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Published in: Virology Journal 1/2014

Open Access 01-12-2014 | Research

Genetic analysis and comparative virulence of infectious salmon anemia virus (ISAV) types HPR7a and HPR7b from recent field outbreaks in Chile

Authors: Marcos G Godoy, Rudy Suarez, Eduardo S Lazo, Katerina O Llegues, Molly JT Kibenge, Yingwei Wang, Frederick SB Kibenge

Published in: Virology Journal | Issue 1/2014

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Abstract

Background

Infectious salmon anemia (ISA) is a serious disease of marine farmed Atlantic salmon, Salmo salar L. caused by ISA virus (ISAV). ISAV genomic segments 5 and 6 encode surface glycoproteins hemagglutinin-esterase (HE) and F protein important for the pathogenicity of ISAV. In this study, we describe the genetic characteristics and relationship between ISAV-HPR7a and ISAV-HPR7b strains that caused the ISA outbreaks in Chile in 2013 and 2014, respectively, and the evolution of the ISAV clades since 2009 based on segment 5 and 6 sequences.

Methods

The study material included samples from six ISA cases in Chile. RNA was extracted from salmon tissues and ISAV isolated from cell culture; segments 5 and 6 were amplified by RT-PCR and compared by alignment with ISAV sequences from the GenBank database.

Results

ISAV-HPR7a and ISAV-HPR7b belong to the European Genotype I strains only found in Europe and Chile, and in both cases, show high similarity in segments 5 and 6 with identity between 95–96%. Our data confirm the hypothesis that the original virus was introduced to Chile in 1996. Compared to the 2007 ISAV-HPR7b isolate, the 2014 ISAV-HPR7b does not have an insertion in segment 5 and was associated with low mortality, which suggests that ISAV virulence was attenuated by the absence of the insertion in segment 5. In contrast, the highly virulent ISAV-HPR14 from April 2013 outbreak did not have the insertion in segment 5 either.

