First insight into the virome composition of the vulnerable <em>Naemorhedus griseus</em>

Yu Guo; Meijing Hong; Xuefei Sun; Yuhang Liu; Yue Sun; Le Yi; Biao He; Changchun Tu; Guoqiang Zhu; Zhongzhong Tu

doi:10.1016/j.virs.2026.08.009

October 2026

. doi: 10.1016/j.virs.2026.08.009

Citation: Yu Guo, Meijing Hong, Xuefei Sun, Yuhang Liu, Yue Sun, Le Yi, Biao He, Changchun Tu, Guoqiang Zhu, Zhongzhong Tu. First insight into the virome composition of the vulnerable Naemorhedus griseus .VIROLOGICA SINICA, 2026, 41(5) : 1033-1044. http://dx.doi.org/10.1016/j.virs.2026.08.009

中华斑羚病毒组组成的初步研究

郭玉 ^a,b ,
洪美静 ^c ,
孙雪霏 ^b,d ,
刘雨行 ^b ,
孙悦 ^b ,
易乐 ^b ,
何彪 ^b ,
涂长春 ^a,b ,
朱国强 ^a,, ,
涂忠忠 ^b,,

a. 扬州大学, 江苏省动物重要疫病与人兽共患病防控协同创新中心;
b. 军事科学院军事医学研究院, 吉林省人兽共患病预防与控制重点实验室, 病原微生物生物安全全国重点实验室;
c. 内蒙古赤峰赛罕乌拉国家级自然保护区管理局;
d. 吉林大学动物医学学院

通讯作者： 朱国强, yzgqzhu@yzu.edu.cn; 涂忠忠, tudong890901@163.com
收稿日期： 2026-01-09
录用日期： 2026-08-10

摘要

中华斑羚（Naemorhedus griseus）被列入《中国生物多样性红色名录》易危物种，同时也是我国国家二级重点保护野生动物。尽管该物种在我国分布范围较广，但针对其携带病原体的相关研究十分匮乏，人们对其体内病毒多样性的认知仍较为有限。本研究对一例救治无效而死亡的中华斑羚开展全病毒组图谱解析，在该动物多种脏器组织中检出种类丰富的病毒群落，包括大量噬菌体、几种植物病毒以及多种哺乳动物病毒包含两种不同的细小病毒、新型小双节段 RNA病毒与一种新型白纤病毒。此外，宿主溯源分析结果显示，中华斑羚携带病毒的宿主来源涵盖植物、哺乳动物与节肢动物。上述研究数据首次揭示了中华斑羚携带病毒的遗传多样性，以及这类病毒在人类、家养动物、节肢动物和野生动物之间的传播动态。本研究不仅丰富了现有病毒基因组数据库、明确了相关病原体的宿主范围，也凸显了依托同一健康理念开展野生动物源病毒监测与疫病防控的必要性。
- 中华斑羚
- , 病毒组
- , 细小病毒
- , 小双节RNA病毒
- , 白纤病毒

First insight into the virome composition of the vulnerable Naemorhedus griseus

Yu Guo ^a,b ,
Meijing Hong ^c ,
Xuefei Sun ^b,d ,
Yuhang Liu ^b ,
Yue Sun ^b ,
Le Yi ^b ,
Biao He ^b ,
Changchun Tu ^a,b ,
Guoqiang Zhu ^a,, ,
Zhongzhong Tu ^b,,

a. Jiangsu Co-Innovation Center for the Prevention and Control of Important Animal Infectious Disease and Zoonoses, Yangzhou University, Yangzhou 225009, China;
b. Key Laboratory of Jilin Province for Zoonoses Prevention and Control, State Key Laboratory of Pathogen and Biosecurity, Academy of Military Medical Sciences, Changchun 130122, China;
c. Chifeng Saihanwula National Nature Reserve Administration, Daban 025150, China;
d. College of Veterinary Medicine, Jilin University, Changchun 130062, China

Corresponding author: Guoqiang Zhu, yzgqzhu@yzu.edu.cn Zhongzhong Tu, tudong890901@163.com
Received Date: 09 January 2026
Accepted Date: 10 August 2026

