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Abstract

Paramyxoviruses are a group of single-stranded, negative-sense RNA viruses, some of which are responsible for acute human disease, including parainfluenza virus, measles virus, Nipah virus and Hendra virus. In recent years, a large number of novel paramyxoviruses, particularly members of the genus , have been discovered in wild mammals, suggesting that the diversity of paramyxoviruses may be underestimated. Here we used hemi-nested reverse transcription PCR to obtain 190 paramyxovirus sequences from 969 small mammals in Hubei Province, Central China. These newly identified paramyxoviruses were classified into four clades: genera , , and , with most of them belonging to the genus . Using Illumina sequencing and Sanger sequencing, we successfully recovered six near-full-length genomes with different genomic organizations, revealing the more complex genome content of paramyxoviruses. Co-divergence analysis of jeilongviruses and their known hosts indicates that host-switching occurred more frequently in the evolutionary histories of the genus . Together, our findings demonstrate the high prevalence of paramyxoviruses in small mammals, especially jeilongviruses, and highlight the diversity of paramyxoviruses and their genome content, as well as the evolution of jeilongviruses.

Funding
This study was supported by the:
  • the Translational Medicine and Interdisciplinary Research Joint Fund of Zhongnan Hospital of Wuhan University (Award ZNLH202203)
    • Principle Award Recipient: NotApplicable
  • the Translational Medicine and Interdisciplinary Research Joint Fund of Zhongnan Hospital of Wuhan University (Award ZNLH201905)
    • Principle Award Recipient: NotApplicable
  • the Young Elite Scientist Sponsorship Program by CAST (Award YESS20200394)
    • Principle Award Recipient: Liang-junChen
  • National Key Research and Development Program of China (Award 2018YFE0204500)
    • Principle Award Recipient: Yi-rongLi
  • National Natural Science Foundation of China (Award 82000021)
    • Principle Award Recipient: Liang-junChen
  • National Natural Science Foundation of China (Award 81991220308)
    • Principle Award Recipient: WeiHou
  • National Natural Science Foundation of China (Award U20A20396)
    • Principle Award Recipient: WeiHou
  • National Key R&D Program of China (Award 2023YFC2605504)
    • Principle Award Recipient: NotApplicable
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2024-05-03
2024-05-18
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References

  1. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D et al. Global trends in emerging infectious diseases. Nature 2008; 451:990–993 [View Article] [PubMed]
    [Google Scholar]
  2. Woolhouse MEJ, Gowtage-Sequeria S. Host range and emerging and reemerging pathogens. Emerg Infect Dis 2005; 11:1842–1847 [View Article] [PubMed]
    [Google Scholar]
  3. Taylor LH, Latham SM, Woolhouse ME. Risk factors for human disease emergence. Philos Trans R Soc Lond B Biol Sci 2001; 356:983–989 [View Article] [PubMed]
    [Google Scholar]
  4. Daszak P, Cunningham AA, Hyatt AD. Emerging infectious diseases of wildlife--threats to biodiversity and human health. Science 2000; 287:443–449 [View Article] [PubMed]
    [Google Scholar]
  5. Johnson CK, Hitchens PL, Pandit PS, Rushmore J, Evans TS et al. Global shifts in mammalian population trends reveal key predictors of virus spillover risk. Proc Biol Sci 2020; 287:20192736 [View Article] [PubMed]
