Contaminant-degrading bacteria are super carriers of antibiotic resistance genes in municipal landfills: A metagenomics-based study

Municipal landfills are hotspot sources of antimicrobial resistance (AMR) and are also important habitats of contaminant-degrading bacteria. However, high diversity of antibiotic resistance genes (ARGs) in landfills hinders assessing AMR risks in the affected environment. More concerned, whether the...

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Main Authors: Fang-Zhou Gao, Wei-Li Jia, Bing Li, Min Zhang, Liang-Ying He, Hong Bai, You-Sheng Liu, Guang-Guo Ying
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Environment International
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Online Access:http://www.sciencedirect.com/science/article/pii/S0160412024008262
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author Fang-Zhou Gao
Wei-Li Jia
Bing Li
Min Zhang
Liang-Ying He
Hong Bai
You-Sheng Liu
Guang-Guo Ying
author_facet Fang-Zhou Gao
Wei-Li Jia
Bing Li
Min Zhang
Liang-Ying He
Hong Bai
You-Sheng Liu
Guang-Guo Ying
author_sort Fang-Zhou Gao
collection DOAJ
description Municipal landfills are hotspot sources of antimicrobial resistance (AMR) and are also important habitats of contaminant-degrading bacteria. However, high diversity of antibiotic resistance genes (ARGs) in landfills hinders assessing AMR risks in the affected environment. More concerned, whether there is co-selection or enrichment of antibiotic-resistant bacteria and contaminant-degrading bacteria in these extremely polluted environments is far less understood. Here, we collected metagenomic datasets of 32 raw leachate and 45 solid waste samples in 22 municipal landfills of China. The antibiotic resistome, antibiotic-resistant bacteria and contaminant-degrading bacteria were explored, and were then compared with other environmental types. Results showed that the antibiotic resistome in landfills contained 1,403 ARG subtypes, with the total abundance over the levels in natural environments and reaching the levels in human feces and sewage. Therein, 49 subtypes were listed as top priority ARGs for future surveillance based on the criteria of enrichment in landfills, mobilizable and present in pathogens. By comparing to those in less contaminated river environments, we elucidated an enrichment of antibiotic-resistant bacteria with contaminant-degrading potentials in landfills. Bacteria in Pseudomonadaceae, Moraxellaceae, Xanthomonadaceae and Enterobacteriaceae deserved the most concerns since 72.2 % of ARG hosts were classified to them. Klebsiella pneumoniae, Acinetobacter nosocomialis and Escherichia coli were abundant multidrug-resistant pathogenic species in raw leachate (∼10.2 % of total microbiomes), but they rarely carried contaminant-degradation genes. Notably, several bacterial genera belonging to Pseudomonadaceae had the most antibiotic-resistant, pathogenic, and contaminant-degrading potentials than other bacteria. Overall, the findings highlight environmental selection for contaminant-degrading antibiotic-resistant pathogens, and provide significant insights into AMR risks in municipal landfills.
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spelling doaj-art-7a7ab93549bf4447a6a4c5dce359a3342025-01-24T04:44:11ZengElsevierEnvironment International0160-41202025-01-01195109239Contaminant-degrading bacteria are super carriers of antibiotic resistance genes in municipal landfills: A metagenomics-based studyFang-Zhou Gao0Wei-Li Jia1Bing Li2Min Zhang3Liang-Ying He4Hong Bai5You-Sheng Liu6Guang-Guo Ying7SCNU Environmental Research Institute, Guangdong Provincial Key Laboratory of Chemical Pollution and Environmental Safety & MOE Key Laboratory of Theoretical Chemistry of Environment, South China Normal University, Guangzhou, China; School of Environment, South China Normal University, University Town, Guangzhou, ChinaSCNU Environmental Research Institute, Guangdong Provincial Key Laboratory of Chemical Pollution and Environmental Safety & MOE Key Laboratory of Theoretical Chemistry of Environment, South China Normal University, Guangzhou, China; School of Environment, South China Normal University, University Town, Guangzhou, ChinaInstitute of Environment and Ecology, Tsinghua Shenzhen International Graduate School, Tsinghua University, Shenzhen, ChinaSCNU Environmental Research Institute, Guangdong Provincial Key Laboratory of Chemical Pollution and Environmental Safety & MOE Key Laboratory of Theoretical Chemistry of Environment, South China Normal University, Guangzhou, China; School of Environment, South China Normal University, University Town, Guangzhou, China; Pearl River Water Resources Research Institute, Pearl River Water Resources Commission of the Ministry of Water Resources, Guangzhou, ChinaSCNU Environmental Research Institute, Guangdong Provincial Key Laboratory of Chemical Pollution and Environmental