Skip to main content
SpringerLink
Log in

Morphogenesis of salmonid gill poxvirus associated with proliferative gill disease in farmed Atlantic salmon (Salmo salar) in Norway

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Proliferative gill disease (PGD) is an emerging problem in Norwegian culture of Atlantic salmon (Salmo salar). Parasites (Ichthyobodo spp.) and bacteria (Flexibacter/Flavobacterium) may cause PGD, but for most cases of PGD in farmed salmon in Norway, no specific pathogen has been identified as the causative agent. However, Neoparamoeba sp. and several bacteria and viruses have been associated with this disease. In the spring of 2006, a new poxvirus, salmon gill poxvirus (SGPV), was discovered on the gills of salmon suffering from PGD in fresh water in northern Norway. Later the same year, this virus was also found on gills of salmon at two marine sites in western Norway. All farms suffered high losses associated with the presence of this virus. In this study, we describe the entry and morphogenesis of the SGP virus in epithelial gill cells from Atlantic salmon. Intracellular mature virions (IMVs) are the only infective particles that seem to be produced. These are spread by cell lysis and by “budding” of virus packages, containing more that 100 IMVs, from the apical surface of infected cells. Entry of the IMVs appears to occur by attachment to microridges on the cell surface and fusion of the viral and cell membranes, delivering the cores into the cytoplasm. The morphogenesis starts with the emergence of crescents in viroplasm foci in perinuclear areas of infected cells. These crescents consist of two tightly apposed unit membranes (each 5 nm thick) that seem to be derived from membranes of the endoplasmic reticulum. The crescents develop into spheres, immature virions (IVs), that are 350 nm in diameter and surrounded by two unit membranes. The maturation of the IVs occurs by condensation of the core material and a change from spherical to boat-shaped particles, intracellular mature virions (IMVs), that are about 300 nm long. Hence, the IMVs from the SGP virus have a different morphology compared to other vertebrate poxviruses that are members of the subfamily Chordopoxvirinae, and they are more similar to members of subfamily Entomopoxvirinae, genus Alphaentomopoxvirus. However, it is premature to make a taxonomic assignment until the genome of the SGP virus has been sequenced, but morphogenesis clearly shows that this virus is a member of family Poxviridae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  1. Bergoin M, Devauchelle G, Vago C (1969) Electron microscopy study of the pox-like virus of Melolontha melolontha L (Coleoptera, Scarabeidae). Virus morphogenesis. Arch Gesamte Virusforsch 28:285–308

    Article  PubMed  CAS  Google Scholar 

  2. Carter GC, Law M, Hollinshead M, Smith GL (2005) Entry of the vaccinia virus intracellular mature virion and its interactions with glycosamineiglycans. J Gen Virol 86:1279–1290

    Article  PubMed  CAS  Google Scholar 

  3. Dales S, Siminovitch I (1961) The development of vaccinia virus in Earles L strain cells as examined by electron microscopy. J Biophys Biochem Cytol 10:475–503

    Article  PubMed  CAS  Google Scholar 

  4. Dales S, Mosbach EH (1968) Vaccinia as a model for membrane biogenesis. Virology 35:564–583

    Article  PubMed  CAS  Google Scholar 

  5. Devold M, Falk K, Dale OB, Krossøy B, Biering E, Aspehaug V, Nilsen F, Nylund A (2001) Strain variation, based on the hemagglutinin gene, in Norwegian ISA virus isolates collected from 1987 to 2001: indications of recombination. Dis Aquat Org 47:119–128

    Article  PubMed  CAS  Google Scholar 

  6. Drahgi A, Vsevolod LP, Kahl MM, Stanton JB, Brown CC, Tsongalis G, West AB, Frasca S (2004) Characterization of “Candidatus Piscichlamydia salmonis” (Order Chlamydiales), a Chlamydia-like bacterium associated with epitheliocystis in farmed Atlantic salmon (Salmo salar). J Clin Microbiol 42:5286–5297

    Article  CAS  Google Scholar 

  7. Duteyrat JL, Gelfi J, Bertagnoli S (2006) Ultrastructural study of myxoma virus morphogenesis. Arch Virol 151:2161–2180

    Article  PubMed  CAS  Google Scholar 

  8. Fridell F (2003) Detection of a paramyxovirus in selected tissues from Salmo salar after experimental challenge, Master thesis. Department of Fisheries and Marine Biology, University of Bergen, Norway, pp 68 (in Norwegian)

  9. Fridell F, Devold M, Nylund A (2004) Phylogenetic position of a paramyxovirus from Atlantic salmon Salmo salar. Dis Aquat Org 59:11–15

    Article  PubMed  CAS  Google Scholar 

  10. Griffiths G, Roos N, Schleich S, Krijnse Locker J (2001) Structure and assembly of intracellular mature vaccinia virus: thin-section analysis. J Virol 75:11056–11070

