Host taxonomy and environment shapes insectivore viromes and viral spillover risks in Southwestern China

Abstract Background Zoonotic viruses originating from small mammals pose significant challenges to public health on a global scale. Insectivores, serving as natural reservoirs for a diverse array of zoonotic viruses, are known to carry a multitude of viral species. However, compared to the extensive...

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Main Authors: Ji-Hu Yang, Chun-Feng Luo, Rong Xiang, Jiu-Meng Min, Zong-Ti Shao, Yi-Lin Zhao, Lu Chen, Lin Huang, Yun Zhang, Shun-Shuai Liu, Yu-Qiong Li, En-Nian Pu, Wen-Qiang Shi, Hai-Feng Pan, Wei-Jun Chen, Chun-Hong Du, Jia-Fu Jiang
Format: Article
Language:English
Published: BMC 2025-05-01
Series:Microbiome
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Online Access:https://doi.org/10.1186/s40168-025-02115-9
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author Ji-Hu Yang
Chun-Feng Luo
Rong Xiang
Jiu-Meng Min
Zong-Ti Shao
Yi-Lin Zhao
Lu Chen
Lin Huang
Yun Zhang
Shun-Shuai Liu
Yu-Qiong Li
En-Nian Pu
Wen-Qiang Shi
Hai-Feng Pan
Wei-Jun Chen
Chun-Hong Du
Jia-Fu Jiang
author_facet Ji-Hu Yang
Chun-Feng Luo
Rong Xiang
Jiu-Meng Min
Zong-Ti Shao
Yi-Lin Zhao
Lu Chen
Lin Huang
Yun Zhang
Shun-Shuai Liu
Yu-Qiong Li
En-Nian Pu
Wen-Qiang Shi
Hai-Feng Pan
Wei-Jun Chen
Chun-Hong Du
Jia-Fu Jiang
author_sort Ji-Hu Yang
collection DOAJ
description Abstract Background Zoonotic viruses originating from small mammals pose significant challenges to public health on a global scale. Insectivores, serving as natural reservoirs for a diverse array of zoonotic viruses, are known to carry a multitude of viral species. However, compared to the extensive research conducted on rodents (Rodentia) and bats (Chiroptera), the role of insectivores in harboring and transmitting unknown pathogens remains underexplored, which may lead to a severe underestimation of their contributions and impact to global public health. Results This study employed a meta-transcriptomic approach to profile the viromes of 214 individual insectivores, encompassing 13 species from the families Soricidae, Erinaceidae, and Talpidae, collected across 12 counties in Yunnan Province, a recognized zoonotic hotspot. Based on virus reads, the analysis identified 42 viral families associated with vertebrates, highlighting significant virome diversity and host-specific viral tropisms among shrews, hedgehogs, and moles, along with notable geographic and environmental specificity of the viruses. Shrews exhibited greater viral richness and abundance compared to hedgehogs and moles, with variations influenced predominantly by host taxonomy, altitude, and geographic location. A total of 114 RNA-dependent RNA polymerase sequences were obtained, leading to the identification of 68 viruses, including 57 novel species. Instances of host jumping were observed in 11 viruses, with potential pathogenic viruses related to Mojiang paramyxovirus and members of the Hantaviridae family. Cross-species transmission was predominantly observed in viruses carried by shrews, while moles may play a pivotal role in facilitating viral transmission among insectivores. Conclusions This study enhances the understanding of the high diversity of mammalian viruses among insectivores in a relatively confined region and underscores the associations between virome composition and related zoonotic risks, providing a foundation for proactive measures to prevent and control the spillover of emerging zoonotic pathogens and potential future outbreaks. Video Abstract
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spelling doaj-art-5ef647a239f14f6c90aeb22bd38b7fae2025-08-20T03:10:30ZengBMCMicrobiome2049-26182025-05-0113111410.1186/s40168-025-02115-9Host taxonomy and environment shapes insectivore viromes and viral spillover risks in Southwestern ChinaJi-Hu Yang0Chun-Feng Luo1Rong Xiang2Jiu-Meng Min3Zong-Ti Shao4Yi-Lin Zhao5Lu Chen6Lin Huang7Yun Zhang8Shun-Shuai Liu9Yu-Qiong Li10En-Nian Pu11Wen-Qiang Shi12Hai-Feng Pan13Wei-Jun Chen14Chun-Hong Du15Jia-Fu Jiang16State Key Laboratory of Pathogen and Biosecurity, Academy of Military Medical SciencesState Key Laboratory of Pathogen and Biosecurity, Academy of Military Medical SciencesState Key Laboratory of Pathogen and Biosecurity, Academy of Military Medical SciencesHuo-Yan Engineering Technology, BGI-ShenzhenYunnan Key Laboratory for Zoonosis Control and Prevention, Yunnan Institute for Endemic Diseases Control and PreventionState Key Laboratory of Pathogen and Biosecurity, Academy