Safety & MOE Key Laboratory of Theoretical Chemistry of Environment, South China Normal University, Guangzhou, China; School of Environment, South China Normal University, University Town, Guangzhou, ChinaSCNU Environmental Research Institute, Guangdong Provincial Key Laboratory of Chemical Pollution and Environmental Safety & MOE Key Laboratory of Theoretical Chemistry of Environment, South China Normal University, Guangzhou, China; School of Environment, South China Normal University, University Town, Guangzhou, ChinaSCNU Environmental Research Institute, Guangdong Provincial Key Laboratory of Chemical Pollution and Environmental Safety & MOE Key Laboratory of Theoretical Chemistry of Environment, South China Normal University, Guangzhou, China; School of Environment, South China Normal University, University Town, Guangzhou, ChinaSCNU Environmental Research Institute, Guangdong Provincial Key Laboratory of Chemical Pollution and Environmental Safety & MOE Key Laboratory of Theoretical Chemistry of Environment, South China Normal University, Guangzhou, China; School of Environment, South China Normal University, University Town, Guangzhou, China; Corresponding author.Municipal landfills are hotspot sources of antimicrobial resistance (AMR) and are also important habitats of contaminant-degrading bacteria. However, high diversity of antibiotic resistance genes (ARGs) in landfills hinders assessing AMR risks in the affected environment. More concerned, whether there is co-selection or enrichment of antibiotic-resistant bacteria and contaminant-degrading bacteria in these extremely polluted environments is far less understood. Here, we collected metagenomic datasets of 32 raw leachate and 45 solid waste samples in 22 municipal landfills of China. The antibiotic resistome, antibiotic-resistant bacteria and contaminant-degrading bacteria were explored, and were then compared with other environmental types. Results showed that the antibiotic resistome in landfills contained 1,403 ARG subtypes, with the total abundance over the levels in natural environments and reaching the levels in human feces and sewage. Therein, 49 subtypes were listed as top priority ARGs for future surveillance based on the criteria of enrichment in landfills, mobilizable and present in pathogens. By comparing to those in less contaminated river environments, we elucidated an enrichment of antibiotic-resistant bacteria with contaminant-degrading potentials in landfills. Bacteria in Pseudomonadaceae, Moraxellaceae, Xanthomonadaceae and Enterobacteriaceae deserved the most concerns since 72.2 % of ARG hosts were classified to them. Klebsiella pneumoniae, Acinetobacter nosocomialis and Escherichia coli were abundant multidrug-resistant pathogenic species in raw leachate (∼10.2 % of total microbiomes), but they rarely carried contaminant-degradation genes. Notably, several bacterial genera belonging to Pseudomonadaceae had the most antibiotic-resistant, pathogenic, and contaminant-degrading potentials than other bacteria. Overall, the findings highlight environmental selection for contaminant-degrading antibiotic-resistant pathogens, and provide significant insights into AMR risks in municipal landfills.http://www.sciencedirect.com/science/article/pii/S0160412024008262Antibiotic resistanceMunicipal landfillAntibiotic-resistant pathogenRisk assessmentEnvironmental selectionMeta-analysis
spellingShingle Fang-Zhou Gao
Wei-Li Jia
Bing Li
Min Zhang
Liang-Ying He
Hong Bai
You-Sheng Liu
Guang-Guo Ying
Contaminant-degrading bacteria are super carriers of antibiotic resistance genes in municipal landfills: A metagenomics-based study
Environment International
Antibiotic resistance
Municipal landfill
Antibiotic-resistant pathogen
Risk assessment
Environmental selection
Meta-analysis
title Contaminant-degrading bacteria are super carriers of antibiotic resistance genes in municipal landfills: A metagenomics-based study
title_full Contaminant-degrading bacteria are super carriers of antibiotic resistance genes in municipal landfills: A metagenomics-based study
title_fullStr Contaminant-degrading bacteria are super carriers of antibiotic resistance genes in municipal landfills: A metagenomics-based study
title_full_unstemmed Contaminant-degrading bacteria are super carriers of antibiotic resistance genes in municipal landfills: A metagenomics-based study
title_short Contaminant-degrading bacteria are super carriers of antibiotic resistance genes in municipal landfills: A metagenomics-based study
title_sort contaminant degrading bacteria are super carriers of antibiotic resistance genes in municipal landfills a metagenomics based study
topic Antibiotic resistance
Municipal landfill
Antibiotic-resistant pathogen
Risk assessment
Environmental selection
Meta-analysis
url http://www.sciencedirect.com/science/article/pii/S0160412024008262
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