1887

Abstract

Sequencing of the full coding region of both genomic segments of seven betanodavirus strains isolated from different farmed species in Spain and Portugal revealed that six were reassortants, exhibiting a red-spotted grouper nervous necrosis virus (RGNNV)-type RNA1 and a striped jack nervous necrosis virus (SJNNV)-type RNA2. Analysis of sequences of reassortant strains at both the genomic and protein levels revealed the existence of differences compared with type strains of both genotypes. These differences were greater in the polymerase sequence, which is remarkable because viral structural proteins generally diverge more rapidly than non-structural proteins. Changes in two amino acids observed in the SJNNV capsid protein might be involved in the colonization of new host species by these reassortant strains. In addition, a more extensive phylogenetic analysis, including partial sequences of both RNA segments of 16 other Iberian nodaviruses, confirmed the existence of reassortment between RGNNV and SJNNV.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.013912-0
2009-12-01
2019-10-16
Loading full text...

Full text loading...

/deliver/fulltext/jgv/90/12/2940.html?itemId=/content/journal/jgv/10.1099/vir.0.013912-0&mimeType=html&fmt=ahah

References

  1. Aspehaug, V., Devold, M. & Nylund, A. ( 1999; ). The phylogenetic relationship of nervous necrosis virus from halibut (Hippoglossus hippoglossus). Bull Eur Assoc Fish Pathol 19, 196–202.
    [Google Scholar]
  2. Baranowski, E., Ruiz-Jarabo, C. M. & Domingo, E. ( 2001; ). Evolution of cell recognition by viruses. Science 292, 1102–1105.[CrossRef]
    [Google Scholar]
  3. Bryson, K., McGuffin, L. J., Marsden, R. L., Ward, J. J., Sodhi, J. S. & Jones, D. T. ( 2005; ). Protein structure prediction servers at University College London. Nucleic Acids Res 33, W36–W38.[CrossRef]
    [Google Scholar]
  4. Carlsson, B., Lindberg, A. M., Rodriguez-Díaz, J., Hedlund, K.-O., Persson, B. & Svensson, L. ( 2009; ). Quasispecies dynamics and molecular evolution of human norovirus capsid P region during chronic infection. J Gen Virol 90, 432–441.[CrossRef]
    [Google Scholar]
  5. Chi, S. C., Shieh, J. R. & Lin, S. J. ( 2003; ). Genetic and antigenic analysis of betanodaviruses isolated from aquatic organisms in Taiwan. Dis Aquat Organ 55, 221–228.[CrossRef]
    [Google Scholar]
  6. Combet, C., Blanchet, C., Geourjon, C. & Deléage, G. ( 2000; ). [email protected]: network protein sequence analysis. Trends Biochem Sci 25, 147–150.[CrossRef]
    [Google Scholar]
  7. Cutrín, J. M., Thiéry, R., Leao, P., Olveira, J. G., Barja, J. L. & Bandín, I. ( 2007; ). Emergence of pathogenic betanodaviruses belonging to SJNNV genogroup in farmed fish species from the Iberian Peninsula. J Fish Dis 30, 225–232.[CrossRef]
    [Google Scholar]
  8. Dalla Valle, L., Negrisolo, E., Patarnello, P., Zanella, L., Maltese, C., Bovo, G. & Colombo, L. ( 2001; ). Sequence comparison and phylogenetic analysis of fish nodaviruses based on the coat protein gene. Arch Virol 146, 1125–1137.[CrossRef]
    [Google Scholar]
  9. Delsert, C., Morin, N. & Comps, M. ( 1997; ). A fish encephalitis virus that differs from other nodaviruses by its capsid protein processing. Arch Virol 142, 2359–2371.[CrossRef]
    [Google Scholar]
  10. Fenner, B. J., Thiagarajan, R., Kheng Chua, H. & Kwang, J. ( 2006a; ). Betanodavirus B2 is an RNA interference antagonist that facilitates intracellular viral RNA accumulation. J Virol 80, 85–94.[CrossRef]
    [Google Scholar]
  11. Fenner, B. J., Goh, W. & Kwang, J. ( 2006b; ). Sequestration and protection of double-stranded RMA by the betanodavirus B2 protein. J Virol 80, 6822–6833.[CrossRef]
    [Google Scholar]
  12. Frerichs, G. N., Rodger, H. D. & Peric, Z. ( 1996; ). Cell culture isolation of piscine neuropathy nodavirus from juvenile sea bass, Dicentrarchus labrax. J Gen Virol 77, 2067–2071.[CrossRef]
    [Google Scholar]
  13. Gagné, N., Johnson, S. C., Cook-Versloot, M., MacKinnon, A. M. & Olivier, G. ( 2004; ). Molecular detection and characterization of nodavirus in several marine fish species from the northeastern Atlantic. Dis Aquat Organ 62, 181–189.[CrossRef]
