1887

Abstract

A novel fish reovirus, Hubei grass carp disease reovirus (HGDRV; formerly grass carp reovirus strain 104, GCRV104), was isolated from diseased grass carp in China in 2009 and the full genome sequence was determined. This reovirus was propagated in a grass carp kidney cell line with a typical cytopathic effect. The total size of the genome was 23 706 bp with a 51 mol% G+C content, and the 11 dsRNA segments encoded 12 proteins (two proteins encoded by segment 11). A nucleotide sequence similarity search using found no significant matches except for segment 2, which partially matched that of the RNA-dependent RNA polymerase (RdRp) from several viruses in the genera and of the family . At the amino acid level, seven segments (Seg-1 to Seg-6, and Seg-8) matched with species in the genera (15–46 % identities) and (12–44 % identities), while for four segments (Seg-7, Seg-9, Seg-10 and Seg-11) no similarities in these genera were found. Conserved terminal sequences, 5′-GAAUU----UCAUC-3′, were found in each HGDRV segment at the 5′ and 3′ ends, and the 5′-terminal nucleotides were different from any known species in the genus . Phylogenetic analysis based on RdRp amino acid sequences from members of the family showed that HGDRV clustered with aquareoviruses prior to joining a branch common with orthoreoviruses. Based on these observations, we propose that HGDRV is a new species in the genus that is distantly related to any known species within this genus.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.054767-0
2013-10-01
2019-10-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/10/2266.html?itemId=/content/journal/jgv/10.1099/vir.0.054767-0&mimeType=html&fmt=ahah

References

  1. Anzola J. V., Xu Z. K., Asamizu T., Nuss D. L.. ( 1987;). Segment-specific inverted repeats found adjacent to conserved terminal sequences in wound tumor virus genome and defective interfering RNAs. . Proc Natl Acad Sci U S A 84:, 8301–8305. [CrossRef][PubMed]
    [Google Scholar]
  2. Attoui H., Billoir F., Biagini P., de Micco P., de Lamballerie X.. ( 2000a;). Complete sequence determination and genetic analysis of Banna virus and Kadipiro virus: proposal for assignment to a new genus (Seadornavirus) within the family Reoviridae. . J Gen Virol 81:, 1507–1515.[PubMed]
    [Google Scholar]
  3. Attoui H., Billoir F., Biagini P., Cantaloube J. F., de Chesse R., de Micco P., de Lamballerie X.. ( 2000b;). Sequence determination and analysis of the full-length genome of colorado tick fever virus, the type species of genus Coltivirus (Family Reoviridae). . Biochem Biophys Res Commun 273:, 1121–1125. [CrossRef][PubMed]
    [Google Scholar]
  4. Attoui H., Fang Q., Mohd Jaafar F., Cantaloube J. F., Biagini P., de Micco P., de Lamballerie X.. ( 2002a;). Common evolutionary origin of aquareoviruses and orthoreoviruses revealed by genome characterization of Golden shiner reovirus, Grass carp reovirus, Striped bass reovirus and golden ide reovirus (genus Aquareovirus, family Reoviridae). . J Gen Virol 83:, 1941–1951.[PubMed]
    [Google Scholar]
  5. Attoui H., Mohd Jaafar F., Biagini P., Cantaloube J. F., de Micco P., Murphy F. A., de Lamballerie X.. ( 2002b;). Genus Coltivirus (family Reoviridae): genomic and morphologic characterization of Old World and New World viruses. . Arch Virol 147:, 533–561. [CrossRef][PubMed]
    [Google Scholar]
  6. Attoui H., Mohd Jaafar F., Belhouchet M., Biagini P., Cantaloube J. F., de Micco P., de Lamballerie X.. ( 2005;). Expansion of family Reoviridae to include nine-segmented dsRNA viruses: isolation and characterization of a new virus designated Aedes pseudoscutellaris reovirus assigned to a proposed genus (Dinovernavirus).. Virology 343:, 212–223. [CrossRef][PubMed]
    [Google Scholar]
  7. Attoui H., Jaafar F. M., Belhouchet M., de Micco P., de Lamballerie X., Brussaard C. P.. ( 2006a;). Micromonas pusilla reovirus: a new member of the family Reoviridae assigned to a novel proposed genus (Mimoreovirus). . J Gen Virol 87:, 1375–1383. [CrossRef][PubMed]
    [Google Scholar]
  8. Attoui H., Mohd Jaafar F., Belhouchet M., Tao S., Chen B., Liang G., Tesh R. B., de Micco P., de Lamballerie X.. ( 2006b;). Liao ning virus, a new Chinese seadornavirus that replicates in transformed and embryonic mammalian cells. . J Gen Virol 87:, 199–208. [CrossRef][PubMed]
    [Google Scholar]
  9. Attoui H., Mertens P. P. C., Becnel J., Belaganahalli S., Bergoin M., Brussaard C. P., Chappell J. D., Ciarlet M., del Vas M.. & other authors ( 2012;). Family Reoviridae. . In Virus Taxonomy: classification and nomenclature of viruses. Ninth Report of the International Committee on Taxonomy of Viruses, pp. 541–637. Edited by King A. M. Q., Adams M. J., Carstens E. B., Lefkowitz E. J... London:: Academic Press;.
