Viral metagenomic analysis reveals potential biological hazards in non-human primates in a zoo

Ruiying Liang , Xinming Tang , Lin Liang , Jiabo Ding , Ye Tian , Yixian Qin , Sufen Zhao , Lixia Zhang , Tianchun Pu , Xuefeng Liu , Jinpeng Liu , Chenglin Zhang , Zibin Li , Ting Jia

Animal Research and One Health ›› 2025, Vol. 3 ›› Issue (2) : 217 -228.

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Animal Research and One Health ›› 2025, Vol. 3 ›› Issue (2) : 217 -228. DOI: 10.1002/aro2.79
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Viral metagenomic analysis reveals potential biological hazards in non-human primates in a zoo

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Abstract

Pathogens have been documented to be transmissible between humans and non-human primates (NHPs), with NHPs demonstrating susceptibility to human viruses. Conducting surveillance for viruses in NHPs to identify potential zoonotic agents that may emerge or pose a high risk of spillover remains a critical strategy for preparing for and responding to future zoonotic events. This study employed viral metagenomic analysis on nine randomly selected NHPs from the Zoo in China to detect potential pathogens within captive environments. The analysis identified the presence of picornavirus Encephalomyocarditis virus (EMCV), poxvirus (BeAn 58,058 virus, BAV), and retroviruses (human endogenous retrovirus, HERV and baboon endogenous virus, BaEV). These viruses exhibited significant genetic homology to established viral strains, with EMCV demonstrating close relatedness to a strain previously detected in the United States, and BAV beling newly identified in NHPs. The study suggests that zoo rodents, particularly rats, serve as the primary reservoirs for the viruses, thereby posing a potential threat to public health. Therefore, this underscores the imperative to enhance rodent control measures within zoological institutions and provides strategic recommendations for mitigating interspecies viral transmission.

Keywords

non-human primates / picornavirus / poxvirus / retrovirus / viral metagenomics

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Ruiying Liang, Xinming Tang, Lin Liang, Jiabo Ding, Ye Tian, Yixian Qin, Sufen Zhao, Lixia Zhang, Tianchun Pu, Xuefeng Liu, Jinpeng Liu, Chenglin Zhang, Zibin Li, Ting Jia. Viral metagenomic analysis reveals potential biological hazards in non-human primates in a zoo. Animal Research and One Health, 2025, 3(2): 217-228 DOI:10.1002/aro2.79

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References

[1]

Thompson, S.J., Pearce, J.M., & Ramey, A.M. (2017). Vectors, hosts, and control measures for Zika virus in the americas. EcoHealth, 14(4), 821-839. https://doi.org/10.1007/s10393-017-1277-2

[2]

Hanley, K.A., Monath, T.P., Weaver, S.C., Rossi, S.L., Richman, R.L., & Vasilakis, N. (2013). Fever versus fever: The role of host and vector susceptibility and interspecific competition in shaping the current and future distributions of the sylvatic cycles of dengue virus and yellow fever virus. Infection, Genetics and Evolution, 19, 292-311. https://doi.org/10.1016/j.meegid.2013.03.008

[3]

Roodgar, M., Babveyh, A., Nguyen, L.H., Zhou, W., Sinha, R., Lee, H., Hanks, J.B., Avula, M., Jiang, L., Jian, R., Lee, H., Song, G., Chaib, H., Weissman, I.L., Batzoglou, S., Holmes, S., Smith, D.G., Mankowski, J.L., Prost, S., & Snyder, M.P. (2020). Chromosome-level de novo assembly of the pig-tailed macaque genome using linked-read sequencing and HiC proximity scaffolding. GigaScience, 9(7). https://doi.org/10.1093/gigascience/giaa069

[4]

Salguero, F.J., White, A.D., Slack, G.S., Fotheringham, S.A., Bewley, K.R., Gooch, K.E., Longet, S., Humphries, H.E., Watson, R.J., Hunter, L., Ryan, K.A., Hall, Y., Sibley, L., Sarfas, C., Allen, L., Aram, M., Brunt, E., Brown, P., Buttigieg, K. R, … Carroll, M.W. (2021). Comparison of rhesus and cynomolgus macaques as an infection model for COVID-19. Nature Communications, 12(1), 1260. https://doi.org/10.1038/s41467-021-21389-9

[5]

Li, Z., Wang, Z., Dinh, P.C., Zhu, D., Popowski, K.D., Lutz, H., Hu, S., Lewis, M.G., Cook, A., Andersen, H., Greenhouse, J., Pessaint, L., Lobo, L.J., & Cheng, K. (2021). Cell-mimicking nanodecoys neutralize SARS-CoV-2 and mitigate lung injury in a non-human primate model of COVID-19. Nature Nanotechnology, 16(8), 942-951. https://doi.org/10.1038/s41565-021-00923-2

