Genome Analysis of Dasineura jujubifolia Toursvirus 2, A Novel Ascovirus

Abstract

So far, ascoviruses have only been identified from Lepidoptera host insects and their transmission vectors—endoparasitic wasps. Here, we reported the first finding of a complete novel ascovirus genome from a Diptera insect, Dasineura jujubifolia. Initially, sequence fragments with homology to ascoviruses were incidentally identified during metagenomic sequencing of the mitochondria of D. jujubifolia (Cecidomyiidae, Diptera) which is a major pest on Ziziphus jujuba. Then a full circular viral genome was assembled from the metagenomic data, which has an A+T percentage of 74% and contains 142,600 bp with 141 open reading frames (ORFs). Among the 141 ORFs, 37 were conserved in all sequenced ascoviruses (core genes) including proteins predicted to participate in DNA replication, gene transcription, protein modification, virus assembly, lipid metabolism and apoptosis. Multi-gene families including those encode for baculovirus repeated open reading frames (BROs), myristylated membrane proteins, RING/U-box E3 ubiquitin ligases, and ATP-binding cassette (ABC) transporters were found in the virus genome. Phylogenetic analysis showed that the newly identified virus belongs to genus Toursvirus of Ascoviridae, and is therefore named as Dasineura jujubifolia toursvirus 2 (DjTV-2a). The virus becomes the second reported species of the genus after Diadromus pulchellus toursvirus 1 (DpTV-1a). The genome arrangement of DjTV-2a is quite different from that of DpTV-1a, suggesting these two viruses separated in an early time of evolution. The results suggest that the ascoviruses may infect a much broader range of hosts than our previous knowledge, and shed lights on the evolution of ascoviruses and particularly on that of the toursviruses.

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References

  1. Arai E, Ishii K, Ishii H, Sagawa S, Makiyama N, Mizutani T, Omatsu T, Katayama Y, Kunimi Y, Inoue MN, Nakai M (2018) An ascovirus isolated from Spodoptera litura (Noctuidae: Lepidoptera) transmitted by the generalist endoparasitoid Meteorus pulchricornis (Braconidae: Hymenoptera). J Gen Virol 99:574–584

    CAS  Article  Google Scholar 

  2. Asgari S, Davis J, Wood D, Wilson P, McGrath A (2007) Sequence and organization of the Heliothis virescens ascovirus genome. J Gen Virol 88:1120–1132

    CAS  Article  Google Scholar 

  3. Asgari S, Bideshi DK, Bigot Y, Federici BA, Cheng XW, Consortium IR (2017) ICTV Virus taxonomy profile: ascoviridae. J Gen Virol 98:4–5

    CAS  Article  Google Scholar 

  4. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    CAS  Article  Google Scholar 

  5. Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580

    CAS  Article  Google Scholar 

  6. Bideshi DK, Renault S, Stasiak K, Federici BA, Bigot Y (2003) Phylogenetic analysis and possible function of bro-like genes, a multigene family widespread among large double-stranded DNA viruses of invertebrates and bacteria. J Gen Virol 84:2531–2544

    CAS  Article  Google Scholar 

  7. Bideshi DK, Demattei M-V, Rouleux-Bonnin F, Stasiak K, Tan Y, Bigot S, Bigot Y, Federici BA (2006) Genomic sequence of Spodoptera frugiperda Ascovirus 1a, an enveloped, double-stranded DNA insect virus that manipulates apoptosis for viral reproduction. J Virol 80:11791–11805

    CAS  Article  Google Scholar 

  8. Bideshi DK, Spears T, Zaghloul HAH, Tan Y, Bigot Y, Federici BA (2018) Ascovirus P64 Homologs: a novel family of large cationic proteins that condense viral genomic DNA for encapsidation. Biology (Basel) 7:44

    CAS  Google Scholar 

  9. Bigot Y, Rabouille A, Doury G, Sizaret PY, Delbost F, Hamelin MH, Periquet G (1997a) Biological and molecular features of the relationships between Diadromus pulchellus ascovirus, a parasitoid hymenopteran wasp (Diadromus pulchellus) and its lepidopteran host, Acrolepiopsis assectella. J Gen Virol 78:1149–1163

