1887

Abstract

The carcass of an Australian little red flying fox () which died following entrapment on a fence was submitted to the laboratory for Australian bat lyssavirus exclusion testing, which was negative. During post-mortem, multiple nodules were noted on the wing membranes, and therefore degenerate PCR primers targeting the poxvirus DNA polymerase gene were used to screen for poxviruses. The poxvirus PCR screen was positive and sequencing of the PCR product demonstrated very low, but significant, similarity with the DNA polymerase gene from members of the family. Next-generation sequencing of DNA extracted from the lesions returned a contig of 132 353 nucleotides (nt), which was further extended to produce a near full-length viral genome of 133 492 nt. Analysis of the genome revealed it to be AT-rich with inverted terminal repeats of at least 1314 nt and to contain 143 predicted genes. The genome contains a surprisingly large number (29) of genes not found in other poxviruses, one of which appears to be a homologue of the mammalian TNF-related apoptosis-inducing ligand (TRAIL) gene. Phylogenetic analysis indicates that the poxvirus described here is not closely related to any other poxvirus isolated from bats or other species, and that it likely should be placed in a new genus.

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2016-09-01
2021-07-29
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References

  1. Afonso C. L., Tulman E. R., Lu Z., Oma E., Kutish G. F., Rock D. L. 1999; The genome of Melanoplus sanguinipes entomopoxvirus. J Virol 73:533–552[PubMed]
    [Google Scholar]
  2. Afonso C. L., Tulman E. R., Lu Z., Zsak L., Osorio F. A., Balinsky C., Kutish G. F., Rock D. L. 2002; The genome of swinepox virus. J Virol 76:783–790 [View Article][PubMed]
    [Google Scholar]
  3. Agnarsson I., Zambrana-Torrelio C. M., Flores-Saldana N. P., May-Collado L. J. 2011; A time-calibrated species-level phylogeny of bats (Chiroptera, Mammalia). PLoS Curr 3:RRN1212 [View Article][PubMed]
    [Google Scholar]
  4. Babkin I. V., Babkina I. N. 2015; The origin of the variola virus. Viruses 7:1100–1112 [View Article][PubMed]
    [Google Scholar]
  5. Baker K. S., Leggett R. M., Bexfield N. H., Alston M., Daly G., Todd S., Tachedjian M., Holmes C. E., Crameri S. et al. 2013; Metagenomic study of the viruses of African straw-coloured fruit bats: detection of a chiropteran poxvirus and isolation of a novel adenovirus. Virology 441:95–106 [View Article][PubMed]
    [Google Scholar]
  6. Bolte A. L., Meurer J., Kaleta E. F. 1999; Avian host spectrum of avipoxviruses. Avian Pathol 28:415–432 [View Article][PubMed]
    [Google Scholar]
  7. Breese M. R., Liu Y. 2013; NGSUtils: a software suite for analyzing and manipulating next-generation sequencing datasets. Bioinformatics 29:494–496 [View Article][PubMed]
    [Google Scholar]
  8. Brodie R., Roper R. L., Upton C. 2004a; JDotter: a Java interface to multiple dotplots generated by dotter. Bioinformatics 20:279–281 [View Article]
    [Google Scholar]
  9. Brodie R., Smith A. J., Roper R. L., Tcherepanov V., Upton C. 2004b; Base-By-Base: single nucleotide-level analysis of whole viral genome alignments. BMC Bioinform 5:1–9 [CrossRef]
    [Google Scholar]
  10. Buller R. M., Chakrabarti S., Moss B., Fredrickson T. 1988; Cell proliferative response to vaccinia virus is mediated by VGF. Virology 164:182–192 [View Article][PubMed]
    [Google Scholar]
  11. Chen N., Danila M. I., Feng Z., Buller R. M., Wang C., Han X., Lefkowitz E. J., Upton C. 2003; The genomic sequence of ectromelia virus, the causative agent of mousepox. Virology 317:165–186 [View Article][PubMed]
