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Metagenomic community composition and resistome analysis in a full-scale cold climate wastewater treatment plant

BACKGROUND: Wastewater treatment plants are an essential part of maintaining the health and safety of the general public. However, they are also an anthropogenic source of antibiotic resistance genes. In this study, we characterized the resistome, the distribution of classes 1–3 integron-integrase g...

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Autores principales: Jankowski, Paul, Gan, Jaydon, Le, Tri, McKennitt, Michaela, Garcia, Audrey, Yanaç, Kadir, Yuan, Qiuyan, Uyaguari-Diaz, Miguel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8760730/
https://www.ncbi.nlm.nih.gov/pubmed/35033203
http://dx.doi.org/10.1186/s40793-022-00398-1
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author Jankowski, Paul
Gan, Jaydon
Le, Tri
McKennitt, Michaela
Garcia, Audrey
Yanaç, Kadir
Yuan, Qiuyan
Uyaguari-Diaz, Miguel
author_facet Jankowski, Paul
Gan, Jaydon
Le, Tri
McKennitt, Michaela
Garcia, Audrey
Yanaç, Kadir
Yuan, Qiuyan
Uyaguari-Diaz, Miguel
author_sort Jankowski, Paul
collection PubMed
description BACKGROUND: Wastewater treatment plants are an essential part of maintaining the health and safety of the general public. However, they are also an anthropogenic source of antibiotic resistance genes. In this study, we characterized the resistome, the distribution of classes 1–3 integron-integrase genes (intI1, intI2, and intI3) as mobile genetic element biomarkers, and the bacterial and phage community compositions in the North End Sewage Treatment Plant in Winnipeg, Manitoba. Samples were collected from raw sewage, returned activated sludge, final effluent, and dewatered sludge. A total of 28 bacterial and viral metagenomes were sequenced over two seasons, fall and winter. Integron-integrase genes, the 16S rRNA gene, and the coliform beta-glucuronidase gene were also quantified during this time period. RESULTS: Bacterial classes observed above 1% relative abundance in all treatments were Actinobacteria (39.24% ± 0.25%), Beta-proteobacteria (23.99% ± 0.16%), Gamma-proteobacteria (11.06% ± 0.09%), and Alpha-proteobacteria (9.18 ± 0.04%). Families within the Caudovirales order: Siphoviridae (48.69% ± 0.10%), Podoviridae (23.99% ± 0.07%), and Myoviridae (19.94% ± 0.09%) were the dominant phage observed throughout the NESTP. The most abundant bacterial genera (in terms of average percent relative abundance) in influent, returned activated sludge, final effluent, and sludge, respectively, includes Mycobacterium (37.4%, 18.3%, 46.1%, and 7.7%), Acidovorax (8.9%, 10.8%, 5.4%, and 1.3%), and Polaromonas (2.5%, 3.3%, 1.4%, and 0.4%). The most abundant class of antibiotic resistance in bacterial samples was tetracycline resistance (17.86% ± 0.03%) followed by peptide antibiotics (14.24% ± 0.03%), and macrolides (10.63% ± 0.02%). Similarly, the phage samples contained a higher prevalence of macrolide (30.12% ± 0.30%), peptide antibiotic (10.78% ± 0.13%), and tetracycline (8.69% ± 0.11%) resistance. In addition, intI1 was the most abundant integron-integrase gene throughout treatment (1.14 × 10(4) gene copies/mL) followed by intI3 (4.97 × 10(3) gene copies/mL) while intI2 abundance remained low (6.4 × 10(1) gene copies/mL). CONCLUSIONS: Wastewater treatment successfully reduced the abundance of bacteria, DNA phage and antibiotic resistance genes although many antibiotic resistance genes remained in effluent and biosolids. The presence of integron-integrase genes throughout treatment and in effluent suggests that antibiotic resistance genes could be actively disseminating resistance between both environmental and pathogenic bacteria. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-022-00398-1.
