Viruses Affecting Salmonids

A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Animal Viruses".

Deadline for manuscript submissions: closed (31 March 2022) | Viewed by 21062

Special Issue Editors


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Guest Editor
Norwegain Veterinary Institute, N-0106 Oslo, Norway
Interests: host–pathogen interactions; sustainable growth of the aquaculture industry; viral diseases; infection kinetics; transmission and immune responses; virological and bacteriological vaccine products

E-Mail Website
Guest Editor
Faculty of Veterinary Medicine, Norwegian University of Life Sciences, 0454 Oslo, Norway
Interests: detection and characterization of fish viruses; viral infections affecting fish heart, Atlantic salmon; host–pathogen interactions; vaccine development

Special Issue Information

Dear Colleagues,

Salmonids are among the three most important fish species in aquaculture worldwide. Viruses causing welfare and health issues in salmonids are among the top listed diseases in the global aquaculture industry, leading to heavy losses. Although some viruses have been well known and described for decades, stories of successful eradication of viruses affecting salmonids are scarce.

In this Special Issue, we aim for peer-reviewed reports, perspectives, reviews, and research articles on recent advances in salmonid virology to increase our knowledge on the identification and discovery of emerging viruses affecting salmonids. Further, our aim is to increase our understanding of individual viruses and virus interplay during co-infections. Studies on factors affecting virulence and how varying virulence manifests as pathology and on the host response is of specific interest, as are also studies on therapeutic and preventative approaches to reduce the accommodating welfare and health issues and heavy losses for the industry. Viral diseases in aquaculture might have an environmental impact either through transmission to wild fish or influence the ecosystem as a whole, impairing further growth of the industry, and thus, we also seek study topics shedding light on this area.

Dr. Sonal Patel
Dr. Aase B Mikalsen
Guest Editors

Manuscript Submission Information

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Keywords

  • Aquaculture
  • Wild fish species
  • Reservoir
  • Transmission
  • Epidemiology
  • Evolution
  • Virulence
  • Pathology
  • Vaccines
  • Host–pathogen interaction

Published Papers (7 papers)