    [Google Scholar]
  12. Chevreux B., Pfisterer T., Drescher B., Driesel A. J., Müller W. E., Wetter T., Suhai S. 2004; Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res 14:1147–1159 [View Article][PubMed]
    [Google Scholar]
  13. Chua K. B., Lek Koh C., Hooi P. S., Wee K. F., Khong J. H., Chua B. H., Chan Y. P., Lim M. E., Lam S. K. 2002; Isolation of nipah virus from Malaysian Island flying-foxes. Microb Infect 4:145–151 [View Article]
    [Google Scholar]
  14. Dacheux L., Cervantes-Gonzalez M., Guigon G., Thiberge J. M., Vandenbogaert M., Maufrais C., Caro V., Bourhy H. 2014; A preliminary study of viral metagenomics of French bat species in contact with humans: identification of new mammalian viruses. PLoS One 9:e87194 [View Article][PubMed]
    [Google Scholar]
  15. Darby A. C., McInnes C. J., Kjaer K. H., Wood A. R., Hughes M., Martensen P. M., Radford A. D., Hall N., Chantrey J. 2014; Novel host-related virulence factors are encoded by squirrelpox virus, the main causative agent of epidemic disease in red squirrels in the UK. PLoS One 9:e96439 [View Article][PubMed]
    [Google Scholar]
  16. Dobson L., Reményi I., Tusnády G. E. 2015; CCTOP: a Consensus Constrained TOPology prediction web server. Nucleic Acids Res 43:W408–W412 [View Article][PubMed]
    [Google Scholar]
  17. Ehlers A., Osborne J., Slack S., Roper R. L., Upton C. 2002; Poxvirus orthologous clusters (POCs). Bioinformatics 18:1544–1545 [View Article][PubMed]
    [Google Scholar]
  18. Emerson G. L., Nordhausen R., Garner M. M., Huckabee J. R., Johnson S., Wohrle R. D., Davidson W. B., Wilkins K., Li Y. et al. 2013; Novel poxvirus in big brown bats, northwestern United States. Emerg Infect Dis 19:1002–1004 [View Article][PubMed]
    [Google Scholar]
  19. Frick W. F., Puechmaille S. J., Hoyt J. R., Nickel B. A., Langwig K. E., Foster J. T., Barlow K. E., Bartonička T., Feller D. et al. 2015; Disease alters macroecological patterns of North American bats. Global Ecol Biogeogr 24:741–749 [View Article]
    [Google Scholar]
  20. Gammon D. B., Gowrishankar B., Duraffour S., Andrei G., Upton C., Evans D. H. 2010; Vaccinia virus-encoded ribonucleotide reductase subunits are differentially required for replication and pathogenesis. PLoS Pathog 6:e1000984 [View Article][PubMed]
    [Google Scholar]
  21. Ge X. Y., Li J. L., Yang X. L., Chmura A. A., Zhu G., Epstein J. H., Mazet J. K., Hu B., Zhang W. et al. 2013; Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 503:535–538 [View Article][PubMed]
    [Google Scholar]
  22. Ge X. Y., Wang N., Zhang W., Hu B., Li B., Zhang Y. Z., Zhou J. H., Luo C. M., Yang X. L. et al. 2016; Coexistence of multiple coronaviruses in several bat colonies in an abandoned mineshaft. Virol Sin 31:31–40 [View Article][PubMed]
    [Google Scholar]
  23. Gjessing M. C., Yutin N., Tengs T., Senkevich T., Koonin E., Rønning H. P., Alarcon M., Ylving S., Lie K. I. et al. 2015; Salmon gill poxvirus, the deepest representative of the chordopoxvirinae. J Virol 89:9348–9367 [View Article][PubMed]
    [Google Scholar]
  24. Gonzalvez F., Ashkenazi A. 2010; New insights into apoptosis signaling by Apo2L/TRAIL. Oncogene 29:4752–4765 [View Article][PubMed]
    [Google Scholar]
  25. Gould A. R., Hyatt A. D., Lunt R., Kattenbelt J. A., Hengstberger S., Blacksell S. D. 1998; Characterisation of a novel lyssavirus isolated from Pteropid bats in Australia. Virus Res 54:165–187 [View Article][PubMed]
    [Google Scholar]
  26. Guyatt K. J., Twin J., Davis P., Holmes E. C., Smith G. A., Smith I. L., Mackenzie J. S., Young P. L. 2003; A molecular epidemiological study of Australian bat lyssavirus. J Gen Virol 84:485–496 [View Article][PubMed]