    [Google Scholar]
  10. Brentano L., Noah D. L., Brown E. G., Sherry B.. ( 1998;). The reovirus protein μ2, encoded by the M1 gene, is an RNA-binding protein. . J Virol 72:, 8354–8357.[PubMed]
    [Google Scholar]
  11. Broering T. J., Kim J., Miller C. L., Piggott C. D. S., Dinoso J. B., Nibert M. L., Parker J. S. L.. ( 2004;). Reovirus nonstructural protein μ NS recruits viral core surface proteins and entering core particles to factory-like inclusions. . J Virol 78:, 1882–1892. [CrossRef][PubMed]
    [Google Scholar]
  12. Chen D., Patton J. T.. ( 1998;). Rotavirus RNA replication requires a single-stranded 3′ end for efficient minus-strand synthesis. . J Virol 72:, 7387–7396.[PubMed]
    [Google Scholar]
  13. Chen J. G., Xiong J., Yang J. F., Mao Z. J., Chen X. X.. ( 2011;). Nucleotide sequences of four RNA segments of a reovirus isolated from the mud crab Scylla serrata provide evidence that this virus belongs to a new genus in the family Reoviridae. . Arch Virol 156:, 523–528. [CrossRef][PubMed]
    [Google Scholar]
  14. Cheng L. P., Fang Q., Shah S., Atanasov I. C., Zhou Z. H.. ( 2008;). Subnanometer-resolution structures of the grass carp reovirus core and virion. . J Mol Biol 382:, 213–222. [CrossRef][PubMed]
    [Google Scholar]
  15. Cheng L. P., Zhu J., Hui W. H., Zhang X. K., Honig B., Fang Q., Zhou Z. H.. ( 2010;). Backbone model of an aquareovirus virion by cryo-electron microscopy and bioinformatics. . J Mol Biol 397:, 852–863. [CrossRef][PubMed]
    [Google Scholar]
  16. Dermody T. S., Schiff L. A., Nibert M. L., Coombs K. M., Fields B. N.. ( 1991;). The S2 gene nucleotide sequences of prototype strains of the three reovirus serotypes: characterization of reovirus core protein σ2. . J Virol 65:, 5721–5731.[PubMed]
    [Google Scholar]
  17. Fan C., Shao L., Fang Q.. ( 2010;). Characterization of the nonstructural protein NS80 of grass carp reovirus. . Arch Virol 155:, 1755–1763. [CrossRef][PubMed]
    [Google Scholar]
  18. Fang Q., Ke L. H., Cai Y. Q.. ( 1989;). Growth characterization and high titre culture of GCHV. . Virol Sin 3:, 315–319.
