Characterization of Metagenomes in Urban Aquatic Compartments Reveals High Prevalence of Clinically Relevant Antibiotic Resistance Genes in Wastewaters
The dissemination of antimicrobial resistance (AMR) is an escalating problem and a threat to public health. Comparative metagenomics was used to investigate the occurrence of antibiotic resistant genes (ARGs) in wastewater and urban surface water environments in Singapore. Hospital and municipal was...
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Frontiers Media S.A.
2017-11-01
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Online Access: | http://journal.frontiersin.org/article/10.3389/fmicb.2017.02200/full |
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doaj-194b3736a271492ba9ca77f099513a62 |
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record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Charmaine Ng Martin Tay Boonfei Tan Thai-Hoang Le Laurence Haller Hongjie Chen Tse H. Koh Timothy M. S. Barkham Janelle R. Thompson Karina Y.-H. Gin Karina Y.-H. Gin |
spellingShingle |
Charmaine Ng Martin Tay Boonfei Tan Thai-Hoang Le Laurence Haller Hongjie Chen Tse H. Koh Timothy M. S. Barkham Janelle R. Thompson Karina Y.-H. Gin Karina Y.-H. Gin Characterization of Metagenomes in Urban Aquatic Compartments Reveals High Prevalence of Clinically Relevant Antibiotic Resistance Genes in Wastewaters Frontiers in Microbiology comparative metagenomics antibiotic resistant genes wastewaters hospital municipal water body |
author_facet |
Charmaine Ng Martin Tay Boonfei Tan Thai-Hoang Le Laurence Haller Hongjie Chen Tse H. Koh Timothy M. S. Barkham Janelle R. Thompson Karina Y.-H. Gin Karina Y.-H. Gin |
author_sort |
Charmaine Ng |
title |
Characterization of Metagenomes in Urban Aquatic Compartments Reveals High Prevalence of Clinically Relevant Antibiotic Resistance Genes in Wastewaters |
title_short |
Characterization of Metagenomes in Urban Aquatic Compartments Reveals High Prevalence of Clinically Relevant Antibiotic Resistance Genes in Wastewaters |
title_full |
Characterization of Metagenomes in Urban Aquatic Compartments Reveals High Prevalence of Clinically Relevant Antibiotic Resistance Genes in Wastewaters |
title_fullStr |
Characterization of Metagenomes in Urban Aquatic Compartments Reveals High Prevalence of Clinically Relevant Antibiotic Resistance Genes in Wastewaters |
title_full_unstemmed |
Characterization of Metagenomes in Urban Aquatic Compartments Reveals High Prevalence of Clinically Relevant Antibiotic Resistance Genes in Wastewaters |
title_sort |
characterization of metagenomes in urban aquatic compartments reveals high prevalence of clinically relevant antibiotic resistance genes in wastewaters |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Microbiology |
issn |
1664-302X |
publishDate |
2017-11-01 |
description |
The dissemination of antimicrobial resistance (AMR) is an escalating problem and a threat to public health. Comparative metagenomics was used to investigate the occurrence of antibiotic resistant genes (ARGs) in wastewater and urban surface water environments in Singapore. Hospital and municipal wastewater (n = 6) were found to have higher diversity and average abundance of ARGs (303 ARG subtypes, 197,816 x/Gb) compared to treated wastewater effluent (n = 2, 58 ARG subtypes, 2,692 x/Gb) and surface water (n = 5, 35 subtypes, 7,985 x/Gb). A cluster analysis showed that the taxonomic composition of wastewaters was highly similar and had a bacterial community composition enriched in gut bacteria (Bacteroides, Faecalibacterium, Bifidobacterium, Blautia, Roseburia, Ruminococcus), the Enterobacteriaceae group (Klebsiella, Aeromonas, Enterobacter) and opportunistic pathogens (Prevotella, Comamonas, Neisseria). Wastewater, treated effluents and surface waters had a shared resistome of 21 ARGs encoding multidrug resistant efflux pumps or resistance to aminoglycoside, macrolide-lincosamide-streptogramins (MLS), quinolones, sulfonamide, and tetracycline resistance which suggests that these genes are wide spread across different environments. Wastewater had a distinctively higher average abundance of clinically relevant, class A beta-lactamase resistant genes (i.e., blaKPC, blaCTX-M, blaSHV, blaTEM). The wastewaters from clinical isolation wards, in particular, had a exceedingly high levels of blaKPC-2 genes (142,200 x/Gb), encoding for carbapenem resistance. Assembled scaffolds (16 and 30 kbp) from isolation ward wastewater samples indicated this gene was located on a Tn3-based transposon (Tn4401), a mobilization element found in Klebsiella pneumonia plasmids. In the longer scaffold, transposable elements were flanked by a toxin–antitoxin (TA) system and other metal resistant genes that likely increase the persistence, fitness and propagation of the plasmid in the bacterial host under conditions of stress. A few bacterial species (Enterobacter cloacae, Klebsiella pneumoniae, Citrobacter freundii, Pseudomonas aeruginosa) that were cultured from the isolation ward wastewaters on CHROMagar media harbored the blaKPC-2 gene. This suggests that hospital wastewaters derived from clinical specialty wards are hotspots for the spread of AMR. Assembled scaffolds of other mobile genetic elements such as IncQ and IncF plasmids bearing quinolone resistance genes (qnrS1, qnrS2) and the class A beta-lactamase gene (blaTEM-1) were recovered in wastewater samples which may aid the transfer of AMR. |