of Military Medical SciencesBeijing Macro & Micro-Test Bio-Tech Co., LtdState Key Laboratory of Pathogen and Biosecurity, Academy of Military Medical SciencesYunnan Key Laboratory for Zoonosis Control and Prevention, Yunnan Institute for Endemic Diseases Control and PreventionState Key Laboratory of Pathogen and Biosecurity, Academy of Military Medical SciencesYunnan Key Laboratory for Zoonosis Control and Prevention, Yunnan Institute for Endemic Diseases Control and PreventionYunnan Key Laboratory for Zoonosis Control and Prevention, Yunnan Institute for Endemic Diseases Control and PreventionState Key Laboratory of Pathogen and Biosecurity, Academy of Military Medical SciencesSchool of Public Health, Anhui Medical UniversityHuo-Yan Engineering Technology, BGI-ShenzhenYunnan Key Laboratory for Zoonosis Control and Prevention, Yunnan Institute for Endemic Diseases Control and PreventionState Key Laboratory of Pathogen and Biosecurity, Academy of Military Medical SciencesAbstract Background Zoonotic viruses originating from small mammals pose significant challenges to public health on a global scale. Insectivores, serving as natural reservoirs for a diverse array of zoonotic viruses, are known to carry a multitude of viral species. However, compared to the extensive research conducted on rodents (Rodentia) and bats (Chiroptera), the role of insectivores in harboring and transmitting unknown pathogens remains underexplored, which may lead to a severe underestimation of their contributions and impact to global public health. Results This study employed a meta-transcriptomic approach to profile the viromes of 214 individual insectivores, encompassing 13 species from the families Soricidae, Erinaceidae, and Talpidae, collected across 12 counties in Yunnan Province, a recognized zoonotic hotspot. Based on virus reads, the analysis identified 42 viral families associated with vertebrates, highlighting significant virome diversity and host-specific viral tropisms among shrews, hedgehogs, and moles, along with notable geographic and environmental specificity of the viruses. Shrews exhibited greater viral richness and abundance compared to hedgehogs and moles, with variations influenced predominantly by host taxonomy, altitude, and geographic location. A total of 114 RNA-dependent RNA polymerase sequences were obtained, leading to the identification of 68 viruses, including 57 novel species. Instances of host jumping were observed in 11 viruses, with potential pathogenic viruses related to Mojiang paramyxovirus and members of the Hantaviridae family. Cross-species transmission was predominantly observed in viruses carried by shrews, while moles may play a pivotal role in facilitating viral transmission among insectivores. Conclusions This study enhances the understanding of the high diversity of mammalian viruses among insectivores in a relatively confined region and underscores the associations between virome composition and related zoonotic risks, providing a foundation for proactive measures to prevent and control the spillover of emerging zoonotic pathogens and potential future outbreaks. Video Abstracthttps://doi.org/10.1186/s40168-025-02115-9Emerging infectious diseasesEnvironmentInsectivoreViral evolutionVirome
spellingShingle Ji-Hu Yang
Chun-Feng Luo
Rong Xiang
Jiu-Meng Min
Zong-Ti Shao
Yi-Lin Zhao
Lu Chen
Lin Huang
Yun Zhang
Shun-Shuai Liu
Yu-Qiong Li
En-Nian Pu
Wen-Qiang Shi
Hai-Feng Pan
Wei-Jun Chen
Chun-Hong Du
Jia-Fu Jiang
Host taxonomy and environment shapes insectivore viromes and viral spillover risks in Southwestern China
Microbiome
Emerging infectious diseases
Environment
Insectivore
Viral evolution
Virome
title Host taxonomy and environment shapes insectivore viromes and viral spillover risks in Southwestern China
title_full Host taxonomy and environment shapes insectivore viromes and viral spillover risks in Southwestern China
title_fullStr Host taxonomy and environment shapes insectivore viromes and viral spillover risks in Southwestern China
title_full_unstemmed Host taxonomy and environment shapes insectivore viromes and viral spillover risks in Southwestern China
title_short Host taxonomy and environment shapes insectivore viromes and viral spillover risks in Southwestern China
title_sort host taxonomy and environment shapes insectivore viromes and viral spillover risks in southwestern china
topic Emerging infectious diseases
Environment
Insectivore
Viral evolution
Virome
url https://doi.org/10.1186/s40168-025-02115-9
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