    [Google Scholar]
  14. Grotmol, S., Nerland, A. H., Biering, E., Totland, G. K. & Nishizawa, T. ( 2000; ). Characterization of the capsid protein gene from a nodavirus strain affecting the Atlantic halibut Hippoglossus hippoglossus and design of an optimal reverse-transcriptase polymerase chain reaction (RT-PCR) detection assay. Dis Aquat Organ 39, 79–88.[CrossRef]
    [Google Scholar]
  15. Ito, Y., Okinaka, Y., Mori, K.-I., Sugaya, T., Nishioka, T., Oka, M. & Nakai, T. ( 2008; ). Variable region of betanodavirus RNA2 is sufficient to determine host specificity. Dis Aquat Organ 79, 199–205.[CrossRef]
    [Google Scholar]
  16. Iwamoto, T., Mise, K., Mori, K., Arimoto, M., Nakai, T. & Okuno, T. ( 2001; ). Establishment of an infectious RNA transcription system for Striped jack nervous necrosis virus, the type species of the betanodaviruses. J Gen Virol 82, 2653–2662.
    [Google Scholar]
  17. Iwamoto, T., Okinaka, Y., Mise, K., Mori, K.-I., Arimoto, M., Okuno, T. & Nakai, T. ( 2004; ). Identification of host-specificity determinants in betanodaviruses by using reassortants between striped jack nervous necrosis virus and sevenband grouper nervous necrosis virus. J Virol 78, 1256–1262.[CrossRef]
    [Google Scholar]
  18. Iwamoto, T., Mise, K., Taked, A., Okinaka, Y., Mori, F., Arimoto, M., Okuno, T. & Nakai, T. ( 2005; ). Characterization of Striped jack nervous necrosis virus subgenomic RNA3 and biological activities of its encoded protein B2. J Gen Virol 86, 2807–2816.[CrossRef]
    [Google Scholar]
  19. Johansen, R., Sommerset, I., Tørud, B., Korsne, K., Hjortaas, M. J., Nilsen, F., Nerland, A. H. & Dannevig, B. H. ( 2004; ). Characterization of nodavirus and viral encephalopathy and retinopathy in farmed turbot, Scophthalmus maximus (L.). J Fish Dis 27, 591–601.[CrossRef]
    [Google Scholar]
  20. Johnson, S. C., Sperker, S. A., Leggiadro, C. T., Groman, D. B., Griffiths, S. G., Ritchie, R. J., Cook, M. D. & Cusak, R. R. ( 2002; ). Identification and characterization of a piscine neuropathy and nodavirus from juvenile Atlantic cod from the Atlantic coast of North America. J Aquat Anim Health 14, 124–133.[CrossRef]
    [Google Scholar]
  21. Joklik, W. K. & Roner, M. R. ( 1995; ). What reassorts when reovirus genome segments reassort? J Biol Chem 270, 4181–4184.[CrossRef]
    [Google Scholar]
  22. Jones, D. T. ( 1999; ). Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292, 195–202.[CrossRef]
    [Google Scholar]
  23. Lee, K. W., Chi, S. C. & Cheng, T. M. ( 2002; ). Interference of the life cycle of fish nodavirus with fish retrovirus. J Gen Virol 83, 2469–2474.
    [Google Scholar]
  24. Lichtarge, O., Bourne, H. R. & Cohen, F. E. ( 1996; ). An evolutionary trace method defines binding surfaces common to protein families. J Mol Biol 257, 342–358.[CrossRef]
    [Google Scholar]
  25. Martin, D. P., Williamson, C. & Posada, D. ( 2005; ). rdp2: recombination detection and analysis from sequence alignments. Bioinformatics 21, 260–262.[CrossRef]
    [Google Scholar]
  26. Milne, I., Lindner, D., Bayer, M., Husmeier, D., McGuire, G., Marshall, D. F. & Wright, F. ( 2009; ). TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics 25, 126–127.[CrossRef]
    [Google Scholar]
  27. Munday, B., Kwang, J. & Moody, N. ( 2002; ). Betanodavirus infections of teleost fish: a review. J Fish Dis 25, 127–142.[CrossRef]
    [Google Scholar]
  28. Nagai, T. & Nishizawa, T. ( 1999; ). Sequence of the non-structural protein gene encoded by RNA1 of striped jack nervous necrosis virus. J Gen Virol 80, 3019–3022.
    [Google Scholar]
  29. Névarez, L., Cozien, J. & Thiéry, R. ( 2005; ). Analyse phylogénétique comparée des gènes de la protéine de capside et de l'ARN polymérase des nodavirus de poissons. A52. VIIèmes Journées francophones de Virologie, 28–29 Avril 2005 Paris. Virologie 9, 115–166 (in French).
    [Google Scholar]