    [Google Scholar]
  27. Halpin K., Young P. L., Field H. E., Mackenzie J. S. 2000; Isolation of hendra virus from pteropid bats: a natural reservoir of Hendra virus. J Gen Virol 81:1927–1932 [View Article][PubMed]
    [Google Scholar]
  28. Han H. J., Wen H. L., Zhou C. M., Chen F. F., Luo L. M., Liu J. W., Yu X. J. 2015; Bats as reservoirs of severe emerging infectious diseases. Virus Res 205:1–6 [View Article][PubMed]
    [Google Scholar]
  29. Herbert M. H., Squire C. J., Mercer A. A. 2015; Poxviral ankyrin proteins. Viruses 7:709–738 [View Article][PubMed]
    [Google Scholar]
  30. Hillary W., Lin S. H., Upton C. 2011; Base-By-Base version 2: single nucleotide-level analysis of whole viral genome alignments. Microb Inform Exp 1:2 [View Article][PubMed]
    [Google Scholar]
  31. Hymowitz S. G., Christinger H. W., Fuh G., Ultsch M., O'Connell M., Kelley R. F., Ashkenazi A., de Vos A. M. 1999; Triggering cell death: the crystal structure of Apo2L/TRAIL in a complex with death receptor 5. Mol Cell 4:563–571[PubMed] [CrossRef]
    [Google Scholar]
  32. Hymowitz S. G., O'Connell M. P., Ultsch M. H., Hurst A., Totpal K., Ashkenazi A., de Vos A. M., Kelley R. F. 2000; A unique zinc-binding site revealed by a high-resolution X-ray structure of homotrimeric Apo2L/TRAIL. Biochemistry 39:633–640 [View Article][PubMed]
    [Google Scholar]
  33. ICTV 2012; Family – Poxviridae. In Virus Taxonomy Edited by King A. M. Q., Adams M. J., Carstens E. B., Lefkowitz E. J. San Diego: Elsevier;
    [Google Scholar]
  34. Katoh K., Asimenos G., Toh H. 2009; Multiple alignment of DNA sequences with MAFFT. Methods Mol Biol 537:39–64 [View Article][PubMed]
    [Google Scholar]
  35. Kim D. E., Chivian D., Baker D. 2004; Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res 32:W526–531 [View Article][PubMed]
    [Google Scholar]
  36. Le Goff C., Lamien C. E., Fakhfakh E., Chadeyras A., Aba-Adulugba E., Libeau G., Tuppurainen E., Wallace D. B., Adam T. et al. 2009; Capripoxvirus G-protein-coupled chemokine receptor: a host-range gene suitable for virus animal origin discrimination. J Gen Virol 90:1967–1977 [View Article][PubMed]
    [Google Scholar]
  37. Leroy E. M., Kumulungui B., Pourrut X., Rouquet P., Hassanin A., Yaba P., Délicat A., Paweska J. T., Gonzalez J. P., Swanepoel R. 2005; Fruit bats as reservoirs of Ebola virus. Nature 438:575–576 [View Article][PubMed]
    [Google Scholar]
  38. Leroy E. M., Epelboin A., Mondonge V., Pourrut X., Gonzalez J.-P., Muyembe-Tamfum J.-J., Formenty P. 2009; Human ebola outbreak resulting from direct exposure to fruit bats in luebo, democratic republic of congo, 2007. Vector Borne Zoonotic Dis 9:723–728 [View Article]
    [Google Scholar]
  39. Li H., Durbin R. 2009; Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760 [View Article][PubMed]
    [Google Scholar]
  40. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R. 2009; The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078–2079 [View Article][PubMed]
    [Google Scholar]
  41. Mariani S. M., Krammer P. H. 1998; Differential regulation of TRAIL and CD95 ligand in transformed cells of the T and B lymphocyte lineage. Eur J Immunol 28:973–982 [View Article][PubMed]
    [Google Scholar]
  42. Mavrommatis E., Fish E. N., Platanias L. C. 2013; The schlafen family of proteins and their regulation by interferons. J Interferon Cytokine Res 33:206–210 [View Article][PubMed]
    [Google Scholar]
  43. McFadden G. 2005; Poxvirus tropism. Nat Rev Microbiol 3:201–213 [View Article][PubMed]
    [Google Scholar]
