1887

Abstract

Interspecies transmission of viruses, where a pathogen crosses species barriers and jumps from its original host into a novel species, has been receiving increasing attention. Viral covert mortality disease, caused by covert mortality nodavirus (CMNV), is an emerging disease that has recently had a substantial impact on shrimp aquaculture in Southeast Asia and Latin America. While investigating the host range of CMNV, we found that this virus is also capable of infecting populations of the farmed Japanese flounder Paralichthys olivaceus, a vertebrate host. The infected fish were being raised in aquaculture facilities that were also producing marine shrimp. Through RT-nPCR, targeting the RNA-dependent RNA polymerase (RdRp) gene of CMNV, we found that 29 % of the fish sampled were positive. The amplicons were sequenced and aligned to the RdRp gene of shrimp CMNV and were found to have 98 % identity. Histopathological examination indicated that CMNV-positive fish showed vacuolation of nervous tissue in the eye and brain, as well as extensive necrosis of cardiac muscle. In situ hybridization showed positive reactions in tissues of the eye, brain, heart, liver, spleen and kidney of infected fish. Transmission electron microscopy showed the presence of CMNV-like particles in all of the above-mentioned tissues, except for brain. The novel finding of a shrimp alphanodavirus that can also infect farmed P. olivaceus indicates that this virus is capable of naturally crossing the species barrier and infecting another vertebrate. This finding will contribute to the development of efficient strategies for disease management in aquaculture.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001177
2018-11-21
2019-08-22
Loading full text...

Full text loading...

