Virome in healthy pangolins reveals compatibility with multiple potentially zoonotic viruses

Feng-Juan Tian; Jing Li; Wen-Li Liu; Yu-Jie Liu; Yun-Jia Hu; Qi-Hang Tu; Yang Li; Yu Bai; Mang Shi; Teng-Cheng Que; Yan-Ling Hu; Yi-Gang Tong

doi:10.24272/j.issn.2095-8137.2022.246

Volume 43 Issue 6

Nov. 2022

Turn off MathJax

Article Contents

Article Navigation > Zoological Research > 2022 > 43(6): 977-988

Feng-Juan Tian, Jing Li, Wen-Li Liu, Yu-Jie Liu, Yun-Jia Hu, Qi-Hang Tu, Yang Li, Yu Bai, Mang Shi, Teng-Cheng Que, Yan-Ling Hu, Yi-Gang Tong. Virome in healthy pangolins reveals compatibility with multiple potentially zoonotic viruses. Zoological Research, 2022, 43(6): 977-988. doi: 10.24272/j.issn.2095-8137.2022.246

Citation:

Feng-Juan Tian, Jing Li, Wen-Li Liu, Yu-Jie Liu, Yun-Jia Hu, Qi-Hang Tu, Yang Li, Yu Bai, Mang Shi, Teng-Cheng Que, Yan-Ling Hu, Yi-Gang Tong. Virome in healthy pangolins reveals compatibility with multiple potentially zoonotic viruses. Zoological Research, 2022, 43(6): 977-988. doi: 10.24272/j.issn.2095-8137.2022.246

Citation:

Feng-Juan Tian, Jing Li, Wen-Li Liu, Yu-Jie Liu, Yun-Jia Hu, Qi-Hang Tu, Yang Li, Yu Bai, Mang Shi, Teng-Cheng Que, Yan-Ling Hu, Yi-Gang Tong. Virome in healthy pangolins reveals compatibility with multiple potentially zoonotic viruses. Zoological Research, 2022, 43(6): 977-988. doi: 10.24272/j.issn.2095-8137.2022.246

PDF( 6520 KB)

Virome in healthy pangolins reveals compatibility with multiple potentially zoonotic viruses

doi: 10.24272/j.issn.2095-8137.2022.246

Feng-Juan Tian^{1, #},
Jing Li^{1, #},
Wen-Li Liu¹,
Yu-Jie Liu¹,
Yun-Jia Hu¹,
Qi-Hang Tu¹,
Yang Li¹,
Yu Bai¹,
Mang Shi^{2
,
,},
Teng-Cheng Que^{3, 4
,
,},
Yan-Ling Hu^{5, 6
,
,},
Yi-Gang Tong^{1
,
,}

1.
College of Life Science and Technology, Beijing University of Chemical Technology, Beijing 100029, China
2.
Centre for Infection and Immunity Studies, School of Medicine, Shenzhen Campus of Sun Yat-Sen University, Sun Yat-Sen University, Shenzhen, Guangdong 518107, China
3.
Faculty of Data Science, City University of Macau, Macau 999078, China
4.
Guangxi Zhuang Autonomous Terrestrial Wildlife Rescue Research and Epidemic Diseases Monitoring Center, Nanning, Guangxi 530025, China
5.
Life Sciences Institute, Guangxi Medical University, Nanning, Guangxi 530021, China
6.
Center for Genomic and Personalized Medicine, Guangxi Medical University, Nanning, Guangxi 530021, China

The data that support our findings were deposited in the NCBI database under BioProjectID PRJNA881017, as well as the Genome Sequence Archive (GSA) under accession no. PRJCA010128, and the Science Data Bank under DOI:10.57760/sciencedb.j00139.00041. The consensus sequences in this study were deposited in GenBank under accession numbers OP474153–OP474178 and in the NGDC Genome Warehouse (GWH) (https://ngdc.cncb.ac.cn/gwh/) under accession numbers GWHBJSI01000000–GWHBJTI01000000 (Supplementary Table S2).
Supplementary data to this article can be found online.
The authors declare that they have no competing interests.
Y.G.T., M.S., T.C.Q., and Y.L.H. designed and supervised the research. T.C.Q. collected the samples. W.L.L., Y.J.L., Y.J.H., Q.H.T., Y.L., and Y.B. processed the samples. F.J.T. and J.L. performed data analysis, genome assembly, and phylogenetic analysis and contributed to data interpretation and wrote the paper. Y.G.T., M.S., T.C.Q., and Y.L.H. edited the paper. All authors read and approved the final version of the manuscript.
#Authors contributed equally to this work

