Abstract
Infectious salmon anaemia virus, ISA virus (genus Isavirus, family Orthomyxoviridae), emerged in Norwegian salmon culture in the mid-80s. The genome consists of eight segments coding for at least 10 proteins. ISA viruses show many of similarities to influenza A viruses but differ in many important aspects such as the number of hosts, the host population structure and the route of transmission. The only known hosts and reservoirs for ISA viruses are salmonids found in countries surrounding the North Atlantic. In this study, four different segments of the genome of about 100 ISA viruses have been sequenced in an attempt to understand the evolution of ISA viruses and how these viruses are maintained in and transmitted between populations of farmed Atlantic salmon. The four gene segments code for the nucleoprotein (NP), the putative acid polymerase (PA), the fusion protein (F) and the haemagglutinin-esterase (HE). Analysis of these four genes showed that the substitution rates of the internal proteins (NP and PA) are lower than those of the two surface proteins (F and HE). All four segments are evolving at a lower rate than similar genes in influenza A viruses. The ISA virus populations consist of avirulent viruses and pathogenic strains with variable virulence in Atlantic salmon. Recombination resulting in inserts close to the proteolytic-cleavage site of the precursor F0 protein and deletions in the stalk region of the HE protein seem to be responsible for the transition from avirulent ISA viruses to pathogenic strains. It is also shown that reassortment is a frequent event among the dominating ISA viruses in farmed Atlantic salmon. The pattern that is obtained after phylogenetic analysis of the four gene segments from ISA viruses suggests that the variation is limited to a few distinct clades and that no major changes have occurred in the ISA virus population in Norway since the first viruses were isolated. Calculation of the time of most recent common ancestor (TMRCA) suggests that the Norwegian ISA viruses separated from the European subtype found in North America between 1932 and 1959. The TMRCA data also suggest that the ISA viruses in Chile were transmitted from Norway in the period from 1995 to 2007, depending on which of the four genes were used in the analysis.
Similar content being viewed by others
References
Aspehaug V, Mikalsen AB, Snow M, Biering E, Villoing S (2005) Characterization of the infectious salmon anemia virus fusion protein. J Virol 79(19):12544–12553
Bahl J, Vijaykrishna D, Holmes EC, Smith GJD, Guan Y (2009) Gene flow and competitive exclusion of avian influenza A virus in natural reservoir hosts. Virology 390(2):289–297
Bean WJ (1984) Correlation of influenza A virus nucleoprotein genes with host species. Virology 133(2):438–442
Bouchard DA, Brockway K, Giray C, Keleher W, Merrill PL (2001) First report of infectious salmon anemia (ISA) in the United States. Bull Eur Ass Fish Pathol 21(2):86–88
Bustos P, Rozas M, Bohle H, Ildefonso R, Sandoval A, Gaete A, Araya C, Grothusen H, Tapia E, Gallardo A, Rojas A, Lara M, Labra A, Galvez C (2011). Primer reporte de piscine reovirus en salmon del Atlantico, Salmo salar, cultivado en Chile. VD Julio
Chen R, Holmes EC (2006) Avian influenza virus exhibits rapid evolutionary dynamics. Mol Biol Evol 23(12):2336–2341
Christiansen DH, Østergaard PS, Snow M, Dale OB, Falk K. (2011). A low-pathogenic variant of infectious salmon anemia virus (ISAV-HPR0) is highly prevalent and causes a non-clinical transient infection in farmed Atlantic salmon (Salmo salar L.) in the Faroe Islands. J Gen Virol 92(Pt 4):909–918. Epub 2010 Dec 9
Cook-Versloot M, Griffiths S, Cusack R, McGeachy S, Ritchie R (2004) Identification and characterization of infectious salmon anaemia virus (ISAV) haemagglutinin gene highly polymorphic regian (HPR) type 0 in North America. Bull Eur Ass Fish Pathol 24(4):203–208