Conclusion

Variability in the ISAV virulence markers supports the quasispecies theory that multiple evolution forces are likely to shape ISAV genetic diversity. Our findings provide evidence of continuing evolution of ISAV in the Chilean aquaculture industry.
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Literature
1.
go back to reference McCauley JW, Hongo S, Kaverin NV, Kochs G, Lamb RA, Matrosovich MN, Perez DR, Palese P, Presti RM, Rimstad E: Family Orthomyxoviridae. In Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Edited by: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ. Academic, San Diego; 2011:749-761. McCauley JW, Hongo S, Kaverin NV, Kochs G, Lamb RA, Matrosovich MN, Perez DR, Palese P, Presti RM, Rimstad E: Family Orthomyxoviridae. In Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Edited by: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ. Academic, San Diego; 2011:749-761.
2.
go back to reference Godoy M, Aedo A, Kibenge M, Groman D, Yason C, Grothusen H, Lisperguer A, Calbucura M, Avendaño F, Imilán M, Jarpa M, Kibenge F: 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 2008, 4: 28. 10.1186/1746-6148-4-28PubMedPubMedCentralCrossRef Godoy M, Aedo A, Kibenge M, Groman D, Yason C, Grothusen H, Lisperguer A, Calbucura M, Avendaño F, Imilán M, Jarpa M, Kibenge F: 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 2008, 4: 28. 10.1186/1746-6148-4-28PubMedPubMedCentralCrossRef
3.
go back to reference Kibenge FS, Kibenge MJ, Gherardelli V, Mansilla S, Lisperger A, Jarpa M, Larroquete G, Avendão F, Lara M, Gallardo A, Godoy MG, Wang Y: 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. Virology J 2009, 6: 88. 10.1186/1743-422X-6-88CrossRef Kibenge FS, Kibenge MJ, Gherardelli V, Mansilla S, Lisperger A, Jarpa M, Larroquete G, Avendão F, Lara M, Gallardo A, Godoy MG, Wang Y: 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. Virology J 2009, 6: 88. 10.1186/1743-422X-6-88CrossRef
4.
go back to reference Nylund H, Plarre M, Karlsen F, Fridell KF, Ottem A, Bratland A, Sæther PA: Transmission of infectious salmon anaemia virus (ISAV) in farmed populations of Atlantic salmon (Salmo salar). Arch Virol 2007, 152: 151-179. 10.1007/s00705-006-0825-9PubMedCrossRef Nylund H, Plarre M, Karlsen F, Fridell KF, Ottem A, Bratland A, Sæther PA: Transmission of infectious salmon anaemia virus (ISAV) in farmed populations of Atlantic salmon (Salmo salar). Arch Virol 2007, 152: 151-179. 10.1007/s00705-006-0825-9PubMedCrossRef
5.
go back to reference Krossøy B, Nilsen F, Falk K, Endresen C, Nylund A: Phylogenetic analysis of infectious salmon anaemia isolates from Norway, Canada and Scotland. Dis Aquat Org 2001, 44: 1-6. 10.3354/dao044001PubMedCrossRef Krossøy B, Nilsen F, Falk K, Endresen C, Nylund A: Phylogenetic analysis of infectious salmon anaemia isolates from Norway, Canada and Scotland. Dis Aquat Org 2001, 44: 1-6. 10.3354/dao044001PubMedCrossRef
6.
go back to reference Raynard RS, Murray AG, Gregory A: Infectious salmon anemia virus in wild fish from Scotland. Dis Aquat Organ 2001, 46: 93-100. 10.3354/dao046093PubMedCrossRef Raynard RS, Murray AG, Gregory A: Infectious salmon anemia virus in wild fish from Scotland. Dis Aquat Organ 2001, 46: 93-100. 10.3354/dao046093PubMedCrossRef
7.
go back to reference Falk K, Aspehaug V, Vlasak R, Endresen C: Identification and characterization of viral structural proteins of infectious salmon anemia virus. J Virol 2004, 78: 3063-3071. 10.1128/JVI.78.6.3063-3071.2004PubMedPubMedCentralCrossRef Falk K, Aspehaug V, Vlasak R, Endresen C: Identification and characterization of viral structural proteins of infectious salmon anemia virus. J Virol 2004, 78: 3063-3071. 10.1128/JVI.78.6.3063-3071.2004PubMedPubMedCentralCrossRef
8.
