The Viral Hemorrhagic Septicemia Virus (VHSV) Markers of Virulence in Rainbow Trout (Oncorhynchus mykiss)

Viral hemorrhagic septicemia virus (VHSV) is a highly contagious virus leading to high mortality in a large panel of freshwater and marine fish species. VHSV isolates originating from marine fish show low pathogenicity in rainbow trout. The analysis of several nearly complete genome sequences from m...

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Main Authors: Laury Baillon, Emilie Mérour, Joëlle Cabon, Lénaïg Louboutin, Estelle Vigouroux, Anna Luiza Farias Alencar, Argelia Cuenca, Yannick Blanchard, Niels Jørgen Olesen, Valentina Panzarin, Thierry Morin, Michel Brémont, Stéphane Biacchesi
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-10-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2020.574231/full
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author Laury Baillon
Emilie Mérour
Joëlle Cabon
Lénaïg Louboutin
Estelle Vigouroux
Anna Luiza Farias Alencar
Argelia Cuenca
Yannick Blanchard
Niels Jørgen Olesen
Valentina Panzarin
Thierry Morin
Michel Brémont
Stéphane Biacchesi
author_facet Laury Baillon
Emilie Mérour
Joëlle Cabon
Lénaïg Louboutin
Estelle Vigouroux
Anna Luiza Farias Alencar
Argelia Cuenca
Yannick Blanchard
Niels Jørgen Olesen
Valentina Panzarin
Thierry Morin
Michel Brémont
Stéphane Biacchesi
author_sort Laury Baillon
collection DOAJ
description Viral hemorrhagic septicemia virus (VHSV) is a highly contagious virus leading to high mortality in a large panel of freshwater and marine fish species. VHSV isolates originating from marine fish show low pathogenicity in rainbow trout. The analysis of several nearly complete genome sequences from marine and freshwater isolates displaying varying levels of virulence in rainbow trout suggested that only a limited number of amino acid residues might be involved in regulating the level of virulence. Based on a recent analysis of 55 VHSV strains, which were entirely sequenced and phenotyped in vivo in rainbow trout, several amino acid changes putatively involved in virulence were identified. In the present study, these amino acid changes were introduced, alone or in combination, in a highly-virulent VHSV 23–75 genome backbone by reverse genetics. A total of 35 recombinant VHSV variants were recovered and characterized for virulence in trout by bath immersion. Results confirmed the important role of the NV protein (R116S) and highlighted a major contribution of the nucleoprotein N (K46G and A241E) in regulating virulence. Single amino acid changes in these two proteins drastically affect virus pathogenicity in rainbow trout. This is particularly intriguing for the N variant (K46G) which is unable to establish an active infection in the fins of infected trout, the main portal of entry of VHSV in this species, allowing further spread in its host. In addition, salmonid cell lines were selected to assess the kinetics of replication and cytopathic effect of recombinant VHSV and discriminate virulent and avirulent variants. In conclusion, three major virulence markers were identified in the NV and N proteins. These markers explain almost all phenotypes (92.7%) observed in trout for the 55 VHSV strains analyzed in the present study and herein used for the backward validation of virulence markers. The identification of VHSV specific virulence markers in this species is of importance both to predict the in vivo phenotype of viral isolates with targeted diagnostic tests and to improve prophylactic methods such as the development of safer live-attenuated vaccines.
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spelling doaj.art-7a231b1a7b204507b5a937a0bbf0bab32022-12-21T18:56:01ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-10-011110.3389/fmicb.2020.574231574231The Viral Hemorrhagic Septicemia Virus (VHSV) Markers of Virulence in Rainbow Trout (Oncorhynchus mykiss)Laury Baillon0Emilie Mérour1Joëlle Cabon2Lénaïg Louboutin3Estelle Vigouroux4Anna Luiza Farias Alencar5Argelia Cuenca6Yannick Blanchard7Niels Jørgen Olesen8Valentina Panzarin9Thierry Morin10Michel Brémont11Stéphane Biacchesi12Virologie et Immunologie Moléculaires (VIM), Université Paris-Saclay, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Université de Versailles Saint-Quentin-en-Yvelines, Jouy-en-Josas, FranceVirologie et Immunologie Moléculaires (VIM), Université Paris-Saclay, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Université de Versailles Saint-Quentin-en-Yvelines, Jouy-en-Josas, FranceANSES, Laboratoire de Ploufragan-Plouzané-Niort, Unité Pathologies Virales des Poissons, Plouzané, FranceANSES, Laboratoire de Ploufragan-Plouzané-Niort, Unité Pathologies Virales des Poissons, Plouzané, FranceANSES, Laboratoire de Ploufragan-Plouzané-Niort, Unité Pathologies Virales des Poissons, Plouzané, FranceUnit for Fish and Shellfish Diseases, EURL for Fish and Crustacean