Funds: This study was supported by the State Key Research Development Program of China (2019YFC1200500, 2019YFC1200502), National Key Research and Development Program of China (2018YFA0903000, 2020YFC2005405, 2020YFA0712100, 2020YFC0840805, 2021YFC0863400) and Key Project of Beijing University of Chemical Technology (XK1803-06)

More Information

Corresponding author: E-mail: shim23@mail.sysu.edu.cn; qtchpost@163.com; huyanling@gxmu.edu.cn; tongyigang@buct.edu.cn
Received Date: 2022-08-27
Accepted Date: 2022-10-09

Published Online: 2022-10-09

Publish Date: 2022-11-18

Abstract

Abstract

Previous studies have identified multiple viruses in dead or severely diseased pangolins, but descriptions of the virome in healthy pangolins are lacking. This poses a greater risk of cross-species transmission due to poor preventive awareness and frequent interactions with breeders. In this study, we investigated the viral composition of 34 pangolins with no signs of disease at the time of sampling and characterized a large number of arthropod-associated viruses belonging to 11 families and vertebrate viruses belonging to eight families, including those with pathogenic potential in humans and animals. Several important vertebrate viruses were identified in the pangolins, including parvovirus, pestivirus, and picobirnavirus. The picobirnavirus was clustered with human and grey teal picobirnaviruses. Viruses with cross-species transmission ability were also identified, including circovirus, rotavirus, and astrovirus. Our study revealed that pangolins are frequently exposed to arthropod-associated viruses in the wild and can carry many vertebrate viruses under natural conditions. This study provides important insights into the virome of pangolins, underscoring the importance of monitoring potential pathogens in healthy pangolins to prevent outbreaks of infectious diseases in domesticated animals and humans.
- Pangolin,
- Virome,
- Arthropod-associated viruses,
- Cross-species transmission,
- Zoonoses

FullText(HTML)

References(45)