    [Google Scholar]
  19. Fang Q., Attoui H., Cantaloube J. F., Biagini P., Zhu Z. Y., de Micco P., de Lamballerie X.. ( 2000;). Sequence of genome segments 1, 2, and 3 of the grass carp reovirus (genus Aquareovirus, family Reoviridae). . Biochem Biophys Res Commun 274:, 762–766. [CrossRef][PubMed]
    [Google Scholar]
  20. Fang Q., Seng E. K., Ding Q. Q., Zhang L. L.. ( 2008;). Characterization of infectious particles of grass carp reovirus by treatment with proteases. . Arch Virol 153:, 675–682. [CrossRef][PubMed]
    [Google Scholar]
  21. Gomatos P. J., Prakash O., Stamatos N. M.. ( 1981;). Small reovirus particle composed solely of sigma NS with specificity for binding different nucleic acids. . J Virol 39:, 115–124.[PubMed]
    [Google Scholar]
  22. Hsiao J., Martínez-Costas J., Benavente J., Vakharia V. N.. ( 2002;). Cloning, expression, and characterization of avian reovirus guanylyltransferase. . Virology 296:, 288–299. [CrossRef][PubMed]
    [Google Scholar]
  23. Jayaram H., Estes M. K., Prasad B. V. V.. ( 2004;). Emerging themes in rotavirus cell entry, genome organization, transcription and replication. . Virus Res 101:, 67–81. [CrossRef][PubMed]
    [Google Scholar]
  24. Ke F., He L. B., Pei C., Zhang Q. Y.. ( 2011;). Turbot reovirus (SMReV) genome encoding a FAST protein with a non-AUG start site. . BMC Genomics 12:, 323–335. [CrossRef][PubMed]
    [Google Scholar]
  25. Kim J., Zhang X., Centonze V. E., Bowman V. D., Noble S., Baker T. S., Nibert M. L.. ( 2002;). The hydrophilic amino-terminal arm of reovirus core shell protein λ1 is dispensable for particle assembly. . J Virol 76:, 12211–12222. [CrossRef][PubMed]
    [Google Scholar]
  26. Kim J., Tao Y., Reinisch K. M., Harrison S. C., Nibert M. L.. ( 2004;). Orthoreovirus and Aquareovirus core proteins: conserved enzymatic surfaces, but not protein–protein interfaces. . Virus Res 101:, 15–28. [CrossRef][PubMed]
    [Google Scholar]
  27. Laemmli U. K.. ( 1970;). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. . Nature 227:, 680–685. [CrossRef][PubMed]
    [Google Scholar]
  28. Liemann S., Chandran K., Baker T. S., Nibert M. L., Harrison S. C.. ( 2002;). Structure of the reovirus membrane-penetration protein, μ1, in a complex with is protector protein, σ3. . Cell 108:, 283–295. [CrossRef][PubMed]
    [Google Scholar]
  29. Luongo C. L., Reinisch K. M., Harrison S. C., Nibert M. L.. ( 2000;). Identification of the guanylyltransferase region and active site in reovirus mRNA capping protein λ2. . J Biol Chem 275:, 2804–2810. [CrossRef][PubMed]
    [Google Scholar]
  30. Lupiani B., Subramanian K., Samal S. K.. ( 1995;). Aquareoviruses. . Annu Rev Fish Dis 5:, 175–208. [CrossRef]
    [Google Scholar]
  31. Maan S., Rao S., Maan N. S., Anthony S. J., Attoui H., Samuel A. R., Mertens P. P. C.. ( 2007;). Rapid cDNA synthesis and sequencing techniques for the genetic study of bluetongue and other dsRNA viruses. . J Virol Methods 143:, 132–139. [CrossRef][PubMed]
    [Google Scholar]
  32. Marchler-Bauer A., Lu S., Anderson J. B., Chitsaz F., Derbyshire M. K., DeWeese-Scott C., Fong J. H., Geer L. Y., Geer R. C.. & other authors ( 2011;). CDD: a Conserved Domain Database for the functional annotation of proteins. . Nucleic Acids Res 39: (Database issue), D225–D229. [CrossRef][PubMed]
    [Google Scholar]
  33. Mari J., Bonami J. R.. ( 1988;). W2 virus infection of the crustacean Carcinus mediterraneus: a reovirus disease. . J Gen Virol 69:, 561–571. [CrossRef][PubMed]
    [Google Scholar]
  34. Mertens P. P. C., Attoui H., Duncan R., Dermody T. S.. ( 2005;). Reoviridae. . In Virus Taxonomy. Eighth Report of the International Committee on Taxonomy of Viruses, pp. 447–454. Edited by Fauquet C. M., Mayo M. A., Maniloff J., Desselberger U., Ball L. A... London:: Elsevier/Academic Press;.