Abstract

The Chinese goral (Naemorhedus griseus) is identified as a vulnerable species on the Red List of China's Biodiversity and listed as a national second-class key protected wild animal in China. Despite its widespread distribution in China, there has been scant research into the pathogens harbored by this species, and our understanding of the virus diversity remains limited. In the present study, we performed the whole virome profiling of a rescue-failed Naemorhedus griseus, which identified a diverse viral community across multiple organ tissues of the animal. Specifically, abundant bacteriophages, several plant-derived viruses, and multiple mammalian viruses, i.e., two distinct parvoviruses, novel picobirnaviruses, and a novel phenuivirus. Additionally, virus-carrier determination analysis that Naemorhedus griseus-borne viruses are related to plants, mammals, and arthropods. These data provide the first insight into the genetic diversity of Naemorhedus griseus-borne viruses, and their transmission dynamics across humans, domestic animals, arthropods, and wildlife. This study not only expands the existing repertoire of viral genomic information and delineates the host range of these pathogens but also underscores the imperative of implementing a One Health strategy for the surveillance and control of wildlife-borne viral pathogens.
- Naemorhedus griseus
- , Virome
- , Parvovirus
- , Picobirnavirus
- , Phenuivirus

References
1. Baudin, M., Jumaa, A.M., Jomma, H.J.E., Karsany, M.S., Bucht, G., Naslund, J., Ahlm, C., Evander, M., Mohamed, N., 2016. Association of Rift Valley fever virus infection with miscarriage in Sudanese women: a cross-sectional study. Lancet Glob Health, 4, e864-e871.
2. Briese, T., Calisher, C.H.,Higgs, S., 2013. Viruses of the family Bunyaviridae: are all available isolates reassortants? Virology 446, 207-216.
3. Xing Chen, T.G., Wenle Jiang, Dandan Li, Kong Yang, Sheng Li, 2021. Distribution and population status of bovine species in China based on bibliometric analysis. Biodiv. Sci. 29, 668-679.
4. Chen, J., Sun, Y., Yan, X., Ren, Z., Wang, G., Liu, Y., Zhao, Z., Yi, L., Tu, C.,He, B., 2022. Elimination of Foreign Sequences in Eukaryotic Viral Reference Genomes Improves the Accuracy of Virome Analysis. mSystems 7, e0090722.
5. Cotmore, S.F., Agbandje-Mckenna, M., Canuti, M., Chiorini, J.A., Eis-Hubinger, A.M., Hughes, J., Mietzsch, M., Modha, S., Ogliastro, M., Penzes, J.J., Pintel, D.J., Qiu, J., Soderlund-Venermo, M., Tattersall, P., Tijssen, P., Ictv Report, C., 2019. ICTV Virus Taxonomy Profile: Parvoviridae. J. Gen. Virol. 100, 367-368.
6. Delmas, B., Attoui, H., Ghosh, S., Malik, Y.S., Mundt, E., Vakharia, V.N., Ictv Report, C., 2019. ICTV virus taxonomy profile: Picobirnaviridae. J. Gen. Virol. 100, 133-134.
7. Fu, L., Huang, J., Zhang, G., Han, D., Ding, L., Wei, Y., Liu, X., Li, C.,Yu, H., 2025. Abrupt loss of species richness caused by ecosystem transition. Sci. Bull (Beijing) 70, 1523-1532.
8. He, H., Li, Y., Chen, J., Xian, J., Zheng, L., Sun, H., Fan, S., Fu, J., Li, Q., Chen, C., Liang, M., Zhang, M., Wu, R., Xiao, G.,Chen, Q., 2023. Identification and genetic characteristics of tusavirus in fecal samples of patients with chronic diseases in Guangzhou, China. Front Microbiol. 14, 1205134.