  44. McKelvey T. A., Andrews S. C., Miller S. E., Ray C. A., Pickup D. J. 2002; Identification of the orthopoxvirus p4c gene, which encodes a structural protein that directs intracellular mature virus particles into A-type inclusions. J Virol 76:11216–11225 [View Article][PubMed]
    [Google Scholar]
  45. Memish Z. A., Mishra N., Olival K. J., Fagbo S. F., Kapoor V., Epstein J. H., Alhakeem R., Durosinloun A., Al Asmari M. et al. 2013; Middle East respiratory syndrome coronavirus in bats, Saudi Arabia. Emerg Infect Dis 19:1819–1823 [View Article][PubMed]
    [Google Scholar]
  46. Mercer A. A., Fleming S. B., Ueda N. 2005; F-box-like domains are present in most poxvirus ankyrin repeat proteins. Virus Genes 31:127–133 [View Article][PubMed]
    [Google Scholar]
  47. Milne I., Stephen G., Bayer M., Cock P. J., Pritchard L., Cardle L., Shaw P. D., Marshall D. 2013; Using tablet for visual exploration of second – generation sequencing data. Brief Bioinform 14:193–202 [View Article][PubMed]
    [Google Scholar]
  48. Mongkolsapaya J., Grimes J. M., Chen N., Xu X. N., Stuart D. I., Jones E. Y., Screaton G. R. 1999; Structure of the TRAIL-DR5 complex reveals mechanisms conferring specificity in apoptotic initiation. Nat Struct Biol 6:1048–1053 [View Article][PubMed]
    [Google Scholar]
  49. Mortlock M., Kuzmin I. V., Weyer J., Gilbert A. T., Agwanda B., Rupprecht C. E., Nel L. H., Kearney T., Malekani J. M., Markotter W. 2015; Novel paramyxoviruses in bats from sub-Saharan Africa, 2007–2012. Emerg Infect Dis 21:1840–1843 [CrossRef]
    [Google Scholar]
  50. Nelson C. A., Epperson M. L., Singh S., Elliott J. I., Fremont D. H. 2015; Structural conservation and functional diversity of the poxvirus immune evasion (PIE) domain superfamily. Viruses 7:4878–4898 [View Article][PubMed]
    [Google Scholar]
  51. Nemčovičová I., Benedict C. A., Zajonc D. M. 2013; Structure of human cytomegalovirus UL141 binding to TRAIL-R2 reveals novel, non-canonical death receptor interactions. PLoS Pathog 9:e1003224 [View Article][PubMed]
    [Google Scholar]
  52. Ouyang P., Rakus K., van Beurden S. J., Westphal A. H., Davison A. J., Gatherer D., Vanderplasschen A. F. 2014; IL-10 encoded by viruses: a remarkable example of independent acquisition of a cellular gene by viruses and its subsequent evolution in the viral genome. J Gen Virol 95:245–262 [View Article][PubMed]
    [Google Scholar]
  53. Perdiguero B., Esteban M. 2009; The interferon system and vaccinia virus evasion mechanisms. J Interferon Cytokine Res 29:581–598 [View Article][PubMed]
    [Google Scholar]
  54. Pettersen E. F., Goddard T. D., Huang C. C., Couch G. S., Greenblatt D. M., Meng E. C., Ferrin T. E. 2004; UCSF Chimera – a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612 [View Article][PubMed]
    [Google Scholar]
  55. Rehm K. E., Connor R. F., Jones G. J., Yimbu K., Roper R. L. 2010; Vaccinia virus A35R inhibits MHC class II antigen presentation. Virology 397:176–186 [View Article][PubMed]
    [Google Scholar]
  56. Rodhain E. 2015; Bats and Viruses: complex relationships. Bull Soc Pathol Exot 108:272–289 [View Article][PubMed]
    [Google Scholar]
  57. Sano K., Okazaki S., Taniguchi S., Masangkay J. S., Puentespina R., Eres E., Cosico E., Quibod N., Kondo T. et al. 2015; Detection of a novel herpesvirus from bats in the Philippines. Virus Genes 51:136–139 [View Article][PubMed]
    [Google Scholar]
  58. Smith G. L., Vanderplasschen A., Law M. 2002; The formation and function of extracellular enveloped vaccinia virus. J Gen Virol 83:2915–2931 [View Article][PubMed]
    [Google Scholar]
  59. Springer M. S. 2013; Phylogenetics: bats united, microbats divided. Curr Biol 23:R999–R1001 [View Article][PubMed]
    [Google Scholar]