    [Google Scholar]
  35. Mohd Jaafar F., Goodwin A. E., Belhouchet M., Merry G., Fang Q., Cantaloube J. F., Biagini P., de Micco P., Mertens P. P. C., Attoui H.. ( 2008;). Complete characterisation of the American grass carp reovirus genome (genus Aquareovirus: family Reoviridae) reveals an evolutionary link between aquareoviruses and coltiviruses.. Virology 373:, 310–321. [CrossRef][PubMed]
    [Google Scholar]
  36. Noble S., Nibert M. L.. ( 1997;). Core protein μ2 is a second determinant of nucleoside triphosphatase activities by reovirus cores. . J Virol 71:, 7728–7735.[PubMed]
    [Google Scholar]
  37. Noda H., Nakashima N., Omura T.. ( 1994;). Cloning of the Nilaparvata lugens reovirus genome: conserved terminal nucleotide sequences and nucleotide sequence of genome segment S10. . J Gen Virol 75:, 221–225. [CrossRef][PubMed]
    [Google Scholar]
  38. O’Reilly E. K., Kao C. C.. ( 1998;). Analysis of RNA-dependent RNA polymerase structure and function as guided by known polymerase structures and computer predictions of secondary structure. . Virology 252:, 287–303. [CrossRef][PubMed]
    [Google Scholar]
  39. Odegard A. L., Chandran K., Zhang X., Parker J. S. L., Baker T. S., Nibert M. L.. ( 2004;). Putative autocleavage of outer capsid protein μ1, allowing release of myristoylated peptide μ1N during particle uncoating, is critical for cell entry by reovirus. . J Virol 78:, 8732–8745. [CrossRef][PubMed]
    [Google Scholar]
  40. Owens R. J., Limn C., Roy P.. ( 2004;). Role of an arbovirus nonstructural protein in cellular pathogenesis and virus release. . J Virol 78:, 6649–6656. [CrossRef][PubMed]
    [Google Scholar]
  41. Parker J. S., Broering T. J., Kim J., Higgins D. E., Nibert M. L.. ( 2002;). Reovirus core protein μ2 determines the filamentous morphology of viral inclusion bodies by interacting with and stabilizing microtubules. . J Virol 76:, 4483–4496. [CrossRef][PubMed]
    [Google Scholar]
  42. Qiu T., Luongo C. L.. ( 2003;). Identification of two histidines necessary for reovirus mRNA guanylyltransferase activity. . Virology 316:, 313–324. [CrossRef][PubMed]
    [Google Scholar]
  43. Qiu T., Lu R. H., Zhang J., Zhu Z. Y.. ( 2001;). Molecular characterization and expression of the M6 gene of grass carp hemorrhage virus (GCHV), an aquareovirus. . Arch Virol 146:, 1391–1397. [CrossRef][PubMed]
    [Google Scholar]
  44. Rao S.. ( 2002;). Characterization of a Cypovirus from Cabbage Looper (Trichoplusia ni) and development of systems for Cypovirus demarcation: a dissertation submitted in partial fulfillment of the requirement of the Graduate School of Clemson University for the degree of Doctor of Philosophy Genetics. . Clemson;: USA:.
  45. Reed L. J., Muench H.. ( 1938;). A simple method of estimating fifty percent endpoints. . Am J Hyg 27:, 493–497.
    [Google Scholar]
  46. Reinisch K. M., Nibert M. L., Harrison S. C.. ( 2000;). Structure of the reovirus core at 3.6 Å resolution. . Nature 404:, 960–967. [CrossRef][PubMed]
    [Google Scholar]
  47. Saitou N., Nei M.. ( 1987;). The neighbor-joining method: a new method for reconstructing phylogenetic trees. . Mol Biol Evol 4:, 406–425.[PubMed]
    [Google Scholar]
  48. Samal S. K., Attoui H., Mohd Jaafar F., Mertens P. P. C.. ( 2005;). Aquareovirus, Reoviridae. . In Virus Taxonomy. Eighth Report of the International Committee on Taxonomy of Viruses, pp. 511–516. Edited by Fauquet C. M., Mayo M. A., Maniloff J., Desselberger U., Ball L. A... London:: Elsevier/Academic Press;.