  30. Nishizawa, T., Mori, K., Furuhashi, M., Nakai, T., Furusawa, I. & Murog, K. ( 1995; ). Comparison of the coat protein genes of five fish nodaviruses, the causative agents of nervous necrosis in marine fish. J Gen Virol 76, 1563–1569.[CrossRef]
    [Google Scholar]
  31. Nishizawa, T., Furuhashi, M., Nagai, T., Nakai, T. & Muroga, K. ( 1997; ). Genomic classification of fish nodaviruses by molecular phylogenetic analysis of the coat protein gene. Appl Environ Microbiol 63, 1633–1636.
    [Google Scholar]
  32. Nylund, A., Karlsbakk, E. E., Nylund, E. S., Isaksen, E. T. E., Karlsen, M., Korsnes, E. K., Handeland, E. S., Martinsen, E. R., Mork Pedersen, E. T. & Ottem, E. K. F. ( 2008; ). New clade of betanodavirus detected in wild and farmed cod (Gadus morhua) in Norway. Arch Virol 153, 541–547.[CrossRef]
    [Google Scholar]
  33. Okinaka, Y. & Nakai, T. ( 2008; ). Comparison of the complete genome of four betanodavirus genotypes. Dis Aquat Organ 80, 113–121.[CrossRef]
    [Google Scholar]
  34. Olveira, J. G., Soares, F., Engrola, S., Dopazo, C. P. & Bandín, I. ( 2008; ). Antemortem versus postmortem methods for detection of betanodavirus in Senegalese sole (Solea senegalensis). J Vet Diagn Invest 20, 215–219.[CrossRef]
    [Google Scholar]
  35. Roner, M. R., Basset, K. & Roehr, J. ( 2004; ). Identification of the 5′ sequences required for incorporation of an engineered ssRNA into the Reovirus genome. Virology 329, 348–360.[CrossRef]
    [Google Scholar]
  36. Ronquist, F. & Huelsenbeck, J. P. ( 2003; ). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.[CrossRef]
    [Google Scholar]
  37. Rozas, J., Sánchez-DelBarrio, J. C., Messeguer, X. & Rozas, J. R. ( 2003; ). DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497.[CrossRef]
    [Google Scholar]
  38. Schneemann, A., Ball, L. A., Delsert, C., Johnson, J. E. & Nishizawa, T. ( 2005; ). Family Nodaviridae. In Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses, pp. 865–872. Edited by C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger & L. A. Ball. San Diego, CA: Elsevier Academic Press.
  39. Skliris, G. P., Krondiris, J. V., Sideris, D. C., Shinn, A. P., Starkey, W. G. & Richards, R. H. ( 2001; ). Phylogenetic and antigenic characterization of new fish nodavirus isolates from Europe and Asia. Virus Res 75, 59–67.[CrossRef]
    [Google Scholar]
  40. Sommerset, I. & Nerland, A. H. ( 2004; ). Complete sequence of RNA1 and subgenomic RNA3 of Atlantic halibut nodavirus (AHNV). Dis Aquat Organ 58, 117–125.[CrossRef]
    [Google Scholar]
  41. Starkey, W. G., Ireland, J. H., Muir, K. F., Shinn, A. P., Richards, R. H. & Ferguson, H. W. ( 2000; ). Isolation of nodavirus from Scottish farmed halibut, Hippoglossus hippoglossus (L). J Fish Dis 23, 418–422.[CrossRef]
    [Google Scholar]
  42. Tan, C., Huang, B., Chang, S., Ngoh, G., Munday, B., Che, S. & Kwang, J. ( 2001; ). Determination of the complete nucleotide sequences of RNA1 and RNA2 from greasy grouper (Epinephelus tauvina) nervous necrosis virus, Singapore strain. J Gen Virol 82, 647–653.
    [Google Scholar]
  43. Tang, L., Lin, C. S., Krishna, N. K., Yeager, M. & Scheemann, J. E. ( 2002; ). Virus-like particles of a fish nodavirus display a capsid subunit domain organization different from that of insect nodaviruses. J Virol 76, 6370–6375.[CrossRef]
    [Google Scholar]
  44. Thiéry, R., Cozien, J., de Boisséson, C., Kerbat-Boscher, S. & Névarez, L. ( 2004; ). Genomic classification of new betanodaviruses isolates by phylogenetic analysis of the coat protein gene suggests a low host-fish species specificity. J Gen Virol 85, 3079–3087.[CrossRef]
    [Google Scholar]
  45. Toffolo, V., Negrisolo, E., Maltese, C., Bovo, G., Belvedere, P., Colombo, L. & Dalla Valle, L. ( 2007; ). Phylogeny of betanodaviruses and molecular evolution of their RNA polymerase and coat proteins. Mol Phylogenet Evol 43, 298–308.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.013912-0
Loading
/content/journal/jgv/10.1099/vir.0.013912-0
Loading

Data & Media loading...

Supplements

vol. , part 12, pp. 2940–2951

Primers used for sequencing [ PDF] (55 KB)



PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error