    [Google Scholar]
  6. Han BA, Kramer AM, Drake JM. Global patterns of zoonotic disease in mammals. Trends Parasitol 2016; 32:565–577 [View Article] [PubMed]
    [Google Scholar]
  7. Zhou P, Yang X-L, Wang X-G, Hu B, Zhang L et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 2020; 579:270–273 [View Article] [PubMed]
    [Google Scholar]
  8. Lau SKP, Woo PCY, Li KSM, Huang Y, Tsoi H-W et al. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci U S A 2005; 102:14040–14045 [View Article] [PubMed]
    [Google Scholar]
  9. Memish ZA, Mishra N, Olival KJ, Fagbo SF, Kapoor V et al. Middle East respiratory syndrome coronavirus in bats, Saudi Arabia. Emerg Infect Dis 2013; 19:1819–1823 [View Article] [PubMed]
    [Google Scholar]
  10. Clayton BA. Nipah virus: transmission of a zoonotic paramyxovirus. Curr Opin Virol 2017; 22:97–104 [View Article] [PubMed]
    [Google Scholar]
  11. Wang L-F, Anderson DE. Viruses in bats and potential spillover to animals and humans. Curr Opin Virol 2019; 34:79–89 [View Article] [PubMed]
    [Google Scholar]
  12. Thibault PA, Watkinson RE, Moreira-Soto A, Drexler JF, Lee B. Zoonotic potential of emerging paramyxoviruses: knowns and unknowns. Adv Virus Res 2017; 98:1–55 [View Article] [PubMed]
    [Google Scholar]
  13. Roeder PL, Taylor WP. Rinderpest. Vet Clin North Am Food Anim Pract 2002; 18:515–547 [View Article] [PubMed]
    [Google Scholar]
  14. Kumar N, Maherchandani S, Kashyap SK, Singh SV, Sharma S et al. Peste des petits ruminants virus infection of small ruminants: a comprehensive review. Viruses 2014; 6:2287–2327 [View Article] [PubMed]
    [Google Scholar]
  15. Branche AR, Falsey AR. Parainfluenza virus infection. Semin Respir Crit Care Med 2016; 37:538–554 [View Article] [PubMed]
    [Google Scholar]
  16. Rubin S, Eckhaus M, Rennick LJ, Bamford CGG, Duprex WP. Molecular biology, pathogenesis and pathology of mumps virus. J Pathol 2015; 235:242–252 [View Article] [PubMed]
    [Google Scholar]
  17. Rima B, Balkema-Buschmann A, Dundon WG, Duprex P, Easton A et al. ICTV virus taxonomy profile: paramyxoviridae. J Gen Virol 2019; 100:1593–1594 [View Article]
    [Google Scholar]
  18. Vanmechelen B, Meurs S, Horemans M, Loosen A, Joly Maes T et al. The characterization of multiple novel paramyxoviruses highlights the diverse nature of the subfamily Orthoparamyxovirinae. Virus Evol 2022; 8:veac061 [View Article] [PubMed]
    [Google Scholar]
  19. Larsen BB, Gryseels S, Otto HW, Worobey M. Evolution and diversity of bat and rodent paramyxoviruses from North America. J Virol 2022; 96:e0109821 [View Article] [PubMed]
    [Google Scholar]
  20. Vanmechelen B, Vergote V, Merino M, Verbeken E, Maes P. Common occurrence of Belerina virus, a novel paramyxovirus found in Belgian hedgehogs. Sci Rep 2020; 10:19341 [View Article] [PubMed]
    [Google Scholar]
  21. Choi EJ, Ortega V, Aguilar HC. Feline morbillivirus, a new paramyxovirus possibly associated with feline kidney disease. Viruses 2020; 12:501 [View Article] [PubMed]
    [Google Scholar]
  22. Darold GM, Alfieri AA, Araújo JP, da Cruz TF, Bertti KM de LB et al. High genetic diversity of paramyxoviruses infecting domestic cats in Western Brazil. Transbound Emerg Dis 2021; 68:3453–3462 [View Article] [PubMed]
    [Google Scholar]