[6]

Liu, Z.J., Qian, X.K., Hong, M.H., Zhang, J.L., Li, D.Y., Wang, T.H., Yang, Z.M., Zhang, L.Y., Wang, Z.M., Nie, H.J., Fan, K.Y., Zhang, X.F., Chen, M.M., Sha, W.L., Roos, C., & Li, M. (2021). Global view on virus infection in non-human primates and implications for public health and wildlife conservation. Zoological Research, 42(5), 626-632. https://doi.org/10.24272/j.issn.2095-8137.2021.080

[7]

Silva, D.C., Moreira-Silva, E.A., Gomes, J.A., Fonseca, F.G., & Correa-Oliveira, R. (2010). Clinical signs, diagnosis, and case reports of Vaccinia virus infections. Brazilian Journal of Infectious Diseases, 14(2), 129-134. https://doi.org/10.1590/s1413-86702010000200003

[8]

Hahn, B.H., Shaw, G.M., De Cock, K.M., & Sharp, P.M. (2000). AIDS as a zoonosis: Scientific and public health implications. Science, 287(5453), 607-614. https://doi.org/10.1126/science.287.5453.607

[9]

He, B.A., Gong, W.J., Yan, X.M., Zhao, Z.H., Yang, L.E., Tan, Z.Z., Xu, L., Zhu, A.W., Zhang, J.N., Rao, J.H., Yu, X.L., Jiang, J.F., Lu, Z.J., Zhang, Y.F., Wu, J.M., Li, Y., Shi, Y.X., Jiang, Q., Chen, X.W., & Tu, C.C. (2021). Viral metagenome-based precision surveillance of pig population at large scale reveals viromic signatures of sample types and influence of farming management on pig virome. mSystems, 6(3). e0042021. https://doi.org/10.1128/mSystems.00420-21

[10]

Vibin, J., Chamings, A., Klaassen, M., & Alexandersen, S. (2020). Metagenomic characterisation of additional and novel avian viruses from Australian wild ducks. Scientific Reports, 10(1), 22284. https://doi.org/10.1038/s41598-020-79413-9

[11]

Fonseca, F.G., Lanna, M. C.S., Campos, M. A.S., Kitajima, E.W., Peres, J.N., Golgher, R.R., Ferreira, P. C.P., & Kroon, E.G. (1998). Morphological and molecular characterization of the poxvirus BeAn 58058. Archives of Virology, 143(6), 1171-1186. https://doi.org/10.1007/s007050050365

[12]

Afonso, P.P., Silva, P.M., Schnellrath, L.C., Jesus, D.M., Hu, J.H., Yang, Y.J., Renne, R., Attias, M., Condit, R.C., Moussatché, N., & Damaso, C.R. (2012). Biological characterization and next-generation genome sequencing of the unclassified Cotia virus SPAn232. Journal of Virology, 86(9), 5039-5054. https://doi.org/10.1128/Jvi.07162-11

[13]

Johnson, R.I., Boczkowska, B., Alfson, K., Weary, T., Menzie, H., Delgado, J., Rodriguez, G., Carrion, R.,Jr., & Griffiths, A. (2021). Identification and characterization of defective viral genomes in ebola virus-infected rhesus macaques. Journal of Virology, 95(17). https://doi.org/10.1128/JVI.00714-21

[14]

Danko, D., Bezdan, D., Afshin, E.E., Ahsanuddin, S., Bhattacharya, C., Butler, D.J., Chng, K.R., Donnellan, D., Hecht, J., Jackson, K., Kuchin, K., Karasikov, M., Lyons, A., Mak, L., Meleshko, D., Mustafa, H., Mutai, B., Neches, R.Y., Ng, A, …, Zubenko, S. (2021). A global metagenomic map of urban microbiomes and antimicrobial resistance. Cell, 184(13), 3376-3393.e17. https://doi.org/10.1016/j.cell.2021.05.002

[15]

Carocci, M., & Bakkali-Kassimi, L. (2012). The encephalomyocarditis virus. Virulence, 3(4), 351-367. https://doi.org/10.4161/viru.20573

[16]

Oberste, M.S., Gotuzzo, E., Blair, P., Nix, W.A., Ksiazek, T.G., Comer, J.A., Rollin, P., Goldsmith, C.S., Olson, J., & Kochel, T.J. (2009). Human febrile illness caused by encephalomyocarditis virus infection, Peru. Emerging Infectious Diseases, 15(4), 640-646. https://doi.org/10.3201/eid1504.081428

[17]

Hubbard, G.B., Soike, K.F., Butler, T.M., Carey, K.D., Davis, H., Butcher, W.I., & Gauntt, C.J. (1992). An encephalomyocarditis virus epizootic in a baboon colony. Laboratory Animal Science, 42(3), 233-239.

