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Characterization of Environmental and Cultivable Antibiotic- Resistant Microbial Communities Associated with Wastewater Treatment

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Characterization of Environmental and Cultivable Antibiotic- Resistant Microbial Communities Associated with Wastewater Treatment antibiotics Article Characterization of Environmental and Cultivable Antibiotic- Resistant Microbial Communities Associated with Wastewater Treatment Alicia Sorgen 1, James Johnson 2, Kevin Lambirth 2, Sandra M. Clinton 3 , Molly Redmond 1 , Anthony Fodor 2 and Cynthia Gibas 2,* 1 Department of Biological Sciences, University of North Carolina at Charlotte, Charlotte, NC 28223, USA; [email protected] (A.S.); [email protected] (M.R.) 2 Department of Bioinformatics and Genomics, University of North Carolina at Charlotte, Charlotte, NC 28223, USA; [email protected] (J.J.); [email protected] (K.L.); [email protected] (A.F.) 3 Department of Geography & Earth Sciences, University of North Carolina at Charlotte, Charlotte, NC 28223, USA; [email protected] * Correspondence: [email protected]; Tel.: +1-704-687-8378 Abstract: Bacterial resistance to antibiotics is a growing global concern, threatening human and environmental health, particularly among urban populations. Wastewater treatment plants (WWTPs) are thought to be “hotspots” for antibiotic resistance dissemination. The conditions of WWTPs, in conjunction with the persistence of commonly used antibiotics, may favor the selection and transfer of resistance genes among bacterial populations. WWTPs provide an important ecological niche to examine the spread of antibiotic resistance. We used heterotrophic plate count methods to identify Citation: Sorgen, A.; Johnson, J.; phenotypically resistant cultivable portions of these bacterial communities and characterized the Lambirth, K.; Clinton, S.M.; composition of the culturable subset of these populations. Resistant taxa were more abundant in raw Redmond, M.; Fodor, A.; Gibas, C. sewage and wastewater before the biological aeration treatment stage. While some antibiotic-resistant Characterization of Environmental and Cultivable Antibiotic-Resistant bacteria (ARB) were detectable downstream of treated wastewater release, these organisms are not Microbial Communities Associated enriched relative to effluent-free upstream water, indicating efficient removal during treatment. with Wastewater Treatment. Combined culture-dependent and -independent analyses revealed a stark difference in community Antibiotics 2021, 10, 352. https:// composition between culturable fractions and the environmental source material, irrespective of doi.org/10.3390/antibiotics10040352 culturing conditions. Higher proportions of the environmental populations were recovered than predicted by the widely accepted 1% culturability paradigm. These results represent baseline Academic Editors: Luciana Migliore abundance and compositional data for ARB communities for reference in future studies addressing and Marco Maria D’Andrea the dissemination of antibiotic resistance associated with urban wastewater treatment ecosystems. Received: 2 March 2021 Keywords: culturability; antibiotic resistance; wastewater treatment Accepted: 22 March 2021 Published: 26 March 2021 Publisher’s Note: MDPI stays neutral 1. Introduction with regard to jurisdictional claims in published maps and institutional affil- Antibiotics are antimicrobial substances that can either kill or inhibit the growth and iations. replication of a bacterium [1]. Antibiotics have revolutionized the field of medicine; yet their increased use has exerted a selective pressure on susceptible bacteria, favoring the survival of antibiotic-resistant bacteria (ARB) and the proliferation of associated antibiotic resistance genes (ARGs) [2]. Some bacterial species are inherently resistant to certain antibiotics as a result of structural or functional characteristics [3,4]. Those not inherently resistant Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. can acquire resistance through mutations in chromosomal genes and via horizontal gene This article is an open access article transfer (HGT) furthering the development of resistance among previously susceptible distributed under the terms and organisms [5]. conditions of the Creative Commons Wastewater treatment plants (WWTP) are major sewage repositories that may receive Attribution (CC BY) license (https:// sewage from both residential and medical treatment facilities. The continuous inflow of pre- creativecommons.org/licenses/by/ existing ARB and antibiotic residues are important sources of resistance material [6,7]. The 4.0/). wastewater treatment process generally involves three stages of treatment where (1) large Antibiotics 2021, 10, 352. https://doi.org/10.3390/antibiotics10040352 https://www.mdpi.com/journal/antibiotics Antibiotics 2021, 10, x 2 of 20 Wastewater treatment plants (WWTP) are major