Rhizosphere-triggered viral lysogeny mediates microbial metabolic reprogramming to enhance arsenic oxidation

Abstract The rhizosphere is a critical hotspot for metabolic activities involving arsenic (As). While recent studies indicate many functions for soil viruses, much remains overlooked regarding their quantitative impact on rhizosphere processes. Here, we analyze time-series metagenomes of rice (Oryza...

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Main Authors: Xinwei Song, Yiling Wang, Youjing Wang, Kankan Zhao, Di Tong, Ruichuan Gao, Xiaofei Lv, Dedong Kong, Yunjie Ruan, Mengcen Wang, Xianjin Tang, Fangbai Li, Yongming Luo, Yongguan Zhu, Jianming Xu, Bin Ma
Format: Article
Language:English
Published: Nature Portfolio 2025-04-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-58695-5
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author Xinwei Song
Yiling Wang
Youjing Wang
Kankan Zhao
Di Tong
Ruichuan Gao
Xiaofei Lv
Dedong Kong
Yunjie Ruan
Mengcen Wang
Xianjin Tang
Fangbai Li
Yongming Luo
Yongguan Zhu
Jianming Xu
Bin Ma
author_facet Xinwei Song
Yiling Wang
Youjing Wang
Kankan Zhao
Di Tong
Ruichuan Gao
Xiaofei Lv
Dedong Kong
Yunjie Ruan
Mengcen Wang
Xianjin Tang
Fangbai Li
Yongming Luo
Yongguan Zhu
Jianming Xu
Bin Ma
author_sort Xinwei Song
collection DOAJ
description Abstract The rhizosphere is a critical hotspot for metabolic activities involving arsenic (As). While recent studies indicate many functions for soil viruses, much remains overlooked regarding their quantitative impact on rhizosphere processes. Here, we analyze time-series metagenomes of rice (Oryza sativa L.)rhizosphere and bulk soil to explore how viruses mediate rhizosphere As biogeochemistry. We observe the rhizosphere favors lysogeny in viruses associated with As-oxidizing microbes, with a positive correlation between As oxidation and the prevalence of these microbial hosts. Moreover, results demonstrate these lysogenic viruses enrich both As oxidation and phosphorus co-metabolism genes and mediated horizontal gene transfers (HGTs) of As oxidases. In silico simulation with genome-scale metabolic models (GEMs) and in vitro validation with experiments estimate that rhizosphere lysogenic viruses contribute up to 25% of microbial As oxidation. These findings enhance our comprehension of the plant-microbiome-virome interplay and highlight the potential of rhizosphere viruses for improving soil health in sustainable agriculture.
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institution Kabale University
issn 2041-1723
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publishDate 2025-04-01
publisher Nature Portfolio
record_format Article
series Nature Communications
spelling doaj-art-873e92ead7634d0393eb58b5fc86ed212025-08-20T03:52:20ZengNature PortfolioNature Communications2041-17232025-04-0116111810.1038/s41467-025-58695-5Rhizosphere-triggered viral lysogeny mediates microbial metabolic reprogramming to enhance arsenic oxidationXinwei Song0Yiling Wang1Youjing Wang2Kankan Zhao3Di Tong4Ruichuan Gao5Xiaofei Lv6Dedong Kong7Yunjie Ruan8Mengcen Wang9Xianjin Tang10Fangbai Li11Yongming Luo12Yongguan Zhu13Jianming Xu14Bin Ma15State Key Laboratory of Soil Pollution Control and Safety, Zhejiang UniversityState Key Laboratory of Soil Pollution Control and Safety, Zhejiang UniversityZhejiang Provincial Key Laboratory of Agricultural, Resources and Environment, College of Environmental and Resource Science, Zhejiang UniversityState Key Laboratory of Soil Pollution Control and Safety, Zhejiang UniversityZhejiang Provincial Key Laboratory of Agricultural, Resources and Environment, College of Environmental and Resource Science, Zhejiang UniversityGuangdong Key Laboratory of Integrated Agro-Environmental Pollution Control and Management, Institute of Eco-environmental and Soil Sciences, Guangdong Academy of SciencesDepartment of Environmental Engineering, China Jiliang UniversityInstitute of Digital Agriculture, Zhejiang Academy of Agricultural SciencesInstitute of Agricultural Bio-Environmental Engineering, College of Bio-Systems Engineering and Food Science, Zhejiang UniversityState Key Laboratory of Rice Biology and Breeding, Ministry of Agricultural and Rural Affairs Laboratory of Molecular Biology of Crop Pathogens and Insects, Zhejiang UniversityState Key Laboratory of Soil Pollution Control and Safety, Zhejiang UniversityGuangdong Key Laboratory of Integrated Agro-Environmental Pollution Control and Management, Institute of Eco-environmental and Soil Sciences, Guangdong Academy of SciencesKey Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of SciencesState Key Laboratory of Urban and Regional Ecology, Research Center for Eco-environmental Sciences, Chinese Academy of SciencesState Key Laboratory of Soil Pollution Control and Safety, Zhejiang UniversityState Key Laboratory of Soil Pollution Control and Safety, Zhejiang UniversityAbstract The rhizosphere is a critical hotspot for metabolic activities involving arsenic (As). While recent studies indicate many functions for soil viruses, much remains overlooked regarding their quantitative impact on rhizosphere processes. Here, we analyze time-series metagenomes of rice (Oryza sativa L.)rhizosphere and bulk soil to explore how viruses mediate rhizosphere As biogeochemistry. We observe the rhizosphere favors lysogeny in viruses associated with As-oxidizing microbes, with a positive correlation between As oxidation and the prevalence of these microbial hosts. Moreover, results demonstrate these lysogenic viruses enrich both As oxidation and phosphorus co-metabolism genes and mediated horizontal gene transfers (HGTs) of As oxidases. In silico simulation with genome-scale metabolic models (GEMs) and in vitro validation with experiments estimate that rhizosphere lysogenic viruses contribute up to 25% of microbial As oxidation. These findings enhance our comprehension of the plant-microbiome-virome interplay and highlight the potential of rhizosphere viruses for improving soil health in sustainable agriculture.https://doi.org/10.1038/s41467-025-58695-5
spellingShingle Xinwei Song
Yiling Wang
Youjing Wang
Kankan Zhao
Di Tong
Ruichuan Gao
Xiaofei Lv
Dedong Kong
Yunjie Ruan
Mengcen Wang
Xianjin Tang
Fangbai Li
Yongming Luo
Yongguan Zhu
Jianming Xu
Bin Ma
Rhizosphere-triggered viral lysogeny mediates microbial metabolic reprogramming to enhance arsenic oxidation
Nature Communications
title Rhizosphere-triggered viral lysogeny mediates microbial metabolic reprogramming to enhance arsenic oxidation
title_full Rhizosphere-triggered viral lysogeny mediates microbial metabolic reprogramming to enhance arsenic oxidation
title_fullStr Rhizosphere-triggered viral lysogeny mediates microbial metabolic reprogramming to enhance arsenic oxidation
title_full_unstemmed Rhizosphere-triggered viral lysogeny mediates microbial metabolic reprogramming to enhance arsenic oxidation
title_short Rhizosphere-triggered viral lysogeny mediates microbial metabolic reprogramming to enhance arsenic oxidation
title_sort rhizosphere triggered viral lysogeny mediates microbial metabolic reprogramming to enhance arsenic oxidation
url https://doi.org/10.1038/s41467-025-58695-5
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