References

[1]	Berg MG, Forberg K, Perez LJ, Luk KC, Meyer TV, Cloherty GA. 2021. Emergence of a distinct picobirnavirus genotype circulating in patients hospitalized with acute respiratory illness. Viruses, 13(12): 2534. doi: 10.3390/v13122534
[2]	Buchfink B, Xie C, Huson DH. 2015. Fast and sensitive protein alignment using DIAMOND. Nature Methods, 12(1): 59−60. doi: 10.1038/nmeth.3176
[3]	CDC. 2021. Zoonotic Diseases.
[4]	Chen SF, Zhou YQ, Chen YR, Gu J. 2018. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 34(17): i884−i890. doi: 10.1093/bioinformatics/bty560
[5]	Choo SW, Rayko M, Tan TK, Hari R, Komissarov A, Wee WY, et al. 2016. Pangolin genomes and the evolution of mammalian scales and immunity. Genome Research, 26(10): 1312−1322. doi: 10.1101/gr.203521.115
[6]	Cotmore SF, Agbandje-McKenna M, Canuti M, Chiorini JA, Eis-Hubinger AM, Hughes J, et al. 2019. ICTV virus taxonomy profile: parvoviridae. Journal of General Virology, 100(3): 367−368. doi: 10.1099/jgv.0.001212
[7]	Gao WH, Lin XD, Chen YM, Xie CG, Tan ZZ, Zhou JJ, et al. 2020. Newly identified viral genomes in pangolins with fatal disease. Virus Evolution, 6(1): veaa020. doi: 10.1093/ve/veaa020
[8]	Ghosh S, Kobayashi N. 2014. Exotic rotaviruses in animals and rotaviruses in exotic animals. Virusdisease, 25(2): 158−172. doi: 10.1007/s13337-014-0194-z
[9]	Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59(3): 307−321. doi: 10.1093/sysbio/syq010
[10]	Haley PJ. 2022. From bats to pangolins: new insights into species differences in the structure and function of the immune system. Innate Immunity, 28(3–4): 107–121.
[11]	Harrison RL, Herniou EA, Jehle JA, Theilmann DA, Burand JP, Becnel JJ, et al. 2018. ICTV virus taxonomy profile: baculoviridae. Journal of General Virology, 99(9): 1185–1186.
[12]	Harvey E, Holmes EC. 2022. Diversity and evolution of the animal virome. Nature Reviews Microbiology, 20(6): 321−334. doi: 10.1038/s41579-021-00665-x
[13]	Hassan M, Sulaiman MH, Lian CJ. 2013. The prevalence and intensity of Amblyomma javanense infestation on Malayan pangolins (Manis javanica Desmarest) from Peninsular Malaysia. Acta Tropica, 126(2): 142−145. doi: 10.1016/j.actatropica.2013.02.001
[14]	Hassanin A, Tu VT, Curaudeau M, Csorba G. 2021. Inferring the ecological niche of bat viruses closely related to SARS-CoV-2 using phylogeographic analyses of Rhinolophus species. Scientific Reports, 11(1): 14276. doi: 10.1038/s41598-021-93738-z
[15]	He WT, Hou X, Zhao J, Sun JM, He HJ, Si W, et al. 2022. Virome characterization of game animals in China reveals a spectrum of emerging pathogens. Cell, 185(7): 1117−1129.E8. doi: 10.1016/j.cell.2022.02.014
[16]	Heath M, Coulson I. 1997. Home range size and distribution in a wild population of Cape pangolins, Manis temminckii, in north-west Zimbabwe. African Journal of Ecology, 35(2): 94−109. doi: 10.1111/j.1365-2028.1997.080-89080.x
[17]	Huaman JL, Pacioni C, Sarker S, Doyle M, Forsyth DM, Pople A, et al. 2021. Molecular epidemiology and characterization of picobirnavirus in wild deer and cattle from australia: evidence of genogroup I and II in the upper respiratory Tract. Viruses, 13(8): 1492. doi: 10.3390/v13081492
[18]	Islam A, Ferdous J, Islam S, Sayeed A, Rahman K, Saha O, et al. 2021. Transmission dynamics and susceptibility patterns of SARS-CoV-2 in domestic, farmed and wild animals: Sustainable One Health surveillance for conservation and public health to prevent future epidemics and pandemics. Transboundary and Emerging Diseases,doi: 10.1111/tbed.14356.
[19]	Kashnikov AY, Epifanova NV, Novikova NA. 2020. Picobirnaviruses: prevalence, genetic diversity, detection methods. Vavilov Journal of Genetics and Breeding, 24(6): 661−672. doi: 10.18699/VJ20.660
[20]	Katoh K, Misawa K, Kuma KI, Miyata T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30(14): 3059−3066. doi: 10.1093/nar/gkf436
[21]	Lam TTY, Jia N, Zhang YW, Shum MHH, Jiang JF, Zhu HC, et al. 2020. Identifying SARS-CoV-2-related coronaviruses in Malayan pangolins. Nature, 583(7815): 282−285. doi: 10.1038/s41586-020-2169-0
[22]	Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods, 9(4): 357−359. doi: 10.1038/nmeth.1923
[23]	Li DH, Liu CM, Luo RB, Sadakane K, Lam TW. 2015. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics, 31(10): 1674–1676.
[24]	Li DH, Luo RB, Liu CM, Leung CM, Ting HF, Sadakane K, et al. 2016. MEGAHIT v1.0: a fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods, 102: 3−11. doi: 10.1016/j.ymeth.2016.02.020