[18]

Hill, B.D., Ketterer, P.J., Rodwell, B.J., Eaves, F.W., & Webster, W.R. (1985). Encephalomyocarditis virus infection and pig disease in Queensland. Australian Veterinary Journal, 62(12), 433-434. https://doi.org/10.1111/j.1751-0813.1985.tb14138.x

[19]

Gainer, J.H. (1967). Encephalomyocarditis virus infections in Florida, 1960-1966. Journal of the American Veterinary Medical Association, 151(4), 421-425.

[20]

Ghosh, S.N., & Rajagopalan, P.K. (1973). Encephalomyocarditis virus activity in Mus booduga (gray) in Barur village (1961-1962), Sagar KFD area, Mysore state, India. Indian Journal of Medical Research, 61(7), 989-991.

[21]

Roca-Garcia, M., & Sanmartinbarberi, C. (1957). The isolation of encephalomyocarditis virus from Aotus monkeys. The American Journal of Tropical Medicine and Hygiene, 6(5), 840-852. https://doi.org/10.4269/ajtmh.1957.6.840

[22]

Vizoso, A.D., Vizoso, M.R., & Hay, R. (1964). Isolation of a virus resembling encephalomyocarditis from a red squirrel. Nature, 201(4921), 849-850. https://doi.org/10.1038/201849a0

[23]

Amaddeo, D., Cardeti, G., & Autorino, G.L. (1995). Isolation of encephalomyocarditis virus from dormice (Myoxus glis) in Italy. Journal of Wildlife Diseases, 31(2), 238-242. https://doi.org/10.7589/0090-3558-31.2.238

[24]

Pope, J.H. (1959). A virus of the encephalomyocarditis group from a water-rat, Hydromys chrysogaster, in North Queensland. Australian Journal of Experimental Biology & Medical Science, 37(2), 117-124. https://doi.org/10.1038/icb.1959.13

[25]

Niewiesk, S., & Prince, G. (2002). Diversifying animal models: The use of hispid cotton rats (sigmodon hispidus) in infectious diseases. Laboratory Animals, 36(4), 357-372. https://doi.org/10.1258/002367702320389026

[26]

Spyrou, V., Maurice, H., Billinis, C., Papanastassopoulou, M., Psalla, D., Nielen, M., Koenen, F., & Papadopoulos, O. (2004). Transmission and pathogenicity of encephalomyocarditis virus (EMCV) among rats. Veterinary Research, 35(1), 113-122. Epub 2004/04/22 https://doi.org/10.1051/vetres:2003044

[27]

Zhang, G.Q., Ge, X.N., Guo, X., & Yang, H.C. (2007). Genomic analysis of two porcine encephalomyocarditis virus strains isolated in China. Archives of Virology, 152(6), 1209-1213. https://doi.org/10.1007/s00705-006-0930-9

[28]

Maurice, H., Nielen, M., Vyt, P., Frankena, K., & Koenen, F. (2007). Factors related to the incidence of clinical encephalomyocarditis virus (EMCV) infection on Belgian pig farms. Preventive Veterinary Medicine, 78(1), 24-34. https://doi.org/10.1016/j.prevetmed.2006.09.002

[29]

Koenen, F., Vanderhallen, H., Castryck, F., & Miry, C. (1999). Epidemiologic, pathogenic and molecular analysis of recent encephalomyocarditis outbreaks in Belgium. Zentralblatt für Veterinarmedizin B, 46(4), 217-231.

[30]

Medkour, H., Castaneda, S., Amona, I., Fenollar, F., Andre, C., Belais, R., Mungongo, P., Muyembe-Tamfum, J.J., Levasseur, A., Raoult, D., Davoust, B., & Mediannikov, O. (2021). Potential zoonotic pathogens hosted by endangered bonobos. Scientific Reports, 11(1), 6331. https://doi.org/10.1038/s41598-021-85849-4

[31]

Cardeti, G., Mariano, V., Eleni, C., Aloisi, M., Grifoni, G., Sittinieri, S., Dante, G., Antognetti, V., Foglia, E.A., Cersini, A., & Nardi, A. (2016). Encephalomyocarditis virus infection in Macaca sylvanus and Hystrix cristata from an Italian rescue centre for wild and exotic animals. Virology Journal, 13(1), 193. https://doi.org/10.1186/s12985-016-0653-9

[32]

Jones, P., Cordonnier, N., Mahamba, C., Burt, F.J., Rakotovao, F., Swanepoel, R., Andre, C., Dauger, S., & Bakkali Kassimi, L. (2011). Encephalomyocarditis virus mortality in semi-wild bonobos (Pan panicus). Journal of Medical Primatology, 40(3), 157-163. https://doi.org/10.1111/j.1600-0684.2010.00464.x

[33]

Efridi, W., & Lappin, S.L. (2023). Poxviruses. StatPearls. Treasure Island (FL) ineligible companies. Disclosure: Sarah Lappin declares no relevant financial relationships with ineligible companies.