go back to reference Aspehaug V, Mikalsen AB, Snow M, Biering E, Villoing S: Characterization of the infectious salmon anemia virus fusion protein. J Virol 2005, 79: 12544-12553. 10.1128/JVI.79.19.12544-12553.2005PubMedPubMedCentralCrossRef Aspehaug V, Mikalsen AB, Snow M, Biering E, Villoing S: Characterization of the infectious salmon anemia virus fusion protein. J Virol 2005, 79: 12544-12553. 10.1128/JVI.79.19.12544-12553.2005PubMedPubMedCentralCrossRef
9.
go back to reference Devold M, Karlsen M, Nylund A: Sequence analysis of the fusion protein gene from infectious salmon anemia virus isolates: evidence of recombination and reassortment. J Gen Virol 2006, 87: 2031-2040. 10.1099/vir.0.81687-0PubMedCrossRef Devold M, Karlsen M, Nylund A: Sequence analysis of the fusion protein gene from infectious salmon anemia virus isolates: evidence of recombination and reassortment. J Gen Virol 2006, 87: 2031-2040. 10.1099/vir.0.81687-0PubMedCrossRef
10.
go back to reference Markussen T, Monceyron C, Numanovic S, Braaen S, Hjortaas M, Nilsen H, Mjaaland S: Evolutionary mechanisms involved in the virulence of infectious salmon anaemia virus (ISAV), a piscine orthomyxovirus. Virology 2008, 374: 515-527. 10.1016/j.virol.2008.01.019PubMedCrossRef Markussen T, Monceyron C, Numanovic S, Braaen S, Hjortaas M, Nilsen H, Mjaaland S: Evolutionary mechanisms involved in the virulence of infectious salmon anaemia virus (ISAV), a piscine orthomyxovirus. Virology 2008, 374: 515-527. 10.1016/j.virol.2008.01.019PubMedCrossRef
11.
go back to reference Cardenas C, Carmona M, Gallardo A, Labra A, Marshall SH: Coexistence in field samples of two variants of the infectious salmon anemia virus: a putative shift to pathogenicity. Plos One 2014, 9: e87832. 10.1371/journal.pone.0087832PubMedPubMedCentralCrossRef Cardenas C, Carmona M, Gallardo A, Labra A, Marshall SH: Coexistence in field samples of two variants of the infectious salmon anemia virus: a putative shift to pathogenicity. Plos One 2014, 9: e87832. 10.1371/journal.pone.0087832PubMedPubMedCentralCrossRef
12.
go back to reference Cunningham C, Gregory A, Black J, Simpson I, Raynard R: A novel variant of the infectious salmon anaemia virus (ISAV) haemagglutinin gene suggests mechanisms for virus diversity. Bull Eur Assoc Fish Pathol 2002, 22: 366-374. Cunningham C, Gregory A, Black J, Simpson I, Raynard R: A novel variant of the infectious salmon anaemia virus (ISAV) haemagglutinin gene suggests mechanisms for virus diversity. Bull Eur Assoc Fish Pathol 2002, 22: 366-374.
13.
go back to reference Mjaaland S, Hungnes O, Teig A, Dannevig BH, Thorud K, Rimstad E: Polymorphism in the infectious salmon anaemia virus haemagglutinin gene: importance and possible implications for evolution and ecology of infectious salmon anaemia disease. Virology 2002, 304: 379-391. 10.1006/viro.2002.1658PubMedCrossRef Mjaaland S, Hungnes O, Teig A, Dannevig BH, Thorud K, Rimstad E: Polymorphism in the infectious salmon anaemia virus haemagglutinin gene: importance and possible implications for evolution and ecology of infectious salmon anaemia disease. Virology 2002, 304: 379-391. 10.1006/viro.2002.1658PubMedCrossRef
14.
go back to reference Cook-Versloot M, Griffiths S, Cusack R, McGeachy S, Ritchie R: Identification and characterization of infectious salmon anemia virus (ISAV) hemagglutinin gene highly polymorphic region (HPR) type 0 in North America. Bull Eur Assoc Fish Path 2004, 24: 203-208. Cook-Versloot M, Griffiths S, Cusack R, McGeachy S, Ritchie R: Identification and characterization of infectious salmon anemia virus (ISAV) hemagglutinin gene highly polymorphic region (HPR) type 0 in North America. Bull Eur Assoc Fish Path 2004, 24: 203-208.
15.