    CAS  Article  Google Scholar 

  10. Bigot Y, Rabouille A, Sizaret PY, Hamelin MH, Periquet G (1997b) Particle and genomic characteristics of a new member of the Ascoviridae: Diadromus pulchellus ascovirus. J Gen Virol 78(Pt 5):1139–1147

    CAS  Article  Google Scholar 

  11. Bigot Y, Renault S, Nicolas J, Moundras C, Demattei M-V, Samain S, Bideshi DK, Federici BA (2009) Symbiotic virus at the evolutionary intersection of three types of large DNA viruses; iridoviruses, ascoviruses, and ichnoviruses. PLoS ONE 4:e6397

    Article  Google Scholar 

  12. Chen ZS, Hou DH, Cheng XW, Wang X, Huang GH (2018) Genomic analysis of a novel isolate Heliothis virescens ascovirus 3i (HvAV-3i) and identification of ascoviral repeat ORFs (aros). Arch Virol 163:2849–2853

    CAS  Article  Google Scholar 

  13. Chen ZS, Cheng XW, Wang X, Hou DH, Huang GH (2019) Proteomic analysis of the Heliothis virescens ascovirus 3i (HvAV-3i) virion. J Gen Virol 100:301–307

    CAS  Article  Google Scholar 

  14. Cullinane M, Baysse C, Morrissey JP, O’Gara F (2005) Identification of two lysophosphatidic acid acyltransferase genes with overlapping function in Pseudomonas fluorescens. Microbiology 151:3071–3080

    CAS  Article  Google Scholar 

  15. Huang GH, Wang YS, Wang X, Garretson TA, Dai LY, Zhang CX, Cheng XW (2012) Genomic sequence of Heliothis virescens ascovirus 3 g isolated from Spodoptera exigua. J Virol 86:12467–12468

    CAS  Article  Google Scholar 

  16. Huang GH, Hou DH, Wang M, Cheng XW, Hu Z (2017) Genome analysis of Heliothis virescens ascovirus 3 h isolated from China. Virol Sin 32:147–154

    CAS  Article  Google Scholar 

  17. Jakob NJ, Müller K, Bahr U, Darai G (2001) Analysis of the first complete DNA sequence of an invertebrate iridovirus: coding strategy of the genome of Chilo iridescent virus. Virology 286:182–196

    CAS  Article  Google Scholar 

  18. Jakobsson A, Westerberg R, Jacobsson A (2006) Fatty acid elongases in mammals: their regulation and roles in metabolism. Prog Lipid Res 45:237–249

    CAS  Article  Google Scholar 

  19. Jiao KL, Han PJ, Yang ML, Xiong RC, Wang YH, Bu WJ (2017) A new species of gall midge (Diptera: Cecidomyiidae) attacking jujube, Ziziphus jujuba in China. Zootaxa 4247:487–493

    Article  Google Scholar 

  20. Kang WK, Imai N, Suzuki M, Iwanaga M, Matsumoto S, Zemskov EA (2003) Interaction of Bombyx mori nucleopolyhedrovirus BRO-A and host cell protein laminin. Arch Virol 148:99–113

    CAS  Article  Google Scholar 

  21. Li L, Shataer A, Pan C, Cao Q (2010) Study on Growth and Decline Law and Control of Dasineura datifolia Jiang in Aksy. J Xinjiang Agric Univ 33:36–39 (in Chinese)

    Google Scholar 

  22. Liu YY, Xian WF, Xue J, Wei YL, Cheng XW, Wang X (2018) Complete genome sequence of a renamed isolate, Trichoplusia ni sscovirus 6b, from the United States. Genome Announc 6:e00148–e00218

    PubMed  PubMed Central  Google Scholar 

  23. Long CM, Rohrmann GF, Merrill GF (2009) The conserved baculovirus protein p33 (Ac92) is a flavin adenine dinucleotide-linked sulfhydryl oxidase. Virology 388:231–235