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spelling pubmed-87607302022-01-18 Metagenomic community composition and resistome analysis in a full-scale cold climate wastewater treatment plant Jankowski, Paul Gan, Jaydon Le, Tri McKennitt, Michaela Garcia, Audrey Yanaç, Kadir Yuan, Qiuyan Uyaguari-Diaz, Miguel Environ Microbiome Research Article BACKGROUND: Wastewater treatment plants are an essential part of maintaining the health and safety of the general public. However, they are also an anthropogenic source of antibiotic resistance genes. In this study, we characterized the resistome, the distribution of classes 1–3 integron-integrase genes (intI1, intI2, and intI3) as mobile genetic element biomarkers, and the bacterial and phage community compositions in the North End Sewage Treatment Plant in Winnipeg, Manitoba. Samples were collected from raw sewage, returned activated sludge, final effluent, and dewatered sludge. A total of 28 bacterial and viral metagenomes were sequenced over two seasons, fall and winter. Integron-integrase genes, the 16S rRNA gene, and the coliform beta-glucuronidase gene were also quantified during this time period. RESULTS: Bacterial classes observed above 1% relative abundance in all treatments were Actinobacteria (39.24% ± 0.25%), Beta-proteobacteria (23.99% ± 0.16%), Gamma-proteobacteria (11.06% ± 0.09%), and Alpha-proteobacteria (9.18 ± 0.04%). Families within the Caudovirales order: Siphoviridae (48.69% ± 0.10%), Podoviridae (23.99% ± 0.07%), and Myoviridae (19.94% ± 0.09%) were the dominant phage observed throughout the NESTP. The most abundant bacterial genera (in terms of average percent relative abundance) in influent, returned activated sludge, final effluent, and sludge, respectively, includes Mycobacterium (37.4%, 18.3%, 46.1%, and 7.7%), Acidovorax (8.9%, 10.8%, 5.4%, and 1.3%), and Polaromonas (2.5%, 3.3%, 1.4%, and 0.4%). The most abundant class of antibiotic resistance in bacterial samples was tetracycline resistance (17.86% ± 0.03%) followed by peptide antibiotics (14.24% ± 0.03%), and macrolides (10.63% ± 0.02%). Similarly, the phage samples contained a higher prevalence of macrolide (30.12% ± 0.30%), peptide antibiotic (10.78% ± 0.13%), and tetracycline (8.69% ± 0.11%) resistance. In addition, intI1 was the most abundant integron-integrase gene throughout treatment (1.14 × 10(4) gene copies/mL) followed by intI3 (4.97 × 10(3) gene copies/mL) while intI2 abundance remained low (6.4 × 10(1) gene copies/mL). CONCLUSIONS: Wastewater treatment successfully reduced the abundance of bacteria, DNA phage and antibiotic resistance genes although many antibiotic resistance genes remained in effluent and biosolids. The presence of integron-integrase genes throughout treatment and in effluent suggests that antibiotic resistance genes could be actively disseminating resistance between both environmental and pathogenic bacteria. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-022-00398-1. BioMed Central 2022-01-15 /pmc/articles/PMC8760730/ /pubmed/35033203 http://dx.doi.org/10.1186/s40793-022-00398-1 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Jankowski, Paul
Gan, Jaydon
Le, Tri
McKennitt, Michaela
Garcia, Audrey
Yanaç, Kadir
Yuan, Qiuyan
Uyaguari-Diaz, Miguel
Metagenomic community composition and resistome analysis in a full-scale cold climate wastewater treatment plant
title Metagenomic community composition and resistome analysis in a full-scale cold climate wastewater treatment plant
title_full Metagenomic community composition and resistome analysis in a full-scale cold climate wastewater treatment plant
title_fullStr Metagenomic community composition and resistome analysis in a full-scale cold climate wastewater treatment plant
title_full_unstemmed Metagenomic community composition and resistome analysis in a full-scale cold climate wastewater treatment plant
title_short Metagenomic community composition and resistome analysis in a full-scale cold climate wastewater treatment plant
title_sort metagenomic community composition and resistome analysis in a full-scale cold climate wastewater treatment plant
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8760730/
https://www.ncbi.nlm.nih.gov/pubmed/35033203
http://dx.doi.org/10.1186/s40793-022-00398-1
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