References

  1. Zhang Q, Liu Q, Liu S, Yang H, Liu S et al. A new nodavirus is associated with covert mortality disease of shrimp. J Gen Virol 2014;95:2700–2709 [CrossRef][PubMed]
    [Google Scholar]
  2. Zhang Q, Xu T, Wan X, Liu S, Wang X et al. Prevalence and distribution of covert mortality nodavirus (CMNV) in cultured crustacean. Virus Res 2017;233:113–119 [CrossRef][PubMed]
    [Google Scholar]
  3. Zhang QH. To be cautious of “bottom death” in the intensive farming of Pacific white shrimp. Sci Fish Farming 2004;10:48–49
    [Google Scholar]
  4. Xing H. Discussion of the control measures for the “bottom death” (covert mortality disease) of Pacific white shrimp. China Fish 2004;4:88–89
    [Google Scholar]
  5. Thitamadee S, Prachumwat A, Srisala J, Jaroenlak P, Salachan PV et al. Review of current disease threats for cultivated penaeid shrimp in Asia. Aquaculture 2016;452:69–87 [CrossRef]
    [Google Scholar]
  6. Pooljun C, Direkbusarakom S, Chotipuntu P, Hirono I, Wuthisuthimethavee S. Development of a TaqMan real-time RT-PCR assay for detection of covert mortality nodavirus (CMNV) in penaeid shrimp. Aquaculture 2016;464:445–450 [CrossRef]
    [Google Scholar]
  7. King AMQ, Lefkowitz E, Adams MJ, Carstens EB. Virus taxonomy classification and nomenclature of viruses: Ninth report of the international committee on taxonomy of viruses. Elsevier Acadmic Press 2012;1019–1025
    [Google Scholar]
  8. Scherer WF, Hurlbut HS. Nodamura virus from Japan: a new and unusual arbovirus resistant to diethyl ether and chloroform. Am J Epidemiol 1967;86:271–285 [CrossRef][PubMed]
    [Google Scholar]
  9. Tesh RB. Infectivity and pathogenicity of nodamura virus for mosquitoes. J Gen Virol 1980;48:177–182 [CrossRef]
    [Google Scholar]
  10. Johnson KL, Price BD, Ball LA. Recovery of infectivity from cDNA clones of nodamura virus and identification of small nonstructural proteins. Virology 2003;305:436–451 [CrossRef][PubMed]
    [Google Scholar]
  11. Scherer WF, Verna JE, Richter W. Nodamura virus, an ether- and chloroform-resistant arbovirus from Japan: physical and biological properties, with ecologic observations. Am J Trop Med Hyg 1968;17:120–128[PubMed]
    [Google Scholar]
  12. Johnson KL, Price BD, Eckerle LD, Ball LA. Nodamura virus nonstructural protein B2 can enhance viral RNA accumulation in both mammalian and insect cells. J Virol 2004;78:6698–6704 [CrossRef][PubMed]
    [Google Scholar]
  13. Iwamoto T, Okinaka Y, Mise K, Mori K, Arimoto M et al. Identification of host-specificity determinants in betanodaviruses by using reassortants between striped jack nervous necrosis virus and sevenband grouper nervous necrosis virus. J Virol 2004;78:1256–1262 [CrossRef][PubMed]
    [Google Scholar]
  14. Chi SC, Lo BJ, Lin SC. Characterization of grouper nervous necrosis virus (GNNV). J Fish Dis 2001;24:3–13 [CrossRef]
    [Google Scholar]
  15. Tanaka S, Kuriyama I, Nakai T, Miyazaki T. Susceptibility of cultured juveniles of several marine fish to the sevenband grouper nervous necrosis virus. J Fish Dis 2003;26:109–115 [CrossRef][PubMed]
    [Google Scholar]
  16. Ucko M, Colorni A, Diamant A. Nodavirus infections in Israeli mariculture. J Fish Dis 2004;27:459–469 [CrossRef][PubMed]
    [Google Scholar]
  17. Walker PJ, Winton JR. Emerging viral diseases of fish and shrimp. Vet Res 2010;41:51 [CrossRef][PubMed]
    [Google Scholar]
  18. Wang F, Ma Y, Barrett JW, Gao X, Loh J et al. Disruption of Erk-dependent type I interferon induction breaks the myxoma virus species barrier. Nat Immunol 2004;5:1266–1274 [CrossRef][PubMed]
    [Google Scholar]
  19. Kuiken T, Holmes EC, McAuley J, Rimmelzwaan GF, Williams CS et al. Host species barriers to influenza virus infections. Science 2006;312:394–397 [CrossRef][PubMed]
    [Google Scholar]
  20. Tang Q, Maul GG. Mouse cytomegalovirus crosses the species barrier with help from a few human cytomegalovirus proteins. J Virol 2006;80:7510–7521 [CrossRef][PubMed]
    [Google Scholar]
  21. Parrish CR, Holmes EC, Morens DM, Park EC, Burke DS et al. Cross-species virus transmission and the emergence of new epidemic diseases. Microbiol Mol Biol Rev 2008;72:457–470 [CrossRef][PubMed]
    [Google Scholar]
  22. Kreuder Johnson C, Hitchens PL, Smiley Evans T, Goldstein T, Thomas K et al. Spillover and pandemic properties of zoonotic viruses with high host plasticity. Sci Rep 2015;5:14830 [CrossRef][PubMed]
    [Google Scholar]
  23. Gibbs MJ, Weiller GF. Evidence that a plant virus switched hosts to infect a vertebrate and then recombined with a vertebrate-infecting virus. Proc Natl Acad Sci USA 1999;96:8022–8027 [CrossRef][PubMed]
    [Google Scholar]
  24. Shi Y, Wu Y, Zhang W, Qi J, Gao GF. Enabling the 'host jump': structural determinants of receptor-binding specificity in influenza A viruses. Nat Rev Microbiol 2014;12:822–831 [CrossRef][PubMed]
    [Google Scholar]
  25. Bourret V, Lyall J, Frost SDW, Teillaud A, Smith CA et al. Adaptation of avian influenza virus to a swine host. Virus Evol 2017;3:vex007 [CrossRef][PubMed]
    [Google Scholar]
  26. Ding NZ, Xu DS, Sun YY, He HB, He CQ. A permanent host shift of rabies virus from Chiroptera to Carnivora associated with recombination. Sci Rep 2017;7:289 [CrossRef][PubMed]
    [Google Scholar]
  27. Selling BH, Allison RF, Kaesberg P. Genomic RNA of an insect virus directs synthesis of infectious virions in plants. Proc Natl Acad Sci USA 1990;87:434–438 [CrossRef][PubMed]
    [Google Scholar]
