Cho, S., Hiott, L.M., Barrett, J.B., McMillan, E.A., House, S.L., Humayoun, S.B., Adams, E.S., Jackson, C.R., and Frye, J.G. (2018). Prevalence and characterization of Escherichia coli isolated from the Upper Oconee Watershed in Northeast Georgia. Plos ONE, 13.","DOI":"10.1371\/journal.pone.0197005"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"3156","DOI":"10.1128\/AAC.46.10.3156-3163.2002","article-title":"\u03b2-Lactamases in Ampicillin-Resistant Escherichia coli Isolates from Foods, Humans, and Healthy Animals","volume":"46","author":"Brinas","year":"2002","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1128\/AEM.70.1.1-7.2004","article-title":"Characterization of Multiple-Antimicrobial-Resistant Salmonella Serovars Isolated from Retail Meats","volume":"70","author":"Chen","year":"2004","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1006\/mcpr.2001.0363","article-title":"Multiplex PCR for the detection of tetracycline resistant genes","volume":"15","author":"Ng","year":"2001","journal-title":"Mol. Cell Probes"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"3214","DOI":"10.1128\/AAC.47.10.3214-3221.2003","article-title":"Antimicrobial Resistance Genes in Enterotoxigenic Escherichia coli O149:K91 Isolates Obtained over a 23-Year Period from Pigs","volume":"47","author":"Maynard","year":"2003","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1093\/jac\/dkh070","article-title":"Antibiotic resistance genes, integrons and multiple antibiotic resistance in thirty-five serotypes of Salmonella enterica isolated from humans and animals in the UK","volume":"53","author":"Randall","year":"2004","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1227","DOI":"10.1007\/s10482-015-0577-1","article-title":"Characterization of antimicrobial resistance in Salmonella enterica strains isolated from Brazilian poultry production","volume":"108","author":"Mattiello","year":"2015","journal-title":"Antonie Leeuwenhoek"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1648","DOI":"10.3201\/eid1510.090696","article-title":"Escherichia coli as reservoir for macrolide resistance genes","volume":"15","author":"Woerther","year":"2009","journal-title":"Emerg. Infect. Dis."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2661","DOI":"10.1128\/AAC.42.10.2661","article-title":"Tenover, gyrA Mutations Associated with Fluoroquinolone Resistance in Eight Species of Enterobacteriaceae","volume":"42","author":"Linda","year":"1998","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"3222","DOI":"10.1128\/AAC.47.10.3222-3232.2003","article-title":"Mutation Rate and Evolution of Fluoroquinolone Resistance in Escherichia coli Isolates from Patients with Urinary Tract Infections","volume":"47","author":"Karlsson","year":"2003","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_15","unstructured":"CLSI (2016). Performance Standards for Antimicrobial Susceptibility Testing, Clinical Laboratory Standards Institute. [26th ed.]. CLSI Supplement M100S."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1089\/fpd.2006.3.59","article-title":"Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet","volume":"3","author":"Ribot","year":"2006","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"2233","DOI":"10.1128\/jcm.33.9.2233-2239.1995","article-title":"Interpreting chromosomal DNA restriction patterns produced by PFGE","volume":"33","author":"Tenover","year":"1995","journal-title":"J. Clin. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"5860","DOI":"10.1128\/JCM.43.12.5860-5864.2005","article-title":"Analysis of a uropathogenic Escherichia coli clonal group by multilocus sequence typing","volume":"43","author":"Tartof","year":"2005","journal-title":"J. Clin. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1355","DOI":"10.1128\/JCM.06094-11","article-title":"Multilocus sequence typing of total-genome-sequenced bacteria","volume":"50","author":"Larsen","year":"2012","journal-title":"J. Clin. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1093\/jac\/dki439","article-title":"Genetic relatedness of a rarely isolated Salmonella: Salmonella enterica serotype Niakhar from NARMS animal isolates","volume":"57","author":"Tankson","year":"2006","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1128\/AEM.01445-06","article-title":"Occurrence of virulence and antimicrobial resistance genes in Escherichia coli isolates from different aquatic ecosystems within the St. Clair River and Detroit River areas","volume":"73","author":"Hamelin","year":"2007","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1016\/j.scitotenv.2015.03.095","article-title":"Antimicrobial resistance determinants of Escherichia coli isolates recovered from some rivers in Osun State, South-Western Nigeria: Implications for public health","volume":"523","author":"Titilawo","year":"2015","journal-title":"Sci. Total Environ."