    Article  PubMed  CAS  Google Scholar 

  11. Griffiths G, Wepf R, Wendt T, Krijnse Locker J, Cyrklaff M, Roos N (2001) Structure and assembly of intracellular mature vaccinia virus: isolated-particle analysis. J Virol 75:11034–11055

    Article  PubMed  CAS  Google Scholar 

  12. Grimley PM, Rosenblum EN, Mims SJ, Moss B (1970) Interruption by rifampin of an early stage in vaccinia virus morphogenesis: accumulation of membranes which are precursors of virus envelopes. J Virol 6:519–533

    PubMed  CAS  Google Scholar 

  13. Heuser J (2005) Deep-etch EM reveals that the early poxvirus envelope is a single membrane bilayer stabilized by a geodetic “honeycomb” surface coat. J Cell Biol 169:269–283

    Article  PubMed  CAS  Google Scholar 

  14. Hussain M, Moss B (2003) Evidence against an essential role of COPII-mediated cargo transport to the endoplasmic reticulum–Golgi intermediate compartment in the formation of the primary membrane of vaccinia virus. J Virol 77:11754–11766

    Article  CAS  Google Scholar 

  15. Isaksen TE, Karlsbakk E, Todal JA, Nylund A (2002) Ichthyobodo infection on salmon at a brood fish site: infection dynamic, morphology and reservoirs. Fiskehelse 4:16–23 (in Norwegian)

    Google Scholar 

  16. Isaksen TE (2003) Protozoan ectosymbionts on Atlantic salmon (Salmo salar L.) in a hatchery in Hordaland, western Norway: morphology and epizootiology, Cand. Scient. thesis. University of Bergen, Department of Biology, pp 131

  17. Karlsen M, Nylund A, Watanabe K, Helvik JV, Nylund S, Plarre H (2008) Characterization of “Candidatus Clavochlamydia salmonicola”: an intracellular bacterium infecting salmonid fish. Environ Microbiol 10:208–218 (E-publ. 2007)

    PubMed  CAS  Google Scholar 

  18. Knipe DM, Howley PM (2007) Fields virology. Lippincott Williams & Wilkins, Philadelphia

    Google Scholar 

  19. Kochan JM, Escors D, Gonzales JM, Casasnovas JM, Esteban M (2007) Membrane cell fusion activity of the vaccinia virus A17–A27 protein complex. Cell Microbiol 10:149–164

    PubMed  Google Scholar 

  20. Krijnse-Locker J, Kuehn A, Schleich S, Rutter G, Hohenberg H, Wepf R, Griffiths G (2000) Entry of the two infectious forms of vaccinia virus at the plasma membrane is signalling-dependent for the IMV but not for the EEV. Mol Biol Cell 11:2497–2511

    Google Scholar 

  21. Kvellestad A, Dannevig BH, Falk K (2003) Isolation and partial characterization of a novel paramyxovirus from gills of diseased seawater reared Atlantic salmon (Salmo salar L). J Gen Virol 84:2179–2189

    Article  PubMed  CAS  Google Scholar 

  22. Kvellestad A, Falk K, Nygaard SMR, Flesjå K, Holm JA (2005) Atlantic salmon paramyxovirus (ASPV) infection contributes to proliferative gill inflammation (PGI) in seawater-reared Salmo salar. Dis Aquat Org 67:47–54

    Article  PubMed  Google Scholar 

  23. Law M, Carter GC, Roberts KL, Hollinshead M, Smith GL (2006) Ligand-induced and nonfusogenic dissolution of a viral membrane. PNAS 103:5989–5994

    Article  PubMed  CAS  Google Scholar 

  24. Lawrene PO (2005) Morphogenesis and cytopathic effects of the Diachasmimorpha longicaudata entomopoxvirus in host haemocytes. J Insect Physiol 51:221–233

    Article  CAS  Google Scholar 

  25. Marlow SA, Billam LJ, Palmer CP, King LA (1993) Replication and morphogenesis of Amsacta moorei entomopoxvirus in cultured cells of Astigmene acrea (salt marsh caterpillar). J Gen Virol 74:1457–1461

    Article  PubMed  Google Scholar 

  26. Miyasaki T, Isshiki T, Katsuyuki H (2005) Histopathological and electron microscopy studies on sleepy disease of koi Cyprinus carpio koi in Japan. Dis Aquat Org 65:197–207

    Article  Google Scholar 

  27. Moss B (2006) Poxvirus entry and membrane fusion. Virology 344:48–54

    Article  PubMed  CAS  Google Scholar 

  28. Nygaard SMR (2004) Mapping of epithelicystis in marine farms. Norsk Fiskeoppdrett 29(11):46–48 (in Norwegian)

    Google Scholar 

  29. Nylund A, Hovland T, Watanabe K, Endresen C (1995) Presence of infectious salmon anaemia virus (ISAV) in tissues of Atlantic salmon, Salmo salar L., collected during three separate outbreaks of the disease. J Fish Dis 18:135–145

