Metagenomic analysis unveils the underexplored roles of prokaryotic viruses in a full-scale landfill leachate treatment plant

Tianyi Chen; Chunfang Deng; Zongzhi Wu; Tang Liu; Yuanyan Zhang; Xuming Xu; Xiaohui Zhao; Jiarui Li; Shaoyang Li; Nan Xu; Ke Yu

doi:10.1016/j.watres.2023.120611

Metagenomic analysis unveils the underexplored roles of prokaryotic viruses in a full-scale landfill leachate treatment plant

Water Res. 2023 Oct 15:245:120611. doi: 10.1016/j.watres.2023.120611. Epub 2023 Sep 10.

Authors

Tianyi Chen¹, Chunfang Deng², Zongzhi Wu³, Tang Liu⁴, Yuanyan Zhang⁵, Xuming Xu⁶, Xiaohui Zhao³, Jiarui Li³, Shaoyang Li⁷, Nan Xu⁷, Ke Yu⁷

Affiliations

¹ Eco-environment and Resource Efficiency Research Laboratory, School of Environment and Energy, Peking University Shenzhen Graduate School, Shenzhen 518055, China; Environmental Microbiome and Innovative Genomics Laboratory, College of Environmental Sciences and Engineering, Peking University, Beijing 100871, China.
² Eco-environment and Resource Efficiency Research Laboratory, School of Environment and Energy, Peking University Shenzhen Graduate School, Shenzhen 518055, China; Environmental Microbiome and Innovative Genomics Laboratory, College of Environmental Sciences and Engineering, Peking University, Beijing 100871, China. Electronic address: dcf@pku.edu.cn.
³ Environmental Microbiome and Innovative Genomics Laboratory, College of Environmental Sciences and Engineering, Peking University, Beijing 100871, China.
⁴ Environmental Microbiome Engineering and Innovative Genomics Laboratory, College of Chemistry and Environmental Engineering, Shenzhen University, Shenzhen 518060, China.
⁵ Jiangxi Academy of Eco-Environmental Sciences & Planning, Nanchang 330029, China.
⁶ Department of Water Ecology and Environment, China Institute of Water Resources and Hydropower Research, Beijing 100038, China.
⁷ Eco-environment and Resource Efficiency Research Laboratory, School of Environment and Energy, Peking University Shenzhen Graduate School, Shenzhen 518055, China.

PMID: 37722141
DOI: 10.1016/j.watres.2023.120611

Abstract

Enormous viral populations have been identified in activated sludge systems, but their ecological and biochemical roles in landfill leachate treatment plants remain poorly understood. To address this knowledge gap, we conducted an in-depth analysis using 36 metagenomic datasets that we collected and sequenced during a half-year time-series sampling campaign at six sites in a full-scale landfill leachate treatment plant (LLTP), elucidating viral distribution, virus‒host dynamics, virus-encoded auxiliary metabolic genes (AMGs), and viral contributions to the spread of virulence and antibiotic resistance genes. Our findings demonstrated that viral and prokaryotic communities differed widely among different treatment units, with stability over time. LLTP viruses were linked to various prokaryotic hosts, spanning 35 bacterial phyla and one archaeal phylum, which included the core microbes involved in biological treatments, as well as some of the less well-characterized microbial dark matter phyla. By encoding 2364 auxiliary metabolic genes (AMGs), viruses harbored the potential to regulate microbial nucleotide metabolism, facilitate the biodegradation of complex organic matter, and enhance flocculation and settling in biological treatment plants. The abundance distribution of AMGs varied considerably across treatment units and showed a lifestyle-dependent pattern with temperate virus-associated AMGs exhibiting a higher average abundance in downstream biological treatment units and effluent water. Meanwhile, temperate viruses tended to carry a higher load of virulence factor genes (VFGs), antibiotic resistance genes (ARGs), and biotic and metal resistance genes (BMRGs), and engaged in more frequent gene exchanges with prokaryotes than lytic viruses, thus acting as a pivotal contributor to the dissemination of pathogenicity and resistance genes in downstream LLTP units. This study provided a comprehensive profile of viral and prokaryotic communities in the LLTP and unveiled the varying roles of different-lifestyle viruses in biochemical processes and water quality safety.

Keywords: Auxiliary metabolic genes; Environmental risk; Host; Landfill leachate treatment plant; Viral community.