9. Hebert, P.D., Cywinska, A., Ball, S.L.,Dewaard, J.R., 2003. Biological identifications through DNA barcodes. Proc. Biol. Sci. 270, 313-321.
10. Hutton, A.L.K., Grigson, S., Bartle, L., Papudeshi, B., Mallawaarachchi, V., Tarasenko, A., Mitchell, J.G.,Edwards, R.A., 2026. Picobirnavirus: how do you find where it's hiding? Crit. Rev. Microbiol, 52, 339-349.
11. Khonmee, J., Brown, J.L., Rojanasthien, S., Aunsusin, A., Thumasanukul, D., Kongphoemphun, A., Siriaroonrat, B., Tipkantha, W., Punyapornwithaya, V.,Thitaram, C., 2014. Gender, season and management affect fecal glucocorticoid metabolite concentrations in captive goral (Naemorhedus griseus) in Thailand. PLoS One 9, e91633.
12. Li, L., Giannitti, F., Low, J., Keyes, C., Ullmann, L.S., Deng, X., Aleman, M., Pesavento, P.A., Pusterla, N.,Delwart, E., 2015. Exploring the virome of diseased horses. J Gen Virol, 96, 2721-2733.
13. Liang, G.,Bushman, F.D., 2021. The human virome: assembly, composition and host interactions. Nat. Rev. Microbiol. 19, 514-527.
14. Liu, Y., Sun, L., Tu, Z., Sun, S., Sun, Y., Yi, L., Tu, C.,He, B., 2022. Virome Profiling of an Amur leopard cat Reveals Multiple Anelloviruses and a Bocaparvovirus. Vet. Sci. 9.
15. Luo, X.L., Lu, S., Jin, D., Yang, J., Wu, S.S.,Xu, J., 2018. Marmota himalayana in the Qinghai-Tibetan plateau as a special host for bi-segmented and unsegmented picobirnaviruses. Emerg. Microbes Infect. 7, 20.
16. Macdonald, D.W., Harrington, L.A., Moorhouse, T.P.,D'cruze, N., 2021. Trading Animal Lives: Ten Tricky Issues on the Road to Protecting Commodified Wild Animals. Bioscience, 71, 846-860.
17. Martha, Clokie, R.J., Andrew, Millard, D., Andrey, Letarov, V., Shaun,Heaphy, 2011. Phages in nature. Bacteriophage.
18. Milbank, C.,Vira, B., 2022. Wildmeat consumption and zoonotic spillover: contextualising disease emergence and policy responses. Lancet Planet Health 6, e439-e448.
19. Phan, T.G., Sdiri-Loulizi, K., Aouni, M., Ambert-Balay, K., Pothier, P., Deng, X.,Delwart, E., 2014. New parvovirus in child with unexplained diarrhea, Tunisia. Emerg Infect Dis, 20, 1911-1913.
20. Reese, S.M., Blitvich, B.J., Blair, C.D., Geske, D., Beaty, B.J.,Black, W.C.T., 2008. Potential for La Crosse virus segment reassortment in nature. Virol. J. 5, 164.
21. Reuter, G., Pankovics, P., Laszlo, Z., Gaspar, G., Hui, A., Delwart, E.,Boros, A., 2022. Human-stool-associated tusavirus (Parvoviridae) in domestic goats and sheep. Arch Virol, 167, 1307-1310.
22. Sasaya, T., Palacios, G., Briese, T., Di Serio, F., Groschup, M.H., Neriya, Y., Song, J.W.,Tomitaka, Y., 2023. ICTV Virus Taxonomy Profile: Phenuiviridae 2023. J. Gen. Virol. 104.
23. Shao, G., Zhao, L., Tang, C.,Yue, H., 2021. Identification and genomic characterization of bovine parvovirus 1 in yaks. J. Vet. Diagn. Invest. 33, 1193-1196.
24. Shi, M., Lin, X.D., Chen, X., Tian, J.H., Chen, L.J., Li, K., Wang, W., Eden, J.S., Shen, J.J., Liu, L., Holmes, E.C.,Zhang, Y.Z., 2018. The evolutionary history of vertebrate RNA viruses. Nature 556, 197-202.