    Article  Google Scholar 

  30. Nylund A, Kvenseth AM, Isdal E (1998) A morphological study of the epitheliocystis agent in farmed Atlantic salmon. J Aquat Anim Health 10:43–55

    Article  Google Scholar 

  31. Nylund A, Karlsbakk E, Koren C, Sæther PA, Larsen T, Nielsen BD, Brøderud AE, Høstlund C, Fjellsøy KR, Lervik K, Rosnes L (2005) Parvicapsula pseudobranchicola (Myxosporea) in farmed Atlantic salmon Salmo salar: tissue distribution, diagnosis and phylogeny. Dis Aquat Org 63:197–204

    Article  PubMed  CAS  Google Scholar 

  32. Nylund A, Watanabe K, Karlsen M, Nylund S, Karlsbakk E, Sæther PA (2006) A new gill disease in salmon—Poxvirus. Norsk Fiskeoppdrett 31(7):54–56 (in Norwegian)

    Google Scholar 

  33. Nylund A, Karlsen M, Watanabe K, Karlsbakk E, Nylund S, Isaksen T, Arnesen CE (2007) A breakthrough in the battle against PGI (Proliferative gill inflammation). Norsk Fiskeoppdrett 32(3):50–53 (in Norwegian)

    Google Scholar 

  34. Nylund S, Karlsen M, Nylund A (2008) The complete genome of the Atlantic salmon paramyxovirus (ASPV). Virology 373:137–148 (E-publ 2007)

    Article  PubMed  CAS  Google Scholar 

  35. Radek R, fable P (2000) A new Entomopoxvirus from cockroach: light and electron microscopy. J Invert Pathol 75:19–27

    Article  CAS  Google Scholar 

  36. Risco C, Rodriguez JR, Lopez-Iglesias C, Carrascosa JL, Esteban M, Rodriguez D (2002) Endoplasmic reticulum–Golgi intermediate compartment membranes and vimentin filaments participate in vaccinia virus assembly. J Virol 76:1839–1855

    Article  PubMed  CAS  Google Scholar 

  37. Schramm B, Krijnse Locker J (2005) Cytoplasmic organization of poxvirus DNA replication. Traffic 6:839–846

    Article  PubMed  CAS  Google Scholar 

  38. Senkevich TG, Ojeda S, Townsley A, Nelson GE, Moss B (2005) Poxvirus multiprotein entry-fusion complex. PNAS USA 102:18572–18577

    Article  PubMed  CAS  Google Scholar 

  39. Sodeik B, Krijnse-Locker J (2002) Assembly of vaccinia virus revisited: de novo membrane synthesis or acquisition from the host? Trends Microbiol 10:15–24

    Article  PubMed  CAS  Google Scholar 

  40. Todal JA, Karlsbakk E, Isaksen TE, Plarre H, Urawa S, Mouton A, Hoel E, Koren CWR, Nylund A (2004) Ichthyobodo necator (Kinetoplastida)—a complex of sibling species. Dis Aquat Org 58:9–16

    Article  PubMed  Google Scholar 

  41. Townsley AC, Weisber AS, Wagnaar TR, Moss B (2006) Vaccinia virus entry into cells via a low-pH-dependent endosomal pathway. J Virol 80(18):8899–8900

    Article  PubMed  CAS  Google Scholar 

  42. Vanderplascchen A, Hollinshead M, Smith GL (1998) Intracellular and extracellular vaccinia virions enter cells by different mechanisms. J Gen Virol 79:877–887

    Google Scholar 

  43. Young ND, Crosbie PBB, Adams MB, Nowak BF, Morrison RN (2007) Neoparamoeba perurans n.sp., an agent of amoebic gill disease of Atlantic salmon (Salmo salar). Int J Parasitol 37:1469–1481

    Article  PubMed  CAS  Google Scholar 

  44. Watanabe K, Økland S, Hovland T, Midttun B, Nylund A (1995) Epitheliocystis in famed salmon. Norsk Fiskeoppdrett 20(21):30 (in Norwegian)

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, University of Bergen, Thormøhlensgt 55, 5020, Bergen, Norway

    Are Nylund, K. Watanabe, S. Nylund, M. Karlsen, P. A. Sæther, C. E. Arnesen & E. Karlsbakk

Authors
  1. Are Nylund
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. Watanabe
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Nylund
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Karlsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P. A. Sæther
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C. E. Arnesen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. E. Karlsbakk
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Are Nylund.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nylund, A., Watanabe, K., Nylund, S. et al. Morphogenesis of salmonid gill poxvirus associated with proliferative gill disease in farmed Atlantic salmon (Salmo salar) in Norway. Arch Virol 153, 1299–1309 (2008). https://doi.org/10.1007/s00705-008-0117-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-008-0117-7

Keywords

Search

Navigation