Evidence of microbial reductive dehalogenation in deep-sea cold seeps and its implications for biogeochemical cycles

Abstract Background Reductive dehalogenation is crucial for halogen cycling and environmental remediation, yet its ecological role is not completely understood, especially in deep-sea environments. To address this gap, we investigated the diversity and expression of genes encoding reductive dehaloge...

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Main Authors: Yingchun Han, Zhaochao Deng, Yongyi Peng, Jiaxue Peng, Lei Cao, Yangru Xu, Yi Yang, Hao Zhou, Chen Zhang, Dongdong Zhang, Minxiao Wang, Chunfang Zhang, Chris Greening, Xiyang Dong
Format: Article
Language:English
Published: BMC 2025-07-01
Series:Microbiome
Online Access:https://doi.org/10.1186/s40168-025-02147-1
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author Yingchun Han
Zhaochao Deng
Yongyi Peng
Jiaxue Peng
Lei Cao
Yangru Xu
Yi Yang
Hao Zhou
Chen Zhang
Dongdong Zhang
Minxiao Wang
Chunfang Zhang
Chris Greening
Xiyang Dong
author_facet Yingchun Han
Zhaochao Deng
Yongyi Peng
Jiaxue Peng
Lei Cao
Yangru Xu
Yi Yang
Hao Zhou
Chen Zhang
Dongdong Zhang
Minxiao Wang
Chunfang Zhang
Chris Greening
Xiyang Dong
author_sort Yingchun Han
collection DOAJ
description Abstract Background Reductive dehalogenation is crucial for halogen cycling and environmental remediation, yet its ecological role is not completely understood, especially in deep-sea environments. To address this gap, we investigated the diversity and expression of genes encoding reductive dehalogenase catalytic subunits (RdhAs), and ecophysiology of potential organohalide reducers in deep-sea cold seeps, which are environments rich in halogenated compounds. Results Through genome-resolved metagenomic analysis of 165 global cold seep sediment samples, 4 types of RdhA-like sequences were identified based on their features and phylogenetic relationships: prototypical respiratory, transmembrane respiratory, cytosolic, and a novel clade. Cold seeps were found to harbor a higher abundance of these rdhA-like genes compared to other marine sediments, highlighting their potential as microbial reductive dehalogenation hotspots. These rdhA-like genes are encoded by a wide range of microorganisms across 4 archaeal and 36 bacterial phyla, significantly expanding the known diversity of organohalide reducers. Halogen geochemistry, laboratory incubations, metatranscriptomic data, and metabolomic profiling confirmed the presence of organohalides at concentrations of up to 18 mg/g in these sediments and suggested the potential for microbial reductive dehalogenation. Our findings suggest that organohalide reducers in cold seep sediments may participate in diverse biogeochemical processes, as inferred from the presence of genes related to carbon, hydrogen, nitrogen, sulfur, and trace element cycling. Additionally, RdhA-like proteins from cold seeps have diverse N-terminal structures across different gene groups. Conclusions These findings collectively suggest that reductive dehalogenation is an important process in deep-sea environments, mediated by a diverse array of microbes and novel enzymes. The discovery of diverse and abundant rdhA-like genes, along with their genomic context and potential metabolic linkages, highlights the role of cold seeps as reservoirs of microbial diversity with possible implications for environmental remediation. Video Abstract
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series Microbiome
spelling doaj-art-050d0de9dac04de2a722848e9430472e2025-08-20T03:45:34ZengBMCMicrobiome2049-26182025-07-0113112210.1186/s40168-025-02147-1Evidence of microbial reductive dehalogenation in deep-sea cold seeps and its implications for biogeochemical cyclesYingchun Han0Zhaochao Deng1Yongyi Peng2Jiaxue Peng3Lei Cao4Yangru Xu5Yi Yang6Hao Zhou7Chen Zhang8Dongdong Zhang9Minxiao Wang10Chunfang Zhang11Chris Greening12Xiyang Dong13Key Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural ResourcesOcean Research Center of Zhoushan, Zhejiang UniversityKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural ResourcesKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural ResourcesDeep Sea Research Center, Institute of Oceanology, Chinese Academy of SciencesInstitute of Marine Biology and Pharmacology, Ocean College, Zhejiang UniversityInstitute of Applied Ecology, Chinese Academy of SciencesSchool of Ocean Science and Technology, Dalian University of TechnologyDepartment of Microbiology, Immunology and Molecular Genetics, University of Texas Health Science CenterInstitute of Marine Biology and Pharmacology, Ocean College, Zhejiang UniversityDeep Sea Research Center, Institute of Oceanology, Chinese Academy of SciencesInstitute of Marine Biology and Pharmacology, Ocean College, Zhejiang UniversityDepartment of Microbiology, Biomedicine Discovery Institute, Monash UniversityKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural ResourcesAbstract Background Reductive dehalogenation is crucial for halogen cycling and environmental remediation, yet its ecological role is not completely understood, especially in deep-sea environments. To address this gap, we investigated the diversity and expression of genes encoding reductive dehalogenase catalytic subunits (RdhAs), and ecophysiology of potential organohalide reducers in deep-sea cold seeps, which are environments rich in halogenated compounds. Results Through genome-resolved metagenomic analysis of 165 global cold seep sediment samples, 4 types of RdhA-like sequences were identified based on their features and phylogenetic relationships: prototypical respiratory, transmembrane respiratory, cytosolic, and a novel clade. Cold seeps were found to harbor a higher abundance of these rdhA-like genes compared to other marine sediments, highlighting their potential as microbial reductive dehalogenation hotspots. These rdhA-like genes are encoded by a wide range of microorganisms across 4 archaeal and 36 bacterial phyla, significantly expanding the known diversity of organohalide reducers. Halogen geochemistry, laboratory incubations, metatranscriptomic data, and metabolomic profiling confirmed the presence of organohalides at concentrations of up to 18 mg/g in these sediments and suggested the potential for microbial reductive dehalogenation. Our findings suggest that organohalide reducers in cold seep sediments may participate in diverse biogeochemical processes, as inferred from the presence of genes related to carbon, hydrogen, nitrogen, sulfur, and trace element cycling. Additionally, RdhA-like proteins from cold seeps have diverse N-terminal structures across different gene groups. Conclusions These findings collectively suggest that reductive dehalogenation is an important process in deep-sea environments, mediated by a diverse array of microbes and novel enzymes. The discovery of diverse and abundant rdhA-like genes, along with their genomic context and potential metabolic linkages, highlights the role of cold seeps as reservoirs of microbial diversity with possible implications for environmental remediation. Video Abstracthttps://doi.org/10.1186/s40168-025-02147-1
spellingShingle Yingchun Han
Zhaochao Deng
Yongyi Peng
Jiaxue Peng
Lei Cao
Yangru Xu
Yi Yang
Hao Zhou
Chen Zhang
Dongdong Zhang
Minxiao Wang
Chunfang Zhang
Chris Greening
Xiyang Dong
Evidence of microbial reductive dehalogenation in deep-sea cold seeps and its implications for biogeochemical cycles
Microbiome
title Evidence of microbial reductive dehalogenation in deep-sea cold seeps and its implications for biogeochemical cycles
title_full Evidence of microbial reductive dehalogenation in deep-sea cold seeps and its implications for biogeochemical cycles
title_fullStr Evidence of microbial reductive dehalogenation in deep-sea cold seeps and its implications for biogeochemical cycles
title_full_unstemmed Evidence of microbial reductive dehalogenation in deep-sea cold seeps and its implications for biogeochemical cycles
title_short Evidence of microbial reductive dehalogenation in deep-sea cold seeps and its implications for biogeochemical cycles
title_sort evidence of microbial reductive dehalogenation in deep sea cold seeps and its implications for biogeochemical cycles
url https://doi.org/10.1186/s40168-025-02147-1
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