Cottet L, Cortez-San Martin M, Tello M, Olivares E, Rivas-Aravena A, Vallejos E, Sandino AM, Spencer E (2010) Bioinformatic analysis of the genome of infectious salmon anemia virus associated with outbreaks with high mortality in Chile. J Virol 84(22):11916–11928
Cunningham CO, Gregory A, Black J, Simpson I, Raynard RS (2002) A novel variant of the infectious salmon anaemia virus (ISAV) haemagglutinin gene suggests mechanisms for virus diversity. Bull Eur Ass Fish Pathol 22(6):366–374
Devold M, Krossøy B, Aspehaug V, Nylund A (2000) Use of RT-PCR for diagnosis of infectious salmon anaemia virus (ISAV) in carrier sea trout Salmo trutta after experimental infection. Dis Aquat Org 40:9–18
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
Devold M, Karlsen M, Nylund A (2006). Sequence analysis of the fusion protein gene from infectious salmon anemia virus isolates: evidence of recombination and reassortment. J Gen Virol 87 (Pt7): 2031–2040
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214
Einer-Jensen K, Ahrens P, Forsberg R, Lorenzen N (2004). Evolution of the fish rhabdovirus viral haemorrhagic septicaemia virus. J Gen Virol 85(Pt5):1167–1179
Einer-Jensen K, Ahrens P, Lorenzen N (2005) Parallel phylogenetic analyses using the N, G or Nv gene from a fixed group of VHSV isolates reveal the same overall genetic typing. Dis Aquat Organ 67(1–2):39–45
Einer-Jensen K, Winton J, Lorenzen N (2005) Genotyping of the fish rhabdovirus, viral haemorrhagic septicaemia virus, by restriction fragment length polymorphisms. Vet Microbiol 106(3–4):167–178
Gammelin M, Altmüller A, Reinhardt U, Mandler J, Harley VR, Hudson PJ, Fitch WM, Scholtissek C (1990) Phylogenetic analysis of nucleoproteins suggests that human influenza A viruses emerged from a 19th-century avian ancestor. Mol Biol Evol 7(2):194–200
Godoy MG, Aedo A, Kibenge MJ, Groman DB, Yason CV, Grothusen H, Lisperguer A, Calbucura M, Avendaño F, Imilán M, Jarpa M, Kibenge FS (2008) First detection, isolation and molecular characterization of infectious salmon anaemia virus associated with clinical disease in farmed Atlantic salmon (Salmo salar) in Chile. BMC Vet Res 4:28
Gorman OT, Bean WJ, Kawaoka Y, Webster RG (1990) Evolution of the nucleoprotein gene of influenza A virus. J Virol col 64(4):1487–1497
Gorman OT, Bean WJ, Kawaoka Y, Donatelli I, Guo YJ, Webster RG (1991) Evolution of influenza A virus nucleoprotein genes: implications for the origins of H1N1 human and classical swine viruses. J Virol 65(7):3704–3714
Gorman OT, Bean WJ, Webster RG (1992) Evolutionary processes in influenza viruses: divergence, rapid evolution, and stasis. Curr Top Microbiol Immunol 176:75–97
Griffiths S, Cook M, Mallory B, Ritchie R (2001) Characterisation of ISAV proteins from cell culture. Dis Aquat Org 45:19–24
Hellebø A, Vilas U, Falk K, Vlasak R (2004) Infectious salmon anemia virus specifically binds to and hydrolyzes 4-O-acetylated sialic acids. J Virol 78(6):3055–3062
Hirst M, Astell CR, Griffith M, Coughlin SM, Moksa M, Zeng T, Smailus DE, Holt RA, Jones S, Marra MA, Petric M, Krajden M, Lawrence D, Mak A, Chow R, Skowronski DM, Tweed SA, Goh S, Brunham RC, Robinson J, Bowes V, Sojonky K, Byrne SK, Li Y, Kobasa D, Booth T, Paetzel M (2004) Novel avian influenza H7N3 strain outbreak British Columbia. Emerg Infect Dis 10(12):2192–2195
Hodneland K, Bratland A, Christie KE, Endresen C, Nylund A (2005) New subtype of salmonid alphavirus (SAV), Togaviridae, from Atlantic salmon Salmo salar and rainbow trout Oncorhynchus mykiss in Noway. Dis Aquat Organ 66(2):113–20. Erratum Dis Aquat Organ 67(1–2):181
Hungnes O, Jonassen TØ, Jonassen CM, Grinde B (2000) Molecular epidemiology of viral infections. How sequence information helps us understand the evolution and dissemination of viruses. APMIS 108:81–97
Karlsen M, Hodneland K, Endresen C, Nylund A (2006). Genetic stability within the Norwegian subtype of salmonid alphavirus (family Togaviridae). Arch Virol 151(5):861–874. Epub 2005 Dec 15