  23. Lee S-H, No JS, Kim K, Budhathoki S, Park K et al. Novel Paju Apodemus paramyxovirus 1 and 2, harbored by Apodemus agrarius in the Republic of Korea. Virology 2021; 562:40–49 [View Article] [PubMed]
    [Google Scholar]
  24. Brooks F, Wood AR, Thomson J, Deane D, Everest DJ et al. Preliminary characterisation of Pentlands paramyxovirus-1, -2 and -3, three new paramyxoviruses of rodents. Vet Microbiol 2014; 170:391–397 [View Article] [PubMed]
    [Google Scholar]
  25. Darcissac E, Donato D, de Thoisy B, Lacoste V, Lavergne A. Paramyxovirus circulation in bat species from French Guiana. Infect Genet Evol 2021; 90:104769 [View Article] [PubMed]
    [Google Scholar]
  26. Drexler JF, Corman VM, Müller MA, Maganga GD, Vallo P et al. Bats host major mammalian paramyxoviruses. Nat Commun 2012; 3:796 [View Article] [PubMed]
    [Google Scholar]
  27. Sieg M, Heenemann K, Rückner A, Burgener I, Oechtering G et al. Discovery of new feline paramyxoviruses in domestic cats with chronic kidney disease. Virus Genes 2015; 51:294–297 [View Article] [PubMed]
    [Google Scholar]
  28. Zhang X-A, Li H, Jiang F-C, Zhu F, Zhang Y-F et al. A zoonotic henipavirus in febrile patients in China. N Engl J Med 2022; 387:470–472 [View Article] [PubMed]
    [Google Scholar]
  29. Naidu A, Fitak RR, Munguia-Vega A, Culver M. Novel primers for complete mitochondrial cytochrome b gene sequencing in mammals. Mol Ecol Resour 2012; 12:191–196 [View Article] [PubMed]
    [Google Scholar]
  30. Guo W-P, Lin X-D, Wang W, Tian J-H, Cong M-L et al. Phylogeny and origins of hantaviruses harbored by bats, insectivores, and rodents. PLoS Pathog 2013; 9:e1003159 [View Article] [PubMed]
    [Google Scholar]
  31. Chen J-J, Zhang X-A, Fan H, Jiang F-C, Jin M-Z et al. Distribution and characteristics of Beilong virus among wild rodents and shrews in China. Infect Genet Evol 2020; 85:104454 [View Article] [PubMed]
    [Google Scholar]
  32. Tong S, Chern S-WW, Li Y, Pallansch MA, Anderson LJ. Sensitive and broadly reactive reverse transcription-PCR assays to detect novel paramyxoviruses. J Clin Microbiol 2008; 46:2652–2658 [View Article] [PubMed]
    [Google Scholar]
  33. Buchfink B, Reuter K, Drost H-G. Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat Methods 2021; 18:366–368 [View Article] [PubMed]
    [Google Scholar]
  34. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article] [PubMed]
    [Google Scholar]
  35. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 2020; 37:1530–1534 [View Article] [PubMed]
    [Google Scholar]
  36. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
    [Google Scholar]
  37. Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 2007; 56:564–577 [View Article] [PubMed]
    [Google Scholar]
  38. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article] [PubMed]
    [Google Scholar]
  39. Conow C, Fielder D, Ovadia Y, Libeskind-Hadas R. Jane: a new tool for the cophylogeny reconstruction problem. Algorithms Mol Biol 2010; 5:16 [View Article] [PubMed]
    [Google Scholar]
  40. Shi M, Lin X-D, Chen X, Tian J-H, Chen L-J et al. The evolutionary history of vertebrate RNA viruses. Nature 2018; 556:197–202 [View Article] [PubMed]
    [Google Scholar]
  41. Xu X, Zhao H, Gong Z, Han G-Z. Endogenous retroviruses of non-avian/mammalian vertebrates illuminate diversity and deep history of retroviruses. PLoS Pathog 2018; 14:e1007072 [View Article] [PubMed]
    [Google Scholar]
  42. Jackson AP, Charleston MA. A cophylogenetic perspective of RNA-virus evolution. Mol Biol Evol 2004; 21:45–57 [View Article] [PubMed]