go back to reference McBeath AJA, Bain N, Snow M: Surveillance for infectious salmon anaemia virus HPR0 in marine Atlantic salmon farms across Scotland. Dis Aquat Org 2009, 87: 161-169. 10.3354/dao02128PubMedCrossRef McBeath AJA, Bain N, Snow M: Surveillance for infectious salmon anaemia virus HPR0 in marine Atlantic salmon farms across Scotland. Dis Aquat Org 2009, 87: 161-169. 10.3354/dao02128PubMedCrossRef
16.
go back to reference Christiansen DH, Østergaard PS, Snow M, Dale OB, Falk K: 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 2011, 92: 909-918. 10.1099/vir.0.027094-0PubMedCrossRef Christiansen DH, Østergaard PS, Snow M, Dale OB, Falk K: 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 2011, 92: 909-918. 10.1099/vir.0.027094-0PubMedCrossRef
17.
go back to reference Lyngstad T, Hjortaas M, Kristoffersen A, Markussen T, Karlsen E, Jonassen C, Jansen P: Use of molecular epidemiology to trace transmission pathways for infectious salmon anaemia virus (ISAV) in Norwegian salmon farming. Epidemics 2011, 3: 1-11. 10.1016/j.epidem.2010.11.001PubMedCrossRef Lyngstad T, Hjortaas M, Kristoffersen A, Markussen T, Karlsen E, Jonassen C, Jansen P: Use of molecular epidemiology to trace transmission pathways for infectious salmon anaemia virus (ISAV) in Norwegian salmon farming. Epidemics 2011, 3: 1-11. 10.1016/j.epidem.2010.11.001PubMedCrossRef
18.
go back to reference Skall HF: Detection of HPR0 in Denmark and Criteria for Diagnosis of ISA. In Report on the 15th Annual Meeting of the National Reference Laboratories for Fish Diseases. DTU Vet - the National Veterinary Institute, Denmark, Copenhagen; 2011:48-49. Downloaded November 25, 2013 Skall HF: Detection of HPR0 in Denmark and Criteria for Diagnosis of ISA. In Report on the 15th Annual Meeting of the National Reference Laboratories for Fish Diseases. DTU Vet - the National Veterinary Institute, Denmark, Copenhagen; 2011:48-49. Downloaded November 25, 2013
19.
go back to reference Plarre H, Nylund A, Karlsen M, Brevik Ø, Sæther PA, Vike S: Evolution of infectious salmon anaemia virus (ISA virus). Arch Virol 2012, 157: 2309-2326. 10.1007/s00705-012-1438-0PubMedCrossRef Plarre H, Nylund A, Karlsen M, Brevik Ø, Sæther PA, Vike S: Evolution of infectious salmon anaemia virus (ISA virus). Arch Virol 2012, 157: 2309-2326. 10.1007/s00705-012-1438-0PubMedCrossRef
20.
go back to reference Godoy M, Kibenge M, Suarez R, Lazo E, Heisinger A, Aguinaga J, Bravo D, Mendoza J, Llegues K, Avendaño-Herrera R, Vera C, Mardones F, Kibenge F: Infectious salmon anaemia virus (ISAV) in Chilean Atlantic salmon (Salmo salar) aquaculture: emergence of low pathogenic ISAV-HPR0 and re-emergence of virulent ISAV-HPRΔ: HPR3 and HPR14. Virol J 2013, 10: 344. 10.1186/1743-422X-10-344PubMedPubMedCentralCrossRef Godoy M, Kibenge M, Suarez R, Lazo E, Heisinger A, Aguinaga J, Bravo D, Mendoza J, Llegues K, Avendaño-Herrera R, Vera C, Mardones F, Kibenge F: Infectious salmon anaemia virus (ISAV) in Chilean Atlantic salmon (Salmo salar) aquaculture: emergence of low pathogenic ISAV-HPR0 and re-emergence of virulent ISAV-HPRΔ: HPR3 and HPR14. Virol J 2013, 10: 344. 10.1186/1743-422X-10-344PubMedPubMedCentralCrossRef
21.
go back to reference EFSA Panel on Animal Health and Welfare (AHAW): Scientific Opinion on infectious salmon anaemia (ISA) EFSA Journal 2012, 10: 2971-2992. EFSA Panel on Animal Health and Welfare (AHAW): Scientific Opinion on infectious salmon anaemia (ISA) EFSA Journal 2012, 10: 2971-2992.
22.
go back to reference Vike S, Nylund S, Nylund A: ISA virus in Chile: evidence of vertical transmission. Arch Virol 2009, 154: 1-8. 10.1007/s00705-008-0251-2PubMedCrossRef Vike S, Nylund S, Nylund A: ISA virus in Chile: evidence of vertical transmission. Arch Virol 2009, 154: 1-8. 10.1007/s00705-008-0251-2PubMedCrossRef
23.
