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

Fang-Zhou Gao; Wei-Li Jia; Bing Li; Min Zhang; Liang-Ying He; Hong Bai; You-Sheng Liu; Guang-Guo Ying

doi:10.1016/j.envint.2024.109239

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

Environ Int. 2024 Dec 25:195:109239. doi: 10.1016/j.envint.2024.109239. Online ahead of print.

Authors

Fang-Zhou Gao¹, Wei-Li Jia¹, Bing Li², Min Zhang³, Liang-Ying He¹, Hong Bai¹, You-Sheng Liu¹, Guang-Guo Ying⁴

Affiliations

¹ SCNU 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.
² Institute of Environment and Ecology, Tsinghua Shenzhen International Graduate School, Tsinghua University, Shenzhen, China.
³ SCNU 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, China.
⁴ SCNU 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. Electronic address: guangguo.ying@m.scnu.edu.cn.

PMID: 39729867
DOI: 10.1016/j.envint.2024.109239

Abstract

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.

Keywords: Antibiotic resistance; Antibiotic-resistant pathogen; Environmental selection; Meta-analysis; Municipal landfill; Risk assessment.