    [Google Scholar]
  43. Martin DP, Lemey P, Lott M, Moulton V, Posada D et al. RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 2010; 26:2462–2463 [View Article] [PubMed]
    [Google Scholar]
  44. Kang H, Zhou L, Xu S, Yuen K-Y, Wah TH et al. The C-Terminal 300 amino acid residues of the G protein and putative open reading frame X of the G gene of tailam paramyxovirus (TlmPV) are not required for replication in tissue culture cells. J Virol 2023; 97:e0180222 [View Article] [PubMed]
    [Google Scholar]
  45. Vanmechelen B, Bletsa M, Laenen L, Lopes AR, Vergote V et al. Discovery and genome characterization of three new Jeilongviruses, a lineage of paramyxoviruses characterized by their unique membrane proteins. BMC Genomics 2018; 19:617 [View Article] [PubMed]
    [Google Scholar]
  46. Han BA, Schmidt JP, Bowden SE, Drake JM. Rodent reservoirs of future zoonotic diseases. Proc Natl Acad Sci U S A 2015; 112:7039–7044 [View Article] [PubMed]
    [Google Scholar]
  47. Zhang Y, Zhang J, Wang Y, Tian F, Zhang X et al. Genetic diversity and expanded host range of J paramyxovirus detected in wild small mammals in China. Viruses 2022; 15:49 [View Article] [PubMed]
    [Google Scholar]
  48. Sasaki M, Muleya W, Ishii A, Orba Y, Hang’ombe BM et al. Molecular epidemiology of paramyxoviruses in Zambian wild rodents and shrews. J Gen Virol 2014; 95:325–330 [View Article] [PubMed]
    [Google Scholar]
  49. Wilkinson DA, Temmam S, Lebarbenchon C, Lagadec E, Chotte J et al. Identification of novel paramyxoviruses in insectivorous bats of the Southwest Indian Ocean. Virus Res 2012; 170:159–163 [View Article] [PubMed]
    [Google Scholar]
  50. Wilkinson DA, Mélade J, Dietrich M, Ramasindrazana B, Soarimalala V et al. Highly diverse morbillivirus-related paramyxoviruses in wild fauna of the southwestern Indian Ocean Islands: evidence of exchange between introduced and endemic small mammals. J Virol 2014; 88:8268–8277 [View Article] [PubMed]
    [Google Scholar]
  51. Zhu W, Huang Y, Yu X, Chen H, Li D et al. Discovery and evolutionary analysis of a novel bat-borne paramyxovirus. Viruses 2022; 14:288 [View Article] [PubMed]
    [Google Scholar]
  52. Nie S-M, Li J, Wang Y-T, An C-H, Zhou H et al. Novel astrovirus and paramyxovirus in Mongolian gerbils (Meriones unguiculatus) from China. Zool Res 2022; 43:418–422 [View Article] [PubMed]
    [Google Scholar]
  53. Debat HJ. A South American mouse morbillivirus provides insight into a clade of rodent-borne morbilliviruses. Viruses 2022; 14:2403 [View Article] [PubMed]
    [Google Scholar]
  54. Wu Z, Yang L, Yang F, Ren X, Jiang J et al. Novel Henipa-like virus, mojiang paramyxovirus, in rats, China, 2012. Emerg Infect Dis 2014; 20:1064–1066 [View Article] [PubMed]
    [Google Scholar]
  55. Jack PJM, Anderson DE, Bossart KN, Marsh GA, Yu M et al. Expression of novel genes encoded by the paramyxovirus J virus. J Gen Virol 2008; 89:1434–1441 [View Article] [PubMed]
    [Google Scholar]
  56. Shi M, Lin X-D, Tian J-H, Chen L-J, Chen X et al. Redefining the invertebrate RNA virosphere. Nature 2016; 540:539–543 [View Article] [PubMed]
    [Google Scholar]
  57. Liang J, Zhu C, Zhang L. Cospeciation of coronavirus and paramyxovirus with their bat hosts in the same geographical areas. BMC Ecol Evol 2021; 21:148 [View Article] [PubMed]
    [Google Scholar]
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