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Factors associated with elevated levels of antibiotic resistance genes in sewer sediments and wastewater.

ABSTRACT: The sewer environment is a potential hotspot for the proliferation of antibiotic resistance genes (ARGs) and other hazardous microbial agents. Understanding the potential for ARG proliferation and retardation and/or accumulation in sewer sediments is of interest for protecting the health of sewage workers and the broader community in the event of sewer overflows as well as for interpreting sewage epidemiology data. To better understand this understudied environment for antibiotic resistance, a field survey was conducted to identify the factors that may control ARGs in sewer sediments and sewage. qPCR was performed for select ARGs and amplicon sequencing was performed for paired samples from combined and separate sanitary sewer systems. Metagenomic sequencing was performed on combined sewer sediments. The relative abundances of sul1, tet(O), tet(W), ermF, and vanA were higher in wastewater compared to sewer sediments, while NDM-1 was greater in sewer sediment and ermF was similar between the two matrices. NDM-1 was observed in sewer sediment but rarely above detection in wastewater in this study. This may indicate that larger/more frequent wastewater samples are needed for detection and/or that retardation and/or accumulation in sewage sediment may need to be considered when interpreting wastewater-based epidemiology data for ARGs. Random forest analyses indicated that season and conductivity were important variables and to a lesser extent so were pH, TSS, heavy metals, and sewer type for explaining the variance of the ARGs. These variables explained the 19-61% of the variance of sul1, tet(O), tet(G), and tet(W) quantified in wastewater. These variables performed less well for explaining the variance in sewer sediments (0.2-24%). Sewer sediment and wastewater had distinct microbial community structures and biomarkers for each are described. Metagenomics indicated that a high diversity of ARGs, including several of medical importance, were observed in the combined sewer sediment. This work provides insight into the complex sewer microbiome and the potential hazard posed by different sewer matrices.

SUBMITTER: Alessia E

PROVIDER: S-EPMC8294613 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The entry of antibiotic resistance genes (ARGs) into aquatic systems has been documented for large municipal wastewater treatment plants (WWTPs), but there is less study of the impact of smaller plants that are situated on small rural rivers. We sampled water metagenomes for ARGs and taxa composition from the Kokosing River, a small rural river in Knox County, Ohio, which has been designated an Ohio State Scenic River for retention of natural character. Samples were obtained 1.0 km upstream, 120 m downstream, and 6.4 km downstream from the effluent release of the Mount Vernon WWTP. ARGs were identified in metagenomes using ShortBRED markers from the comprehensive antibiotic resistance database (CARD) screened against UniPROT. Through all seasons, the metagenome just downstream of the WWTP effluent showed a substantial elevation of at least 15 different ARGs, including 6 ARGs commonly associated with Acinetobacter baumannii, such as msrE, mphE (macrolide resistance), and tet(39) (tetracycline resistance). The ARGs most prevalent near the effluent pipe persisted 6.4 km downriver. Using metagenomic phylogenetic analysis (MetaPhlAn2) clade-specific marker genes, the taxa distribution near the effluent showed elevation of reads annotated as Acinetobacter species as well as gut-associated taxa, Bacteroides and Firmicutes. The ARG levels and taxa prevalence showed little dependence on seasonal chlorination of the effluent. Nitrogen and phosphorus were elevated near the effluent pipe but had no consistent correlation with ARG levels. We show that in a rural river microbiome, year-round wastewater effluent substantially elevates ARGs, including those associated with multidrug-resistant A. baumannii. IMPORTANCE Antibiotic resistance is a growing problem worldwide, with frequent transmission between pathogens and environmental organisms. Rural rivers can support high levels of recreational use by people unaware of inputs from treated wastewater, while wastewater treatment plants (WWTPs) can generate a small but significant portion of flow volume into a river surrounded by forest and agriculture. There is little information on the rural impacts of WWTP effluent on the delivery and transport of antibiotic resistance genes. In our study, the river water proximal to wastewater effluent shows evidence for the influx of multidrug-resistant Acinetobacter baumannii, an opportunistic pathogen of concern for hospitals but also widespread in natural environments. Our work highlights the importance of wastewater effluent in management of environmental antibiotic resistance, even in high quality, rural river systems.

Project description:Environments polluted by direct discharges of effluents from antibiotic manufacturing are important reservoirs for antibiotic resistance genes (ARGs), which could potentially be transferred to human pathogens. However, our knowledge about the identity and diversity of ARGs in such polluted environments remains limited. We applied functional metagenomics to explore the resistome of two Croatian antibiotic manufacturing effluents and sediments collected upstream of and at the effluent discharge sites. Metagenomic libraries built from an azithromycin-production site were screened for resistance to macrolide antibiotics, whereas the libraries from a site producing veterinary antibiotics were screened for resistance to sulfonamides, tetracyclines, trimethoprim, and beta-lactams. Functional analysis of eight libraries identified a total of 82 unique, often clinically relevant ARGs, which were frequently found in clusters and flanked by mobile genetic elements. The majority of macrolide resistance genes identified from matrices exposed to high levels of macrolides were similar to known genes encoding ribosomal protection proteins, macrolide phosphotransferases, and transporters. Potentially novel macrolide resistance genes included one most similar to a 23S rRNA methyltransferase from Clostridium and another, derived from upstream unpolluted sediment, to a GTPase HflX from Emergencia. In libraries deriving from sediments exposed to lower levels of veterinary antibiotics, we found 8 potentially novel ARGs, including dihydrofolate reductases and beta-lactamases from classes A, B, and D. In addition, we detected 7 potentially novel ARGs in upstream sediment, including thymidylate synthases, dihydrofolate reductases, and class D beta-lactamase. Taken together, in addition to finding known gene types, we report the discovery of novel and diverse ARGs in antibiotic-polluted industrial effluents and sediments, providing a qualitative basis for monitoring the dispersal of ARGs from environmental hotspots such as discharge sites of pharmaceutical effluents.

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Factors associated with elevated levels of antibiotic resistance genes in sewer sediments and wastewater.

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