go back to reference Cottet L, Cortez-San Martin M, Tello M, Olivares E, Rivas-Aravena A, Vallejos E, Sandino AM, Spencer E: Bioinformatic analysis of the genome of infectious salmon anemia virus associated with outbreaks with high mortality in Chile. J Virol 2010, 84: 11916-11928. 10.1128/JVI.01202-10PubMedPubMedCentralCrossRef Cottet L, Cortez-San Martin M, Tello M, Olivares E, Rivas-Aravena A, Vallejos E, Sandino AM, Spencer E: Bioinformatic analysis of the genome of infectious salmon anemia virus associated with outbreaks with high mortality in Chile. J Virol 2010, 84: 11916-11928. 10.1128/JVI.01202-10PubMedPubMedCentralCrossRef
24.
go back to reference Devold M, Falk K, Dale OB, Krossøy B, Biering E, Aspehaug V, Nilsen F, Nylund A: Strain variation, based on the hemagglutinin gene, in Norwegian ISA virus isolates collected from 1987 to 2001: indications of recombination. Dis Aquat Org 2001, 47: 119-128. 10.3354/dao047119PubMedCrossRef Devold M, Falk K, Dale OB, Krossøy B, Biering E, Aspehaug V, Nilsen F, Nylund A: Strain variation, based on the hemagglutinin gene, in Norwegian ISA virus isolates collected from 1987 to 2001: indications of recombination. Dis Aquat Org 2001, 47: 119-128. 10.3354/dao047119PubMedCrossRef
25.
go back to reference Plarre H: Infectious salmon anaemia virus (ISAV): Evolution, genotyping, reservoirs and transmission. PhD Thesis, University of Bergen, Bergen, Norway; 2011. Downloaded November 27, 2014, from . http://www.uib.no/filearchive/phd-thesis-heidrun-plarre.pdf Plarre H: Infectious salmon anaemia virus (ISAV): Evolution, genotyping, reservoirs and transmission.PhD Thesis, University of Bergen, Bergen, Norway; 2011. Downloaded November 27, 2014, from . Plarre H: Infectious salmon anaemia virus (ISAV): Evolution, genotyping, reservoirs and transmission. PhD Thesis, University of Bergen, Bergen, Norway; 2011. Downloaded November 27, 2014, from . http://​www.​uib.​no/​filearchive/​phd-thesis-heidrun-plarre.​pdf Plarre H: Infectious salmon anaemia virus (ISAV): Evolution, genotyping, reservoirs and transmission.PhD Thesis, University of Bergen, Bergen, Norway; 2011. Downloaded November 27, 2014, from .
27.
go back to reference Munir K, Kibenge FSB: Detection of infectious salmon anaemia virus by real-time RT-PCR. J Virol Methods 2004, 117: 37-47. 10.1016/j.jviromet.2003.11.020PubMedCrossRef Munir K, Kibenge FSB: Detection of infectious salmon anaemia virus by real-time RT-PCR. J Virol Methods 2004, 117: 37-47. 10.1016/j.jviromet.2003.11.020PubMedCrossRef
28.
go back to reference Snow M, May P, McBeath AJA, Black J, Doig F, Kerr R, Cunningham CO, Nylund A, Devoid M: Development, application and validation of a Taqman* real-time RT-PCR assay for the detection of infectious salmon anaemia virus (ISAV) in Atlantic salmon (salmo salar). Dev Biol Standardization 2006, 126: 133-145. Snow M, May P, McBeath AJA, Black J, Doig F, Kerr R, Cunningham CO, Nylund A, Devoid M: Development, application and validation of a Taqman* real-time RT-PCR assay for the detection of infectious salmon anaemia virus (ISAV) in Atlantic salmon (salmo salar). Dev Biol Standardization 2006, 126: 133-145.
29.
go back to reference Saitou N, Nei M: The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987, 4: 406-425.PubMed Saitou N, Nei M: The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987, 4: 406-425.PubMed
Metadata
Title
Genetic analysis and comparative virulence of infectious salmon anemia virus (ISAV) types HPR7a and HPR7b from recent field outbreaks in Chile
Authors
Marcos G Godoy
Rudy Suarez
Eduardo S Lazo
Katerina O Llegues
Molly JT Kibenge
Yingwei Wang
Frederick SB Kibenge
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2014
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-014-0204-1

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