topic |
comparative metagenomics antibiotic resistant genes wastewaters hospital municipal water body |
url |
http://journal.frontiersin.org/article/10.3389/fmicb.2017.02200/full |
work_keys_str_mv |
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doaj-194b3736a271492ba9ca77f099513a622020-11-24T20:46:22ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-11-01810.3389/fmicb.2017.02200298023Characterization of Metagenomes in Urban Aquatic Compartments Reveals High Prevalence of Clinically Relevant Antibiotic Resistance Genes in WastewatersCharmaine Ng0Martin Tay1Boonfei Tan2Thai-Hoang Le3Laurence Haller4Hongjie Chen5Tse H. Koh6Timothy M. S. Barkham7Janelle R. Thompson8Karina Y.-H. Gin9Karina Y.-H. Gin10Department of Civil and Environmental Engineering, National University of Singapore, Singapore, SingaporeCentre for Environmental Sensing and Modeling, Singapore-MIT Alliance for Research and Technology Centre, Singapore, SingaporeCentre for Environmental Sensing and Modeling, Singapore-MIT Alliance for Research and Technology Centre, Singapore, SingaporeDepartment of Environmental Engineering, Ho Chi Minh City International University, Ho Chi Minh City, VietnamDepartment of Civil and Environmental Engineering, National University of Singapore, Singapore, SingaporeDepartment of Civil and Environmental Engineering, National University of Singapore, Singapore, SingaporeDepartment of Pathology, Singapore General Hospital, Singapore, SingaporeDepartment of Laboratory Medicine, Tan Tock Seng Hospital, Singapore, SingaporeCentre for Environmental Sensing and Modeling, Singapore-MIT Alliance for Research and Technology Centre, Singapore, SingaporeDepartment of Civil and Environmental Engineering, National University of Singapore, Singapore, SingaporeNUS Environmental Research Institute, National University of Singapore, Singapore, SingaporeThe dissemination of antimicrobial resistance (AMR) is an escalating problem and a threat to public health. Comparative metagenomics was used to investigate the occurrence of antibiotic resistant genes (ARGs) in wastewater and urban surface water environments in Singapore. Hospital and municipal wastewater (n = 6) were found to have higher diversity and average abundance of ARGs (303 ARG subtypes, 197,816 x/Gb) compared to treated wastewater effluent (n = 2, 58 ARG subtypes, 2,692 x/Gb) and surface water (n = 5, 35 subtypes, 7,985 x/Gb). A cluster analysis showed that the taxonomic composition of wastewaters was highly similar and had a bacterial community composition enriched in gut bacteria (Bacteroides, Faecalibacterium, Bifidobacterium, Blautia, Roseburia, Ruminococcus), the Enterobacteriaceae group (Klebsiella, Aeromonas, Enterobacter) and opportunistic pathogens (Prevotella, Comamonas, Neisseria). Wastewater, treated effluents and surface waters had a shared resistome of 21 ARGs encoding multidrug resistant efflux pumps or resistance to aminoglycoside, macrolide-lincosamide-streptogramins (MLS), quinolones, sulfonamide, and tetracycline resistance which suggests that these genes are wide spread across different environments. Wastewater had a distinctively higher average abundance of clinically relevant, class A beta-lactamase resistant genes (i.e., blaKPC, blaCTX-M, blaSHV, blaTEM). The wastewaters from clinical isolation wards, in particular, had a exceedingly high levels of blaKPC-2 genes (142,200 x/Gb), encoding for carbapenem resistance. Assembled scaffolds (16 and 30 kbp) from isolation ward wastewater samples indicated this gene was located on a Tn3-based transposon (Tn4401), a mobilization element found in Klebsiella pneumonia plasmids. In the longer scaffold, transposable elements were flanked by a toxin–antitoxin (TA) system and other metal resistant genes that likely increase the persistence, fitness and propagation of the plasmid in the bacterial host under conditions of stress. A few bacterial species (Enterobacter cloacae, Klebsiella pneumoniae, Citrobacter freundii, Pseudomonas aeruginosa) that were cultured from the isolation ward wastewaters on CHROMagar media harbored the blaKPC-2 gene. This suggests that hospital wastewaters derived from clinical specialty wards are hotspots for the spread of AMR. Assembled scaffolds of other mobile genetic elements such as IncQ and IncF plasmids bearing quinolone resistance genes (qnrS1, qnrS2) and the class A beta-lactamase gene (blaTEM-1) were recovered in wastewater samples which may aid the transfer of AMR.http://journal.frontiersin.org/article/10.3389/fmicb.2017.02200/fullcomparative metagenomicsantibiotic resistant geneswastewatershospitalmunicipalwater body |