  60. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013; mega6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729 [View Article][PubMed]
    [Google Scholar]
  61. Tcherepanov V., Ehlers A., Upton C. 2006; Genome Annotation Transfer Utility (GATU): rapid annotation of viral genomes using a closely related reference genome. BMC Genomics 7:1–10 [View Article][PubMed]
    [Google Scholar]
  62. Teeling E. C., Springer M. S., Madsen O., Bates P., O'brien S. J., Murphy W. J. 2005; A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307:580–584 [View Article][PubMed]
    [Google Scholar]
  63. Tuomi P. A., Murray M. J., Garner M. M., Goertz C. E., Nordhausen R. W., Burek-Huntington K. A., Getzy D. M., Nielsen O., Archer L. L. et al. 2014; Novel poxvirus infection in northern and southern sea otters (Enhydra lutris kenyoni and Enhydra lutris neiris), Alaska and California, USA. J Wildl Dis 50:607–615 [View Article][PubMed]
    [Google Scholar]
  64. Upton C., Mossman K., McFadden G. 1992; Encoding of a homolog of the IFN-gamma receptor by myxoma virus. Science 258:1369–1372 [View Article][PubMed]
    [Google Scholar]
  65. Upton C., Hogg D., Perrin D., Boone M., Harris N. L. 2000; Viral genome organizer: a system for analyzing complete viral genomes. Virus Res 70:55–64 [View Article][PubMed]
    [Google Scholar]
  66. Upton C., Slack S., Hunter A. L., Ehlers A., Roper R. L. 2003; Poxvirus orthologous clusters: toward defining the minimum essential poxvirus genome. J Virol 77:7590–7600 [View Article][PubMed]
    [Google Scholar]
  67. Wang Q., Qi J., Yuan Y., Xuan Y., Han P., Wan Y., Ji W., Li Y., Wu Y. et al. 2014; Bat origins of MERS-CoV supported by bat coronavirus HKU4 usage of human receptor CD26. Cell Host Microbe 16:328–337 [View Article][PubMed]
    [Google Scholar]
  68. Wiley S. R., Schooley K., Smolak P. J., Din W. S., Huang C. P., Nicholl J. K., Sutherland G. R., Smith T. D., Rauch C. et al. 1995; Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 3:673–682 [View Article][PubMed]
    [Google Scholar]
  69. Wise L. M., Inder M. K., Real N. C., Stuart G. S., Fleming S. B., Mercer A. A. 2012; The vascular endothelial growth factor (VEGF)-E encoded by orf virus regulates keratinocyte proliferation and migration and promotes epidermal regeneration. Cell Microbiol 14:1376–1390 [View Article][PubMed]
    [Google Scholar]
  70. Yang J., Yan R., Roy A., Xu D., Poisson J., Zhang Y., Suite T. I.-T. 2015a; The I-TASSER Suite: protein structure and function prediction. Nat Methods 12:7–8 [View Article]
    [Google Scholar]
  71. Yang X. L., Hu B., Wang B., Wang M. N., Zhang Q., Zhang W., Wu L. J., Ge X. Y., Zhang Y. Z. et al. 2015b; Isolation and characterization of a novel bat coronavirus closely related to the direct progenitor of severe acute respiratory syndrome coronavirus. J Virol 90:3253–3256 [View Article][PubMed]
    [Google Scholar]
  72. Yang X. L., Tan B., Zhang W., Wang B., Luo C. M., Wang M. N., Zhang W., Li B. et al. 2015c; Isolation and identification of bat viruses closely related to human, porcine and mink orthoreoviruses. J Gen Virol 96:3525–3531 [CrossRef]
    [Google Scholar]
  73. Zhao G., Droit L., Tesh R. B., Popov V. L., Little N. S., Upton C., Virgin H. W., Wang D. 2011; The genome of Yoka poxvirus. J Virol 85:10230–10238 [View Article][PubMed]
    [Google Scholar]
  74. Zhou P., Tachedjian M., Wynne J. W., Boyd V., Cui J., Smith I., Cowled C., Ng J. H., Mok L. et al. 2016; Contraction of the type I IFN locus and unusual constitutive expression of IFN-α in bats. Proc Natl Acad Sci U S A 113:2696–2701 [View Article][PubMed]
    [Google Scholar]
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