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Research

22 pages, 3422 KiB  
Article
Infectious Salmon Anemia Virus Infectivity Is Determined by Multiple Segments with an Important Contribution from Segment 5
by Matías Cárdenas, Sofía Michelson, Daniel R. Pérez, Margarita Montoya, Jorge Toledo, Yesseny Vásquez-Martínez and Marcelo Cortez-San Martin
Viruses 2022, 14(3), 631; https://0-doi-org.brum.beds.ac.uk/10.3390/v14030631 - 18 Mar 2022
Cited by 3 | Viewed by 2585
Abstract
Infectious salmon anemia virus (ISAV) is the etiological agent of infectious salmon anemia. It belongs to the genus isavirus, one of the genera of the Orthomyxoviridae family, as does Influenzavirus A. The ISAV genome comprises eight negative-sense single-stranded RNA segments that code for [...] Read more.
Infectious salmon anemia virus (ISAV) is the etiological agent of infectious salmon anemia. It belongs to the genus isavirus, one of the genera of the Orthomyxoviridae family, as does Influenzavirus A. The ISAV genome comprises eight negative-sense single-stranded RNA segments that code for at least 10 proteins. Although some ISAV strains can reach 100% mortality rates, the factors that determine isavirus infectivity remain unknown. However, some studies suggest that segments 5 and 6 are responsible for the different degrees of virulence and infectivity among ISAV subtypes, unlike the influenza A virus, where most segments are involved in the virus infectivity. In this work, synthetic reassortant viruses for the eight segments of ISAV were generated by reverse genetics, combining a highly virulent virus, ISAV 752_09 (HPR7b), and an avirulent strain, SK779/06 (HPR0). We characterized the rescued viruses and their capacity to replicate and infect different cell lines, produce plaques in ASK cells, and their ability to induce and modulate the cellular immune response in vitro. Our results show that the majority of ISAV segments are involved in at least one of the analyzed characteristics, segment 5 being one of the most important, allowing HPR0 viruses, among other things, to produce plaques and replicate in CHSE-214 cells. We determined that segments 5 and 6 participate in different stages of the viral cycle, and their compatibility is critical for viral infection. Additionally, we demonstrated that segment 2 can modulate the cellular immune response. Our results indicate a high degree of genetic compatibility between the genomic segments of HPR7b and HPR0, representing a latent risk of reassortant that would give rise to a new virus with an unknown phenotype. Full article
(This article belongs to the Special Issue Viruses Affecting Salmonids)
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19 pages, 2052 KiB  
Article
Salmon Erythrocytes Sequester Active Virus Particles in Infectious Salmon Anaemia
by Johanna Hol Fosse, Maria Aamelfot, Tonje Sønstevold, Simon Chioma Weli, Niccolò Vendramin, Petra Elisabeth Petersen, Anita Solhaug, Marit Måsøy Amundsen, Inger Austrheim Heffernan, Argelia Cuenca, Debes Hammershaimb Christiansen and Knut Falk
Viruses 2022, 14(2), 310; https://0-doi-org.brum.beds.ac.uk/10.3390/v14020310 - 02 Feb 2022
Cited by 6 | Viewed by 2802
Abstract
Infectious salmon anaemia virus (ISAV) binds circulating Atlantic salmon erythrocytes, but the relevance of this interaction for the course of infection and development of disease remains unclear. We here characterise ISAV-erythrocyte interactions in experimentally infected Atlantic salmon and show that ISAV-binding to erythrocytes [...] Read more.
Infectious salmon anaemia virus (ISAV) binds circulating Atlantic salmon erythrocytes, but the relevance of this interaction for the course of infection and development of disease remains unclear. We here characterise ISAV-erythrocyte interactions in experimentally infected Atlantic salmon and show that ISAV-binding to erythrocytes is common and precedes the development of disease. Viral RNA and infective particles were enriched in the cellular fraction of blood. While erythrocyte-associated ISAV remained infectious, erythrocytes dose-dependently limited the infection of cultured cells. Surprisingly, immunostaining of blood smears revealed expression of ISAV proteins in a small fraction of erythrocytes in one of the examined trials, confirming that ISAV can be internalised in this cell type and engage the cellular machinery in transcription and translation. However, viral protein expression in erythrocytes was rare and not required for development of disease and mortality. Furthermore, active transcription of ISAV mRNA was higher in tissues than in blood, supporting the assumption that ISAV replication predominantly takes place in endothelial cells. In conclusion, Atlantic salmon erythrocytes bind ISAV and sequester infective virus particles during infection, but do not appear to significantly contribute to ISAV replication. We discuss the implications of our findings for infection dynamics and pathogenesis of infectious salmon anaemia. Full article
(This article belongs to the Special Issue Viruses Affecting Salmonids)
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14 pages, 1216 KiB  
Article
Differential Transcriptomic Response of Rainbow Trout to Infection with Two Strains of IPNV
by David Tapia, Juan Kuznar, Rodolfo Farlora and José M. Yáñez
Viruses 2022, 14(1), 21; https://0-doi-org.brum.beds.ac.uk/10.3390/v14010021 - 23 Dec 2021
Cited by 6 | Viewed by 3135
Abstract
The IPN virus (IPNV) causes a highly contagious disease that affects farmed salmonids. IPNV isolates have been phylogenetically classified into seven genogroups, of which two are present in Chile, genogroups 1 and 5. This study aimed to compare the transcriptomic response of rainbow [...] Read more.