    [Google Scholar]
  49. Seng E. K., Fang Q., Chang S. F., Ngoh G. H., Qin Q. W., Lam T. J., Sin Y. M.. ( 2002;). Characterisation of a pathogenic virus isolated from marine threadfin fish (Eleutheronema tetradactylus) during a disease outbreak. . Aquaculture 214:, 1–18. [CrossRef]
    [Google Scholar]
  50. Shapiro A., Green T., Rao S., White S., Carner G., Mertens P. P. C., Becnel J. J.. ( 2005;). Morphological and molecular characterization of a Cypovirus (Reoviridae) from the mosquito Uranotaenia sapphirina (Diptera: Culicidae). . J Virol 79:, 9430–9438. [CrossRef][PubMed]
    [Google Scholar]
  51. Shaw A. L., Samal S. K., Subramanian K., Prasad B. V.. ( 1996;). The structure of aquareovirus shows how the different geometries of the two layers of the capsid are reconciled to provide symmetrical interactions and stabilization. . Structure 4:, 957–967. [CrossRef][PubMed]
    [Google Scholar]
  52. Su Y. P., Shien J. H., Liu H. J., Yin H. S., Lee L. H.. ( 2007;). Avian reovirus core protein μA expressed in Escherichia coli possesses both NTPase and RTPase activities. . J Gen Virol 88:, 1797–1805. [CrossRef][PubMed]
    [Google Scholar]
  53. Tamura K., Dudley J., Nei M., Kumar S.. ( 2007;). mega4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. . Mol Biol Evol 24:, 1596–1599. [CrossRef][PubMed]
    [Google Scholar]
  54. Thalmann C. M., Cummins D. M., Yu M., Lunt R., Pritchard L. I., Hansson E., Crameri S., Hyatt A., Wang L. F.. ( 2010;). Broome virus, a new fusogenic Orthoreovirus species isolated from an Australian fruit bat. . Virology 402:, 26–40. [CrossRef][PubMed]
    [Google Scholar]
  55. Thompson J. D., Higgins D. G., Gibson T. J.. ( 1994;). clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. . Nucleic Acids Res 22:, 4673–4680. [CrossRef][PubMed]
    [Google Scholar]
  56. Winton J. R., Lannan C. N., Fryer J. L., Hedrick R. P., Meyers T. R., Plumb J. A., Yamamoto T.. ( 1987;). Morphological and biochemical properties of four members of a novel group of reoviruses isolated from aquatic animals. . J Gen Virol 68:, 353–364. [CrossRef][PubMed]
    [Google Scholar]
  57. Ye X., Tian Y. Y., Deng G. C., Chi Y. Y., Jiang X. Y.. ( 2012;). Complete genomic sequence of a reovirus isolated from grass carp in China. . Virus Res 163:, 275–283. [CrossRef][PubMed]
    [Google Scholar]
  58. Yin H. S., Shien J. H., Lee L. H.. ( 2000;). Synthesis in Escherichia coli of avian reovirus core protein varsigmaA and its dsRNA-binding activity. . Virology 266:, 33–41. [CrossRef][PubMed]
    [Google Scholar]
  59. Zhang S., Shi Z., Zhang J., Bonami J. R.. ( 2004;). Purification and characterization of a new reovirus from the Chinese mitten crab, Eriocheir sinensis. . J Fish Dis 27:, 687–692. [CrossRef][PubMed]
    [Google Scholar]
  60. Zhang C., Wang Q., Shi C. B., Zeng W. W., Liu Y. K., Wu S. Q.. ( 2010;). Molecular analysis of grass carp reovirus HZ08 genome segments 1–3 and 5–6. . Virus Genes 41:, 102–104. [CrossRef][PubMed]
    [Google Scholar]
  61. Zou S., Brown E. G.. ( 1992;). Nucleotide sequence comparison of the M1 genome segment of reovirus type 1 Lang and type 3 Dearing. . Virus Res 22:, 159–164. [CrossRef][PubMed]
    [Google Scholar]
  62. Zuo W. G., Qian H. X., Xu Y. F., Du S. Y., Yang X. L.. ( 1986;). A cell line derived from the kidney of grass carp (Ctenopharyngodon idellus). . J Fish China 10:, 11–17.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.054767-0
Loading
/content/journal/jgv/10.1099/vir.0.054767-0
Loading

Data & Media loading...

Supplements

Supplementary material 

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