25. Shi, M., Lin, X.D., Tian, J.H., Chen, L.J., Chen, X., Li, C.X., Qin, X.C., Li, J., Cao, J.P., Eden, J.S., Buchmann, J., Wang, W., Xu, J., Holmes, E.C.,Zhang, Y.Z., 2016. Redefining the invertebrate RNA virosphere. Nature 540, 539-543.
26. Siembieda, J.L., Kock, R.A., Mccracken, T.A.,Newman, S.H., 2011. The role of wildlife in transboundary animal diseases. Anim. Health Res. Rev. 12, 95-111.
27. Smits, S.L., Poon, L.L., Van Leeuwen, M., Lau, P.N., Perera, H.K., Peiris, J.S., Simon, J.H.,Osterhaus, A.D., 2011. Genogroup I and II picobirnaviruses in respiratory tracts of pigs. Emerg. Infect. Dis. 17, 2328-2330.
28. Sun, Y., Qu, Y., Yan, X., Yan, G., Chen, J., Wang, G., Zhao, Z., Liu, Y., Tu, C.,He, B., 2022. Comprehensive Evaluation of RNA and DNA Viromic Methods Based on Species Richness and Abundance Analyses Using Marmot Rectal Samples. mSystems 7, e0043022.
29. Sun, Y., Sun, L., Sun, S., Tu, Z., Liu, Y., Yi, L., Tu, C.,He, B., 2023. Virome Profiling of an Eastern Roe Deer Reveals Spillover of Viruses from Domestic Animals to Wildlife. Pathogens 12, 156.
30. Wiethoelter, A.K., Beltran-Alcrudo, D., Kock, R., Mor, S.M., 2015. Global trends in infectious diseases at the wildlife-livestock interface. Proc. Natl. Acad. Sci. U. S. A. 112, 9662-9667.
31. Woo, P.C., Lau, S.K., Bai, R., Teng, J.L., Lee, P., Martelli, P., Hui, S.W.,Yuen, K.Y., 2012. Complete genome sequence of a novel picobirnavirus, otarine picobirnavirus, discovered in California sea lions. J. Virol. 86, 6377-6378.
32. Woo, P.C., Teng, J.L., Bai, R., Wong, A.Y., Martelli, P., Hui, S.W., Tsang, A.K., Lau, C.C., Ahmed, S.S., Yip, C.C., Choi, G.K., Li, K.S., Lam, C.S., Lau, S.K.,Yuen, K.Y., 2016. High Diversity of Genogroup I Picobirnaviruses in Mammals. Front Microbiol. 7, 1886.
33. Woo, P.C.Y., Teng, J.L.L., Bai, R., Tang, Y., Wong, A.Y.P., Li, K.S.M., Lam, C.S.F., Fan, R.Y.Y., Lau, S.K.P.,Yuen, K.Y., 2019. Novel Picobirnaviruses in Respiratory and Alimentary Tracts of Cattle and Monkeys with Large Intra- and Inter-Host Diversity. Viruses 11, 574.
34. Wu, R., Zhang, X., Zhao, J., Yi, D., Gao, F., Bao, W., 2024. Population Viability Analysis on Chinese Goral Indicates an Extinction Risk for a Local Population in Beijing, China. Animals (Basel), 14, 1126.
35. Yang, Z., Wang, H., Yang, S., Wang, X., Shen, Q., Ji, L., Zeng, J., Zhang, W., Gong, H.,Shan, T., 2023. Virome diversity of ticks feeding on domestic mammals in China. Virol. Sin. 38, 208-221.
36. Yu, X.J., Liang, M.F., Zhang, S.Y., Liu, Y., Li, J.D., Sun, Y.L., Zhang, L., Zhang, Q.F., Popov, V.L., Li, C., Qu, J., Li, Q., Zhang, Y.P., Hai, R., Wu, W., Wang, Q., Zhan, F.X., Wang, X.J., Kan, B., Wang, S,W., Wan, K.L., Jing, H.Q., Lu, J.X., Yin, W.W., Zhou, H., Guan, X.H., Liu, J.F., Bi, Z.Q., Liu, G.H., Ren, J., Wang, H., Zhao, Z., Song, J.D., H,e J.R., Wan, T., Zhang, J.S., Fu, X.P., Sun, L.N., Dong, X.P., Feng, Z.J., Yang, W.Z., Hong, T., Zhang, Y., Walker, D.H., Wang, Y., Li, D.X., 2011. Fever with thrombocytopenia associated with a novel bunyavirus in China. N. Engl. J. Med. 364, 1523-1532.
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10.1016j.virs.2026.08.009-ESM.docx