[25]	Liu P, Chen W, Chen JP. 2019. Viral metagenomics revealed sendai virus and coronavirus infection of malayan pangolins (Manis javanica). Viruses, 11(11): 979. doi: 10.3390/v11110979
[26]	Navarro R, Yibin C, Nair R, Peda A, Aung MS, Ketzis J, et al. 2017. Molecular characterization of complete genomic segment-2 of picobirnavirus strains detected in a cat and a dog. Infection, Genetics and Evolution, 54: 200−204. doi: 10.1016/j.meegid.2017.07.006
[27]	Nga NTT, Latinne A, Thuy HB, Van Long N, Ngoc PTB, Anh NTL, et al. 2022. Evidence of SARS-CoV-2 related coronaviruses circulating in sunda pangolins (Manis javanica) confiscated from the illegal wildlife trade in viet nam. Frontiers in Public Health, 10: 826116. doi: 10.3389/fpubh.2022.826116
[28]	Ning SY, Dai ZY, Zhao CY, Feng ZH, Jin KX, Yang SX, et al. 2022. Novel putative pathogenic viruses identified in pangolins by mining metagenomic data. Journal of Medical Virology, 94(6): 2500−2509. doi: 10.1002/jmv.27564
[29]	Olendraite I, Brown K, Valles SM, Firth AE, Chen YP, Guérin DMA, et al. 2019. ICTV virus taxonomy profile: Polycipiviridae. Journal of General Virology, 100(4): 554–555.
[30]	Peng MS, Li JB, Cai ZF, Liu H, Tang XL, Ying RC, et al. 2021. The high diversity of SARS-CoV-2-related coronaviruses in pangolins alerts potential ecological risks. Zoological Research, 42(6): 834−844.
[31]	Que TC, Li J, He YG, Chen PY, Lin W, He MH, et al. 2022. Human parainfluenza 3 and respiratory syncytial viruses detected in pangolins. Emerging Microbes & Infections, 11(1): 1657−1663.
[32]	Schweizer M, Peterhans E. 2014. Pestiviruses. Annual Review of Animal Biosciences, 2: 141−163. doi: 10.1146/annurev-animal-022513-114209
[33]	Shi WQ, Shi M, Que TC, Cui XM, Ye RZ, Xia LY, et al. 2022. Trafficked Malayan pangolins contain viral pathogens of humans. Nature Microbiology, 7(8): 1259−1269. doi: 10.1038/s41564-022-01181-1
[34]	Simmonds P, Becher P, Bukh J, Gould EA, Meyers G, Monath T, et al. 2017. ICTV virus taxonomy profile: Flaviviridae. Journal of General Virology, 98(1): 2–3.
[35]	Stoltz DB, Krell P, Summers MD, Vinson SB. 1984. Polydnaviridae - a proposed family of insect viruses with segmented, double-stranded, circular DNA genomes. Intervirology, 21(1): 1−4. doi: 10.1159/000149497
[36]	Valles SM, Chen Y, Firth AE, Guérin DMA, Hashimoto Y, Herrero S, et al. 2017. ICTV virus taxonomy profile: Dicistroviridae. Journal of General Virology, 98(3): 355–356.
[37]	Walker PJ, Blasdell KR, Calisher CH, Dietzgen RG, Kondo H, Kurath G, et al. 2018. ICTV virus taxonomy profile: Rhabdoviridae. Journal of General Virology, 99(4): 447–448.
[38]	Wang SL, Tu YC, Lee MS, Wu LH, Chen TY, Wu CH, et al. 2020. Fatal canine parvovirus-2 (CPV-2) infection in a rescued free-ranging Taiwanese pangolin (Manis pentadactyla pentadactyla). Transboundary and Emerging Diseases, 67(3): 1074−1081. doi: 10.1111/tbed.13469
[39]	Wang XH, Chen W, Xiang R, Li LM, Chen J, Zhong RQ, et al. 2019. Complete genome sequence of parainfluenza virus 5 (PIV5) from a sunda pangolin (Manis javanica) in China. Journal of Wildlife Diseases, 55(4): 947−950. doi: 10.7589/2018-09-211
[40]	Xiao KP, Zhai JQ, Feng YY, Zhou N, Zhang X, Zou JJ, et al. 2020. Isolation of SARS-CoV-2-related coronavirus from Malayan pangolins. Nature, 583(7815): 286−289. doi: 10.1038/s41586-020-2313-x
[41]	Yang SX, Shan TL, Xiao YQ, Zhang HT, Wang XC, Shen Q, et al. 2021. Digging metagenomic data of pangolins revealed SARS-CoV-2 related viruses and other significant viruses. Journal of Medical Virology, 93(3): 1786−1791. doi: 10.1002/jmv.26524
[42]	Ye RZ, Que TC, Xia LY, Cui XM, Zhang YW, Jiang JF, et al. 2022. Natural infection of pangolins with human respiratory syncytial viruses. Current Biology, 32(7): R307−R308. doi: 10.1016/j.cub.2022.02.057
[43]	Zhai SL, Lu SS, Wei WK, Lv DH, Wen XH, Zhai Q, et al. 2019. Reservoirs of porcine circoviruses: a mini review. Frontiers in Veterinary Science, 6: 319. doi: 10.3389/fvets.2019.00319
[44]	Zhang YZ, Shi M, Holmes EC. 2018. Using metagenomics to characterize an expanding virosphere. Cell, 172(6): 1168−1172. doi: 10.1016/j.cell.2018.02.043
[45]	Zhao M, Yue CJ, Yang ZJ, Li YL, Zhang DS, Zhang J, et al. 2022. Viral metagenomics unveiled extensive communications of viruses within giant pandas and their associated organisms in the same ecosystem. Science of the Total Environment, 820: 153317. doi: 10.1016/j.scitotenv.2022.153317