Kibenge FSB, Garate ON, Johnson G, Arriagada R, Kibenge MJT, Wadowska D (2001) Isolation and identification of infectious salmon anaemia virus (ISAV) from Coho salmon in Chile. Dis Aquat Org 45:9–18
Kibenge FS, Kibenge MJ, McKenna PK, Stothard P, Marshall R, Cusack RR, McGeachy S (2001) Antigenic variation among isolates of infectious salmon anaemia virus correlates with genetic variation of the viral haemagglutinin gene. J Gen Virol 82(Pt 12):2869–2879
Kibenge FS, Kibenge MJ, Wang Y, Qian B, Hariharan S, McGeachy S (2007) Mapping of putative virulence motifs on infectious salmon anemia virus surface glycoprotein genes. J Gen Virol 88(Pt 11):3100–3111
Kibenge FSB, Godoy MG, Wang Y, Kibenge MJT, Gherardelli V, Mansilla S, Lisperger A, Jarpa M, Larroquete G, Avendano F, Lara M, Gallardo A (2009) Infectious salmon anaemia virus (ISAV) isolated from the ISA disease outbreaks in Chile diverged from ISAV isolates from Norway around 1996 and was disseminated around 2005, based on surface glycoprotein gene sequences. Virol J 6:88
Kristiansen M, Frøystad MK, Rishovd AL, Gjøen T (2002) Characterization of the receptor-destroying enzyme activity from infectious salmon anaemia virus. J Gen Virol 83(Pt 11):2693–2697
Krossøy B, Devold M, Sanders L, Knappskog PM, Aspehaug V, Falk K, Nylund A, Koumans S, Endresen C, Biering E (2001) Cloning and identification of the Infectious salmon anemia virus hemagglutinin. J Virol 82:1757–1765
Kurath G, Garver KA, Troyer RM, Emmenegger EJ, Einer-Jensen K, Anderson ED (2003) Phylogeography of infectious haematopoietic necrosis virus in North America. J Gen Virol 84(pt 4):803–814
Lyngstad TM, Hjortaas MJ, Kristoffersen AB, Markussen T, Karlsen ET, Jonassen CM, Jansen PA. (2011). Use of molecular epidemiology to trace transmission pathways for infectious salmon anaemia virus (ISAV) in Norwegian salmon farming. Epidemics 3(1):1–11. Epub 2010 Nov 24
Markussen T, Jonassen CM, Numanovic S, Braaen S, Hjortaas M, Nilsen H, Mjaaland S (2008). Evolutionary mechanisms involved in the virulence of infectious salmon anaemia virus (ISAV), a piscine orthomyxovirus. Virology 374(2):515–527. Epub 2008 Feb 20
McBeath AJ, Bain N, Snow M (2009) Surveillance for infectious salmon anaemia virus HPR0 in marine Atlantic salmon farms across Scotland. Dis Aquat Organ 87(3):161–169
Mikalsen AB, Sindre H, Mjaaland S, Rimstad E. (2005). Expression, antigenicity and studies on cell receptor binding of the hemagglutinin of infectious salmon anemia virus. Arch Virol 150(8):1621-1637. Epub 2005 Apr 14
Müller A, Markussen T, Drabløs F, Gjøen T, Jørgensen TØ, Solem ST, Mjaaland S (2010). Structural and functional analysis of the hemagglutinin-esterase of infectious salmon anaemia virus. Virus Res 151(2):131-141. Epub 2010 Apr 14
Mullins JE, Groman D, Wadowska D (1998) Infectious salmon anaemia in salt water Atlantic salmon (Salmo salar L.) in New Brunswick, Canada. Bull Eur Ass. Fish Pathol 18(4):110–114
Mutoloki S, Evensen Ø (2011). Sequence similarities of the capsid gene of Chilean and European isolates of infectious pancreatic necrosis virus point towards a common origin. J Gen Virol 92(Pt 7):1721-1726. Epub 2011 Mar 14
Nobusawa E, Sato K (2006) Comparison of the mutation rates of human influenza A and B viruses. J Virol 80(7):3675–3678
Nylund A, Alexandersen S, Jakobsen P, Rolland JB (1995) Infectious salmon anaemia (ISA) in brown trout. J Aquat Anim Health 7:236–240
Nylund A, Kvenseth AM, Krossøy B (1995) Suceptibility of wild salmon (Salmo salar L.) to infectious salmon anaemia (ISA). Bull Eur Ass. Fish Pathol 15(5):152–156
Nylund A, Jakobsen P (1995) Sea trout as a carrier of infectious salmon anaemia virus. J Fish Biol 47:174–176
Nylund A, Kvenseth AM, Krossøy B, Hodneland K (1997) Rainbow trout (Oncorhynchus mykiss, Walbaum, 1792): A carrier of infectious salmon anaemia (ISAV). J Fish Dis 20:275–279