    CAS  Article  Google Scholar 

  24. Parsons JD (1995) Miropeats: graphical DNA sequence comparisons. Comput Appl Biosci 11:615–619

    CAS  PubMed  Google Scholar 

  25. Piégu B, Asgari S, Bideshi D, Federici BA, Bigot Y (2015) Evolutionary relationships of iridoviruses and divergence of ascoviruses from invertebrate iridoviruses in the superfamily Megavirales. Mol Phylogenetics Evol 84:44–52

    Article  Google Scholar 

  26. Ravanello MP, Hruby DE (1994) Conditional lethal expression of the vaccinia virus L1R myristylated protein reveals a role in virion assembly. J Virol 68:6401–6410

    CAS  Article  Google Scholar 

  27. Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863–864

    CAS  Article  Google Scholar 

  28. Shrestha A, Bao K, Chen Y-R, Chen W, Wang P, Fei Z, Blissard GW (2018) Global analysis of baculovirus Autographa californica multiple nucleopolyhedrovirus gene expression in the midgut of the Lepidopteran host Trichoplusia ni. J Virol 92:e01277–e01318

    CAS  Article  Google Scholar 

  29. Stasiak K, Renault S, Federici BA, Bigot Y (2005) Characteristics of pathogenic and mutualistic relationships of ascoviruses in field populations of parasitoid wasps. J Insect Physiol 51:103–115

    CAS  Article  Google Scholar 

  30. 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

    CAS  Article  Google Scholar 

  31. Wang L, Xue J, Seaborn CP, Arif BM, Cheng X-W (2006) Sequence and organization of the Trichoplusia ni ascovirus 2c (Ascoviridae) genome. Virology 354:167–177

    CAS  Article  Google Scholar 

  32. Wei YL, Hu J, Li SJ, Chen ZS, Cheng XW, Huang GH (2014) Genome sequence and organization analysis of Heliothis virescens ascovirus 3f isolated from a Helicoverpa zea larva. J Invertebr Pathol 122:40–43

    CAS  Article  Google Scholar 

  33. White CL, Senkevich TG, Moss B (2002) Vaccinia virus G4L glutaredoxin is an essential intermediate of a cytoplasmic disulfide bond pathway required for virion assembly. J Virol 76:467–472

    CAS  Article  Google Scholar 

  34. Wilson SK, Knoll LJ (2018) Patatin-like phospholipases in microbial infections with emerging roles in fatty acid metabolism and immune regulation by Apicomplexa. Mol Microbiol 107:34–46

    CAS  Article  Google Scholar 

  35. Wong CK, Young VL, Kleffmann T, Ward VK (2011) Genomic and proteomic analysis of invertebrate iridovirus type 9. J Virol 85:7900–7911

    CAS  Article  Google Scholar 

  36. Zaghloul HAH, Hice R, Arensburger P, Federici BA (2017) Transcriptome analysis of the Spodoptera frugiperda ascovirus in vivo provides insights into how its apoptosis inhibitors and caspase promote increased synthesis of viral vesicles and virion progeny. J Virol 91:e00874–e00917

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the International Science and Technology Cooperation Program of Xinjiang Construction Corps (Grant No. 2017BC004) and the National Natural Science Foundation of China (Grant No. 31900154).

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HX and MY conceived and designed the experiments. HX performed the experiments. JW, ZH, GHH analysis the data. JW, FD, ZH, GHH, and MY wrote the manuscript. All authors read and approved the final manuscript.

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Correspondence to Minglu Yang or Zhihong Hu.

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Wang, J., Yang, M., Xiao, H. et al. Genome Analysis of Dasineura jujubifolia Toursvirus 2, A Novel Ascovirus. Virol. Sin. 35, 134–142 (2020). https://doi.org/10.1007/s12250-019-00177-2

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Keywords

  • Dasineura jujubifolia toursvirus 2 (DjTV-2a)
  • Ascovirus
  • Toursvirus