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
2019-12-14
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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 Virol73:533–552[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 Virol76:783–790 [CrossRef][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 Curr3:RRN1212 [CrossRef][PubMed]
    [Google Scholar]
  4. Babkin I. V., Babkina I. N.. 2015; The origin of the variola virus. Viruses7:1100–1112 [CrossRef][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. Virology441:95–106 [CrossRef][PubMed]
    [Google Scholar]
  6. Bolte A. L., Meurer J., Kaleta E. F.. 1999; Avian host spectrum of avipoxviruses. Avian Pathol28:415–432 [CrossRef][PubMed]
    [Google Scholar]
  7. Breese M. R., Liu Y.. 2013; NGSUtils: a software suite for analyzing and manipulating next-generation sequencing datasets. Bioinformatics29:494–496 [CrossRef][PubMed]
    [Google Scholar]
  8. Brodie R., Roper R. L., Upton C.. 2004a; JDotter: a Java interface to multiple dotplots generated by dotter. Bioinformatics20:279–281 [CrossRef]
    [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 Bioinform5:1–9[CrossRef]
    [Google Scholar]
  10. Buller R. M., Chakrabarti S., Moss B., Fredrickson T.. 1988; Cell proliferative response to vaccinia virus is mediated by VGF. Virology164:182–192 [CrossRef][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. Virology317:165–186 [CrossRef][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 Res14:1147–1159 [CrossRef][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 Infect4:145–151 [CrossRef]
    [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 One9:e87194 [CrossRef][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 One9:e96439 [CrossRef][PubMed]
    [Google Scholar]
  16. Dobson L., Reményi I., Tusnády G. E.. 2015; CCTOP: a Consensus Constrained TOPology prediction web server. Nucleic Acids Res43:W408–W412 [CrossRef][PubMed]
    [Google Scholar]
  17. Ehlers A., Osborne J., Slack S., Roper R. L., Upton C.. 2002; Poxvirus orthologous clusters (POCs). Bioinformatics18:1544–1545 [CrossRef][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 Dis19:1002–1004 [CrossRef][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 Biogeogr24:741–749 [CrossRef]
    [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 Pathog6:e1000984 [CrossRef][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. Nature503:535–538 [CrossRef][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 Sin31:31–40 [CrossRef][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 Virol89:9348–9367 [CrossRef][PubMed]
    [Google Scholar]
  24. Gonzalvez F., Ashkenazi A.. 2010; New insights into apoptosis signaling by Apo2L/TRAIL. Oncogene29:4752–4765 [CrossRef][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 Res54:165–187 [CrossRef][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 Virol84:485–496 [CrossRef][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 Virol81:1927–1932 [CrossRef][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 Res205:1–6 [CrossRef][PubMed]
    [Google Scholar]
  29. Herbert M. H., Squire C. J., Mercer A. A.. 2015; Poxviral ankyrin proteins. Viruses7:709–738 [CrossRef][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 Exp1:2 [CrossRef][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 Cell4:563–571[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. Biochemistry39:633–640 [CrossRef][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 Biol537:39–64 [CrossRef][PubMed]
    [Google Scholar]
  35. Kim D. E., Chivian D., Baker D.. 2004; Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res32:W526–531 [CrossRef][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 Virol90:1967–1977 [CrossRef][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. Nature438:575–576 [CrossRef][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 Dis9:723–728 [CrossRef]
    [Google Scholar]
  39. Li H., Durbin R.. 2009; Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics25:1754–1760 [CrossRef][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. Bioinformatics25:2078–2079 [CrossRef][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 Immunol28:973–982 [CrossRef][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 Res33:206–210 [CrossRef][PubMed]
    [Google Scholar]
  43. McFadden G.. 2005; Poxvirus tropism. Nat Rev Microbiol3:201–213 [CrossRef][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 Virol76:11216–11225 [CrossRef][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 Dis19:1819–1823 [CrossRef][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 Genes31:127–133 [CrossRef][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 Bioinform14:193–202 [CrossRef][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 Biol6:1048–1053 [CrossRef][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 Dis21:1840–1843[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. Viruses7:4878–4898 [CrossRef][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 Pathog9:e1003224 [CrossRef][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 Virol95:245–262 [CrossRef][PubMed]
    [Google Scholar]
  53. Perdiguero B., Esteban M.. 2009; The interferon system and vaccinia virus evasion mechanisms. J Interferon Cytokine Res29:581–598 [CrossRef][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 Chem25:1605–1612 [CrossRef][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. Virology397:176–186 [CrossRef][PubMed]
    [Google Scholar]
  56. Rodhain E.. 2015; Bats and Viruses: complex relationships. Bull Soc Pathol Exot108:272–289 [CrossRef][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 Genes51:136–139 [CrossRef][PubMed]
    [Google Scholar]
  58. Smith G. L., Vanderplasschen A., Law M.. 2002; The formation and function of extracellular enveloped vaccinia virus. J Gen Virol83:2915–2931 [CrossRef][PubMed]
    [Google Scholar]
  59. Springer M. S.. 2013; Phylogenetics: bats united, microbats divided. Curr Biol23:R999–R1001 [CrossRef][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 Evol30:2725–2729 [CrossRef][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 Genomics7:1–10 [CrossRef][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. Science307:580–584 [CrossRef][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 Dis50:607–615 [CrossRef][PubMed]
    [Google Scholar]
  64. Upton C., Mossman K., McFadden G.. 1992; Encoding of a homolog of the IFN-gamma receptor by myxoma virus. Science258:1369–1372 [CrossRef][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 Res70:55–64 [CrossRef][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 Virol77:7590–7600 [CrossRef][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 Microbe16:328–337 [CrossRef][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. Immunity3:673–682 [CrossRef][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 Microbiol14:1376–1390 [CrossRef][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 Methods12:7–8 [CrossRef]
    [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 Virol90:3253–3256 [CrossRef][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 Virol96:3525–3531[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 Virol85:10230–10238 [CrossRef][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 A113:2696–2701 [CrossRef][PubMed]
    [Google Scholar]
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