Nylund A, Devold M, Mullins J, Plarre H (2002) Herring (Clupea harengus): A host for infectious salmon anemia virus (ISAV). Bull Eur Ass Fish Pathol 22(5):311–318
Nylund A, Devold M, Plarre H, Isdal E, Aarseth M (2003) Emergence and maintenance of infectious salmon anemia virus (ISAV) in Europe: a new hypothesis. Dis Aquat Org 56:11–24
Nylund A, Plarre H, Karlsen M, Fridell F, Ottem KF, Bratland A, Saether PA (2007). Transmission of infectious salmon anaemia virus (ISAV) in farmed populations of Atlantic salmon (Salmo salar). Arch Virol 152 (1):151–179. Epub 2006 Aug 28
Nylund A, Karlsbakk E, Nylund S, Isaksen TE, Karlsen M, Korsnes K, Handeland S, Martinsen R, Mork Pedersen T, Ottem KF (2008) New clade of betanodaviruses detected in wild and farmed cod (Gadus morhua) in Norway. Arch Virol 153:541–547
Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358
Plarre H, Devold M, Snow M, Nylund A (2005) Prevalence of infectious salmon anaemia virus (ISAV) in wild salmonids in western Norway. Dis Aquat Organ 66(1):71–79
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25(7):1253–1256
Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14(9):817–818
Qu Y, Zhang R, Cui P, Song G, Duan Z, Lei F (2011) Evolutionary genomics of the pandemic H1N1 influenza viruses (pH1 N 1v). Virol J 8:250
Raynard RS, Murray AG, Gregory A (2001) Infectious salmon anaemia virus in wild fish from Scotland. Dis Aquat Org 46:93–100
Rimstad E, Mjaaland S, Snow M, Mikalsen AB, Cunningham CO (2001) Characterization of infectious salmon anemia virus genomic segment that encodes the putative hemagglutinin. J Virol 75(11):5352–5356
Rodger HD, Turnbull T, Muir F, Millar S, Richards RH (1998) Infectious salmon anaemia (ISA) in the United Kingdom. Bull Eur Ass Fish Pathol 18(4):115–116
Rolland JB, Winton JR (2003) Relative resistance of Pacific salmon to infectious salmon anaemia virus. J Fish Dis 26:511–520
Snow M, Raynard RS, Bruno DW (2001) Comparative susceptibility of Artic char (Salvelinus alpinus), rainbow trout (Oncorhynchus mykiss) and brown trout (Salmo trutta) to the Scottish isolate of infectious salmon anaemia virus. Aquaculture 196:47–54
Snow M, Raynard RS, Inglis J, Bruno DW (2001) Investigation into the potential for seawater rainbowtrout (Oncorhynchus mykiss) to act as vectors of infectious salmon anaemia virus (ISAV). Bull. Eur Ass Fish Pathol 21(6):252–262
Snow M, Bain N, Black J, Taupin V, Cunningham CO, King JA, Skall HF, Raynard RS (2004) Genetic population structure of marine viral haemorrhagic septicaemia virus (VHSV). Dis Aquat Organ 61(1–2):11–21
Thiéry R, Cozien J, de Boisséson C, Kerbart-Boscher S, Névarez L (2004) Genomic classification of new betanodavirus isolates by phylogenetic analysis of the coat protein gene suggests a low host-fish species specificity. J Gen Virol 85(Pt 10):3079–3087
Vike S, Nylund S, Nylund A (2009). ISA virus in Chile: evidence of vertical transmission. Arch Virol 154(1):1–8. Epub 2008 Nov 26
Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y (1992) Evolution and ecology of influenza A viruses. Microbiol Rev 56:152–179
Wong KK, Bull RA, Stelzer-Braid S, Fennell M, Rawlinson W (2011). Effect of reassortment on the nucleotide and amino acid changes of human A/H3N2 RNP subunits during 1998-2009. J Clin Virol 51(4):270–275. Epub 2011 Jun 14
Xu J, Christman MC, Donis RO, Lu G (2011). Evolutionary dynamics of influenza A nucleoprotein (NO) lineages revealed by large-scale sequence analyses. Infect Genet Evol 11(8):2125-2132. Epub 2011
Acknowledgments
This work was financed by the Norwegian Research Council.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Plarre, H., Nylund, A., Karlsen, M. et al. Evolution of infectious salmon anaemia virus (ISA virus). Arch Virol 157, 2309–2326 (2012). https://doi.org/10.1007/s00705-012-1438-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-012-1438-0