  28. Stock SP, Vandenburg J, Glazer I, Boemare N, Stock SP et al. Insect Pathogens: Molecular Approaches and Techniques Wallingford, UK: CAB International; 2009
    [Google Scholar]
  29. Bailey L, Newman JF, Porterfield JS. The multiplication of Nodamura virus in insect and mammalian cell cultures. J Gen Virol 1975;26:15–20 [CrossRef][PubMed]
    [Google Scholar]
  30. Bailey L, Scott HA. The pathogenicity of Nodamura virus for insects. Nature 1973;241:545 [CrossRef][PubMed]
    [Google Scholar]
  31. Ball LA, Johnson KL. Reverse genetics of nodaviruses. Adv Virus Res 1999;53:229–244[PubMed]
    [Google Scholar]
  32. Scotti PD, Dearing S, Mossop DW. Flock House virus: a nodavirus isolated from Costelytra zealandica (White) (Coleoptera: Scarabaeidae). Arch Virol 1983;75:181–189 [CrossRef][PubMed]
    [Google Scholar]
  33. Furusawa R, Okinaka Y, Uematsu K, Nakai T. Screening of freshwater fish species for their susceptibility to a betanodavirus. Dis Aquat Organ 2007;77:119–125 [CrossRef][PubMed]
    [Google Scholar]
  34. Bigarré L, Cabon J, Baud M, Heimann M, Body A et al. Outbreak of betanodavirus infection in tilapia, Oreochromis niloticus (L.), in fresh water. J Fish Dis 2009;32:667–673 [CrossRef][PubMed]
    [Google Scholar]
  35. Souto S, Lopez-Jimena B, Alonso MC, García-Rosado E, Bandín I. Experimental susceptibility of European sea bass and Senegalese sole to different betanodavirus isolates. Vet Microbiol 2015;177:53–61 [CrossRef][PubMed]
    [Google Scholar]
  36. Gomez DK, Baeck GW, Kim JH, Choresca CH, Park SC. Molecular detection of betanodaviruses from apparently healthy wild marine invertebrates. J Invertebr Pathol 2008;97:197–202 [CrossRef][PubMed]
    [Google Scholar]
  37. Chi SC, Lo CF, Kou GH, Chang PS, Peng SE et al. Mass mortalities associated with viral nervous necrosis (VNN) disease in two species of hatchery-reared grouper, Epinephelus fuscogutatus and Epinephelus akaara (Temminck & Schlegel). J Fish Dis 1997;20:185–193 [CrossRef]
    [Google Scholar]
  38. Azad IS, Shekhar MS, Thirunavukkarasu AR, Poornima M, Kailasam M et al. Nodavirus infection causes mortalities in hatchery produced larvae of Lates calcarifer: first report from India. Dis Aquat Organ 2005;63:113–118 [CrossRef][PubMed]
    [Google Scholar]
  39. Fujiwara A, Fujiwara M, Nishida-Umehara C, Abe S, Masaoka T. Characterization of Japanese flounder karyotype by chromosome bandings and fluorescence in situ hybridization with DNA markers. Genetica 2007;131:267–274 [CrossRef][PubMed]
    [Google Scholar]
  40. Shao C, Niu Y, Rastas P, Liu Y, Xie Z et al. Genome-wide SNP identification for the construction of a high-resolution genetic map of Japanese flounder (Paralichthys olivaceus): applications to QTL mapping of Vibrio anguillarum disease resistance and comparative genomic analysis. DNA Res 2015;22:161–170 [CrossRef][PubMed]
    [Google Scholar]
  41. Seikai T. Flounder culture and its challenges in Asia. Reviews in Fisheries Science 2002;10:421–432 [CrossRef]
    [Google Scholar]
  42. Nystoyl R, Tveteras R. Fish production estimates and trends 2012–2013. 2013; Available athttp://www.gaalliance.org/cmsAdmin/uploads/tveteras.pdf
  43. World Organization for Animal Health (OIE) Viral encephalopathy and retinopathy. Manual of Diagnostic Tests for Aquatic Animals Paris, France: OIE; 2017
    [Google Scholar]
  44. Howard CR, Fletcher NF. Emerging virus diseases: can we ever expect the unexpected?. Emerg Microbes Infect 2012;1:e46 [CrossRef][PubMed]
    [Google Scholar]
  45. Longdon B, Brockhurst MA, Russell CA, Welch JJ, Jiggins FM. The evolution and genetics of virus host shifts. PLoS Pathog 2014;10:e1004395 [CrossRef][PubMed]
    [Google Scholar]
  46. Tamura K, Peterson D, Peterson N, Stecher G, Nei M et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011;28:2731–2739 [CrossRef][PubMed]
    [Google Scholar]
  47. Bell TA, Lightner DV. A Handbook of Normal Penaeid Shrimp Histology Baton Rouge, LA: World Aquaculture Society; 1988
    [Google Scholar]
  48. Lightner DV. A handbook of shrimp pathology and diagnostic procedures for diseases of cultured penaeid shrimp Baton Rouge, LA: World Aquaculture Society; 1996
    [Google Scholar]
  49. Piette D, Hendrickx M, Willems E, Kemp CR, Leyns L. An optimized procedure for whole-mount in situ hybridization on mouse embryos and embryoid bodies. Nat Protoc 2008;3:1194–1201 [CrossRef][PubMed]
    [Google Scholar]
  50. Chen S, Zhang G, Shao C, Huang Q, Liu G et al. Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. Nat Genet 2014;46:253–260 [CrossRef][PubMed]
    [Google Scholar]
  51. Nuovo GJ, Plaia TW, Belinsky SA, Baylin SB, Herman JG. In situ detection of the hypermethylation-induced inactivation of the p16 gene as an early event in oncogenesis. Proc Natl Acad Sci USA 1999;96:12754–12759 [CrossRef][PubMed]
    [Google Scholar]
  52. Graham L, Orenstein JM. Processing tissue and cells for transmission electron microscopy in diagnostic pathology and research. Nat Protoc 2007;2:2439–2450 [CrossRef][PubMed]
    [Google Scholar]
  53. Panphut W, Senapin S, Sriurairatana S, Withyachumnarnkul B, Flegel TW. A novel integrase-containing element may interact with Laem-Singh virus (LSNV) to cause slow growth in giant tiger shrimp. BMC Vet Res 2011;7:18 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001177
Loading
/content/journal/jgv/10.1099/jgv.0.001177
Loading

Data & Media loading...

Supplementary File 1

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