sewage repositories that may re- ceive sewage from both residential and medical treatment facilities. The continuous in- Antibiotics 2021, 10, 352 flow of pre-existing ARB and antibiotic residues are important sources of resistance2 ofma- 19 terial [6,7]. The wastewater treatment process generally involves three stages of treatment where (1) large solids are removed through physical processes before (2) entering a sedi- solidsmentation are removed tank in which through remaining physical processessuspended before solids (2) sink entering to form a sedimentation activated sludge tank and in whichwhere remainingbiological suspendedand chemical solids processes sink to are form employed activated to sludge remove and organic where matter biological [6]. andAny chemicaladditional processes organic areor chemical employed components to remove organic are removed matter using [6]. Any (3) additionaladditional organic treatment or chemicalprocesses components such as chemical are removed and biological-chemical using (3) additional contact treatment filters processes [8,9]. Prior such to as environ- chemi- calmental and biological-chemicalrelease, wastewater contact undergoes filters a [disinf8,9]. Priorection to stage environmental to eliminate release, harmful wastewater bacteria undergoesin the effluent a disinfection [10]. WWTPs stage are to considered eliminate harmful “hotspots” bacteria for resi in thestance effluent dissemination [10]. WWTPs due are to consideredthe sub-inhibitory “hotspots” concentrations for resistance of dissemination antibiotic compounds due to the sub-inhibitoryand the favorable concentrations conditions ofthat antibiotic promote compounds HGT [11–13]. and Insight the favorable into ARB conditions community that trends promote throughout HGT [11 the–13 treatment]. Insight intoprocess ARB can community help us understand trends throughout the effect the of treatment released process treated canwastewater help us understand on natural themi- effectcrobial of communities released treated [11–13]. wastewater on natural microbial communities [11–13]. AreasAreas withwith limitedlimited waterwater treatmenttreatment infrastructureinfrastructure havehave beenbeen shownshown toto passpass humanhuman microbialmicrobial resistomesresistomes intointo thethe environmentenvironment viavia mobilemobile geneticgenetic elementselements (MGEs),(MGEs), suchsuch asas plasmids,plasmids, transposons,transposons, and and integrons integrons [14 ,15[14,]. Even15]. Even in locations in locations with innovative with innovative wastew- aterwastewater treatment treatment systems, systems, the degree the degree of contaminant of contaminant removal removal depends depends on the on particularthe partic- technologyular technology and operatingand operating parameters parameters used, used, whether whether it be UV,it be chlorine, UV, chlorine, or microfiltration or microfil- disinfectiontration disinfection methods methods [16]. [16]. InIn thisthis study,study, wewe sampledsampled sitessites alongalong WWTP-associatedWWTP-associated urbanurban streams.streams. WeWe sampled sampled streamstream locationslocations upstreamupstream (UP)(UP) andand downstreamdownstream (DS)(DS) ofof thethe treatedtreated wastewaterwastewater releaserelease pointpoint toto understandunderstand thethe overalloverall impactimpact ofof treatedtreated waterwater releaserelease onon thethe streamstream microbialmicrobial communitycommunity (Figure(Figure1 1).). Inside Inside the the WWTP, WWTP, we we sampled sampled untreated untreated sewage sewage influent influent and and the the effluenteffluent ofof eacheach treatmenttreatment stagestage toto identifyidentify whichwhich taxataxa areare introducedintroduced toto thethe WWTPWWTP viavia influentinfluent andand whetherwhether theythey areare subsequentlysubsequently completelycompletely removed.removed. SamplesSamples pulledpulled atat eacheach sitesite withinwithin the the stream stream environment environment and and within within the the WWTP WWTP (as (as described described in Lambirthin Lambirth et al., et 2018)al., 2018) were were characterized characterized using using 16S rRNA16S rRNA amplicon amplicon and and metagenomic metagenomic sequencing. sequencing. FigureFigure 1.1. SchematicSchematic ofof thethe wastewaterwastewater treatment process and sampling sites utilized for this study. study. RawRaw sewagesewage from residential (RES) (RES) and and hospital hospital (HOS) (HOS) sources sources are are routed routed to toa main a main sewer sewer line. line. The combined raw influent (INF) is then passed through a physical screen to filter out large solids. The combined raw influent (INF) is then passed through a physical screen to filter out large solids. The screen-filtered wastewater (PCI) undergoes primary clarification. The primary clarifier efflu- The screen-filtered wastewater (PCI) undergoes primary clarification. The primary
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