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"4200","DOI":"10.1128\/AEM.00137-06","article-title":"A virulence and antimicrobial resistance DNA microarray detects a high frequency of virulence genes in Escherichia coli isolates from Great Lakes recreational waters","volume":"72","author":"Hamelin","year":"2006","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1016\/j.ijantimicag.2005.02.006","article-title":"Mechanisms of quinolone resistance in Escherichia coli and Salmonella: Recent developments","volume":"25","author":"Hopkins","year":"2005","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1128\/CMR.00125-13","article-title":"Escherichia coli ST131, an intriguing clonal group","volume":"27","author":"Bertrand","year":"2014","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"466","DOI":"10.1016\/j.mib.2006.08.011","article-title":"The CTX-M beta-lactamase pandemic","volume":"9","author":"Canton","year":"2006","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1128\/CMR.00036-08","article-title":"AmpC beta-lactamases","volume":"22","author":"Jacoby","year":"2009","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"E238","DOI":"10.1111\/1469-0691.12128","article-title":"IncI1 plasmids associated with the spread of CMY-2, CTX-M-1 and SHV-12 in Escherichia coli of animal and human origin","volume":"19","author":"Accogli","year":"2013","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1089\/mdr.2013.0224","article-title":"IncI1 plasmids carrying bla(CTX-M-1) or bla(CMY-2) genes in Escherichia coli from healthy humans and animals in Tunisia","volume":"20","author":"Jouini","year":"2014","journal-title":"Microb. Drug Resist."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1235","DOI":"10.1089\/fpd.2009.0294","article-title":"Genetic and phenotypic characterization of the bla(CMY) gene from Escherichia coli and Salmonella enterica isolated from food-producing animals, humans, the environment, and retail meat","volume":"6","author":"Heider","year":"2009","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"448","DOI":"10.1016\/j.vetmic.2014.03.007","article-title":"Prevalence and characteristics of ESBL-producing E. coli in Dutch recreational waters influenced by wastewater treatment plants","volume":"171","author":"Blaak","year":"2014","journal-title":"Vet. Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1016\/j.watres.2016.08.015","article-title":"Free water surface constructed wetlands limit the dissemination of extended-spectrum beta-lactamase producing Escherichia coli in the natural environment","volume":"104","author":"Vivant","year":"2016","journal-title":"Water Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1051\/vetres:2001122","article-title":"Importance of integrons in the diffusion of resistance","volume":"32","author":"Carattoli","year":"2001","journal-title":"Vet. Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1089\/fpd.2011.0961","article-title":"Associations between multidrug resistance, plasmid content, and virulence potential among extraintestinal pathogenic and commensal Escherichia coli from humans and poultry","volume":"9","author":"Johnson","year":"2012","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"5095","DOI":"10.1128\/JB.00152-08","article-title":"The evolution of class 1 integrons and the rise of antibiotic resistance","volume":"190","author":"Gillings","year":"2008","journal-title":"J. Bacteriol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"822","DOI":"10.3201\/eid0907.020529","article-title":"Antimicrobial Resistance Markers of Class 1 and Class 2 Integron-bearing Escherichia coli from Irrigation Water and Sediments","volume":"9","author":"Roe","year":"2003","journal-title":"Emerg. Infect. Dis."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1111\/j.1574-6941.2009.00655.x","article-title":"Occurrence of antibiotic resistance and class 1, 2 and 3 integrons in Escherichia coli isolated from a densely populated estuary (Seine, France)","volume":"68","author":"Laroche","year":"2009","journal-title":"FEMS Microbiol. Ecol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"96","DOI":"10.1016\/j.ecoenv.2013.01.014","article-title":"Antibiotic resistant Escherichia coli in hospital and municipal sewage and their emission to the environment","volume":"91","author":"Korzeniewska","year":"2013","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Agga, G.E., Arthur, T.M., Durso, L.M., Harhay, D.M., and Schmidt, J.W. (2015). Antimicrobial-Resistant Bacterial Populations and Antimicrobial Resistance Genes Obtained from Environments Impacted by Livestock and Municipal Waste. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0132586"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"840","DOI":"10.1007\/s00248-015-0678-4","article-title":"Patterns of Multi-Antibiotic-Resistant Escherichia Coli from Streams with No History of Antimicrobial Inputs","volume":"72","author":"McArthur","year":"2016","journal-title":"Microb. Ecol."}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/16\/19\/3761\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:28:00Z","timestamp":1760189280000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/16\/19\/3761"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,10,7]]},"references-count":40,"journal-issue":{"issue":"19","published-online":{"date-parts":[[2019,10]]}},"alternative-id":["ijerph16193761"],"URL":"https:\/\/doi.org\/10.3390\/ijerph16193761","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,10,7]]}}}