[34]

Wanzeller, A.L., Souza, A.L., Azevedo, R.S., Junior, E.C., Filho, L.C., Oliveira, R.S., Lemos, P.S., Junior, J.V., & Vasconcelos, P.F. (2017). Complete genome sequence of the BeAn 58058 virus isolated from Oryzomys sp. rodents in the amazon region of Brazil. Genome Announcements, 5(9). https://doi.org/10.1128/genomeA.01575-16

[35]

Goolam, M.T., Peters, R. P.H., Allam, M., Ismail, A., Mtshali, S., Goolam Mahomed, A., Ueckermann, V., Kock, M.M., & Ehlers, M.M. (2021). Lung microbiome of stable and exacerbated COPD patients in Tshwane, South Africa. Scientific Reports, 11(1), 19758. https://doi.org/10.1038/s41598-021-99127-w

[36]

Blanco-Picazo, P., Fernandez-Orth, D., Brown-Jaque, M., Miro, E., Espinal, P., Rodriguez-Rubio, L., Muniesa, M., & Navarro, F. (2020). Unravelling the consequences of the bacteriophages in human samples. Scientific Reports, 10(1), 6737. https://doi.org/10.1038/s41598-020-63432-7

[37]

Mollerup, S., Mikkelsen, L.H., Hansen, A.J., & Heegaard, S. (2019). High-throughput sequencing reveals no viral pathogens in eight cases of ocular adnexal extranodal marginal zone B-cell lymphoma. Experimental Eye Research, 185, 107677. https://doi.org/10.1016/j.exer.2019.05.017

[38]

Marques, J.T., Trindade, G.D., Da Fonseca, F.G., Dos Santos, J.R., Bonjardim, C.A., Ferreira, P.C., & Kroon, E.G. (2001). Characterization of ATI, TK and IFN-alpha/betaR genes in the genome of the BeAn 58058 virus, a naturally attenuated wild Orthopoxvirus. Virus Genes, 23(3), 291-301. https://doi.org/10.1023/a:1012521322845

[39]

Haller, S.L., Peng, C., McFadden, G., & Rothenburg, S. (2014). Rothenburg S. Poxviruses and the evolution of host range and virulence. Infection, Genetics and Evolution, 21, 15-40. https://doi.org/10.1016/j.meegid.2013.10.014

[40]

Shao, Y., Zhou, L., Li, F., Zhao, L., Zhang, B.L., Shao, F., Chen, J.W., Chen, C.Y., Bi, X.P., Zhuang, X.L., Zhu, H.L., Hu, J., Sun, Z.Y., Li, X., Wang, D.P., Rivas-González, I., Wang, S., Wang, Y.M., Chen, W, … Wu, D.D. (2023). Phylogenomic analyses provide insights into primate evolution. Science, 380(6648), 913-924. https://doi.org/10.1126/science.abn6919

[41]

Marti, J.M. (2019). Recentrifuge: Robust comparative analysis and contamination removal for metagenomics. PLoS Computational Biology, 15(4), e1006967. https://doi.org/10.1371/journal.pcbi.1006967

[42]

Greenwood, A.D., Ishida, Y., O'Brien, S.P., Roca, A.L., & Eiden, M.V. (2018). Transmission, evolution, and endogenization: Lessons learned from recent retroviral invasions. Microbiology and Molecular Biology Reviews, 82(1). e0004417. https://doi.org/10.1128/MMBR.00044-17

[43]

Levet, S., Charvet, B., Bertin, A., Deschaumes, A., Perron, H., & Hober, D. (2019). Human endogenous retroviruses and type 1 diabetes. Current Diabetes Reports, 19(12), 141. https://doi.org/10.1007/s11892-019-1256-9

[44]

Garcia-Montojo, M., Doucet-O'Hare, T., Henderson, L., & Nath, A. (2018). Human endogenous retrovirus-K (HML-2): A comprehensive review. Critical Reviews in Microbiology, 44(6), 715-738. https://doi.org/10.1080/1040841x.2018.1501345

[45]

van der Kuyl, A.C., Dekker, J.T., & Goudsmit, J. (1996). Baboon endogenous virus evolution and ecology. Trends in Microbiology, 4(11), 455-459. https://doi.org/10.1016/0966-842x(96)10064-0

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2024 The Author(s). Animal Research and One Health published by John Wiley & Sons Australia, Ltd on behalf of Institute of Animal Science, Chinese Academy of Agricultural Sciences.

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