Diseases, National Institute of Aquatic Resources, Technical University of Denmark (DTU), Kongens Lyngby, DenmarkUnit for Fish and Shellfish Diseases, EURL for Fish and Crustacean Diseases, National Institute of Aquatic Resources, Technical University of Denmark (DTU), Kongens Lyngby, DenmarkANSES, Laboratoire de Ploufragan-Plouzané-Niort, Unité Génétique Virale et Biosécurité, Ploufragan, FranceUnit for Fish and Shellfish Diseases, EURL for Fish and Crustacean Diseases, National Institute of Aquatic Resources, Technical University of Denmark (DTU), Kongens Lyngby, DenmarkDivision of Comparative Biomedical Sciences, Istituto Zooprofilattico Sperimentale delle Venezie (IZSVe), Padua, ItalyANSES, Laboratoire de Ploufragan-Plouzané-Niort, Unité Pathologies Virales des Poissons, Plouzané, FranceVirologie et Immunologie Moléculaires (VIM), Université Paris-Saclay, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Université de Versailles Saint-Quentin-en-Yvelines, Jouy-en-Josas, FranceVirologie et Immunologie Moléculaires (VIM), Université Paris-Saclay, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Université de Versailles Saint-Quentin-en-Yvelines, Jouy-en-Josas, FranceViral hemorrhagic septicemia virus (VHSV) is a highly contagious virus leading to high mortality in a large panel of freshwater and marine fish species. VHSV isolates originating from marine fish show low pathogenicity in rainbow trout. The analysis of several nearly complete genome sequences from marine and freshwater isolates displaying varying levels of virulence in rainbow trout suggested that only a limited number of amino acid residues might be involved in regulating the level of virulence. Based on a recent analysis of 55 VHSV strains, which were entirely sequenced and phenotyped in vivo in rainbow trout, several amino acid changes putatively involved in virulence were identified. In the present study, these amino acid changes were introduced, alone or in combination, in a highly-virulent VHSV 23–75 genome backbone by reverse genetics. A total of 35 recombinant VHSV variants were recovered and characterized for virulence in trout by bath immersion. Results confirmed the important role of the NV protein (R116S) and highlighted a major contribution of the nucleoprotein N (K46G and A241E) in regulating virulence. Single amino acid changes in these two proteins drastically affect virus pathogenicity in rainbow trout. This is particularly intriguing for the N variant (K46G) which is unable to establish an active infection in the fins of infected trout, the main portal of entry of VHSV in this species, allowing further spread in its host. In addition, salmonid cell lines were selected to assess the kinetics of replication and cytopathic effect of recombinant VHSV and discriminate virulent and avirulent variants. In conclusion, three major virulence markers were identified in the NV and N proteins. These markers explain almost all phenotypes (92.7%) observed in trout for the 55 VHSV strains analyzed in the present study and herein used for the backward validation of virulence markers. The identification of VHSV specific virulence markers in this species is of importance both to predict the in vivo phenotype of viral isolates with targeted diagnostic tests and to improve prophylactic methods such as the development of safer live-attenuated vaccines.https://www.frontiersin.org/articles/10.3389/fmicb.2020.574231/fullnovirhabdovirusviral hemorrhagic septicemia virusVHSVrainbow troutvirulence markers
spellingShingle Laury Baillon
Emilie Mérour
Joëlle Cabon
Lénaïg Louboutin
Estelle Vigouroux
Anna Luiza Farias Alencar
Argelia Cuenca
Yannick Blanchard
Niels Jørgen Olesen
Valentina Panzarin
Thierry Morin
Michel Brémont
Stéphane Biacchesi
The Viral Hemorrhagic Septicemia Virus (VHSV) Markers of Virulence in Rainbow Trout (Oncorhynchus mykiss)
Frontiers in Microbiology
novirhabdovirus
viral hemorrhagic septicemia virus
VHSV
rainbow trout
virulence markers
title The Viral Hemorrhagic Septicemia Virus (VHSV) Markers of Virulence in Rainbow Trout (Oncorhynchus mykiss)
title_full The Viral Hemorrhagic Septicemia Virus (VHSV) Markers of Virulence in Rainbow Trout (Oncorhynchus mykiss)
title_fullStr The Viral Hemorrhagic Septicemia Virus (VHSV) Markers of Virulence in Rainbow Trout (Oncorhynchus mykiss)
title_full_unstemmed The Viral Hemorrhagic Septicemia Virus (VHSV) Markers of Virulence in Rainbow Trout (Oncorhynchus mykiss)
title_short The Viral Hemorrhagic Septicemia Virus (VHSV) Markers of Virulence in Rainbow Trout (Oncorhynchus mykiss)
title_sort viral hemorrhagic septicemia virus vhsv markers of virulence in rainbow trout oncorhynchus mykiss
topic novirhabdovirus
viral hemorrhagic septicemia virus
VHSV
rainbow trout
virulence markers
url https://www.frontiersin.org/articles/10.3389/fmicb.2020.574231/full
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