The IPN virus (IPNV) causes a highly contagious disease that affects farmed salmonids. IPNV isolates have been phylogenetically classified into seven genogroups, of which two are present in Chile, genogroups 1 and 5. This study aimed to compare the transcriptomic response of rainbow trout fry challenged with two Chilean isolates of IPNV, RTTX (genogroup 1), and ALKA (genogroup 5). Tissue samples from challenged individuals and controls were taken at 1, 7, and 20 days post-challenge and analyzed by RNA-Seq. The results revealed that infection with RTTX elicited a greater modulation of the trout transcriptome compared to ALKA infection, generating a greater number of highly differentially expressed genes in relation to the control fish. Gene Ontology enrichment indicated that functions related to the inflammatory and immune responses were modulated in fish challenged with both isolates throughout the trial, but with different regulation patterns. On day 1 post challenge, these functions were activated in those challenged with ALKA, but suppressed in RTTX-challenged fish. These results suggest that rainbow trout exhibit a differential transcriptomic response to infection with the two genetically distinct IPNV isolates, especially at early times post-infection. Full article
(This article belongs to the Special Issue Viruses Affecting Salmonids)
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16 pages, 3016 KiB  
Article
Genomic Epidemiology of Salmonid Alphavirus in Norwegian Aquaculture Reveals Recent Subtype-2 Transmission Dynamics and Novel Subtype-3 Lineages
by Daniel J. Macqueen, Oliver Eve, Manu Kumar Gundappa, Rose Ruiz Daniels, Michael D. Gallagher, Svein Alexandersen and Marius Karlsen
Viruses 2021, 13(12), 2549; https://0-doi-org.brum.beds.ac.uk/10.3390/v13122549 - 20 Dec 2021
Cited by 2 | Viewed by 3243
Abstract
Viral disease poses a major barrier to sustainable aquaculture, with outbreaks causing large economic losses and growing concerns for fish welfare. Genomic epidemiology can support disease control by providing rapid inferences on viral evolution and disease transmission. In this study, genomic epidemiology was [...] Read more.
Viral disease poses a major barrier to sustainable aquaculture, with outbreaks causing large economic losses and growing concerns for fish welfare. Genomic epidemiology can support disease control by providing rapid inferences on viral evolution and disease transmission. In this study, genomic epidemiology was used to investigate salmonid alphavirus (SAV), the causative agent of pancreas disease (PD) in Atlantic salmon. Our aim was to reconstruct SAV subtype-2 (SAV2) diversity and transmission dynamics in recent Norwegian aquaculture, including the origin of SAV2 in regions where this subtype is not tolerated under current legislation. Using nanopore sequencing, we captured ~90% of the SAV2 genome for n = 68 field isolates from 10 aquaculture production regions sampled between 2018 and 2020. Using time-calibrated phylogenetics, we infer that, following its introduction to Norway around 2010, SAV2 split into two clades (SAV2a and 2b) around 2013. While co-present at the same sites near the boundary of Møre og Romsdal and Trøndelag, SAV2a and 2b were generally detected in non-overlapping locations at more Southern and Northern latitudes, respectively. We provide evidence for recent SAV2 transmission over large distances, revealing a strong connection between Møre og Romsdal and SAV2 detected in 2019/20 in Rogaland. We also demonstrate separate introductions of SAV2a and 2b outside the SAV2 zone in Sognefjorden (Vestland), connected to samples from Møre og Romsdal and Trøndelag, respectively, and a likely 100 km Northward transmission of SAV2b within Trøndelag. Finally, we recovered genomes of SAV2a and SAV3 co-infecting single fish in Rogaland, involving novel SAV3 lineages that diverged from previously characterized strains >25 years ago. Overall, this study demonstrates useful applications of genomic epidemiology for tracking viral disease spread in aquaculture. Full article
(This article belongs to the Special Issue Viruses Affecting Salmonids)
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19 pages, 4660 KiB  
Article
No Evidence of the Vertical Transmission of Non-Virulent Infectious Salmon Anaemia Virus (ISAV-HPR0) in Farmed Atlantic Salmon
by Debes Hammershaimb Christiansen, Petra Elisabeth Petersen, Maria Marjunardóttir Dahl, Nicolina Vest, Maria Aamelfot, Anja Bråthen Kristoffersen, Mona Dverdal Jansen, Iveta Matejusova, Michael D. Gallagher, Gísli Jónsson, Eduardo Rodriguez, Johanna Hol Fosse and Knut Falk
Viruses 2021, 13(12), 2428; https://0-doi-org.brum.beds.ac.uk/10.3390/v13122428 - 03 Dec 2021
Cited by 3 | Viewed by 2902
Abstract
The nonvirulent infectious salmon anaemia virus (ISAV-HPR0) is the putative progenitor for virulent-ISAV, and a potential risk factor for the development of infectious salmon anaemia (ISA). Understanding the transmission dynamics of ISAV-HPR0 is fundamental to proper management and mitigation strategies. Here, we demonstrate [...] Read more.
The nonvirulent infectious salmon anaemia virus (ISAV-HPR0) is the putative progenitor for virulent-ISAV, and a potential risk factor for the development of infectious salmon anaemia (ISA). Understanding the transmission dynamics of ISAV-HPR0 is fundamental to proper management and mitigation strategies. Here, we demonstrate that ISAV-HPR0 causes prevalent and transient infections in all three production stages of Atlantic salmon in the Faroe Islands. Phylogenetic analysis of the haemagglutinin-esterase gene from 247 salmon showed a clear geographical structuring into two significantly distinct HPR0-subgroups, which were designated G2 and G4. Whereas G2 and G4 co-circulated in marine farms, Faroese broodfish were predominantly infected by G2, and smolt were predominantly infected by G4. This infection pattern was confirmed by our G2- and G4-specific RT-qPCR assays. Moreover, the HPR0 variants detected in Icelandic and Norwegian broodfish were never detected in the Faroe Islands, despite the extensive import of ova from both countries. Accordingly, the vertical transmission of HPR0 from broodfish to progeny is uncommon. Phylogenetic and statistical analysis suggest that HPR0 persists in the smolt farms as “house-strains”, and that new HPR0 variants are occasionally introduced from the marine environment, probably by HPR0-contaminated sea-spray. Thus, high biosecurity—including water and air intake—is required to avoid the introduction of pathogens to the smolt farms. Full article
(This article belongs to the Special Issue Viruses Affecting Salmonids)
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15 pages, 2973 KiB  
Article
Infectious Salmon Anemia Virus Shedding from Infected Atlantic Salmon (Salmo salar L.)—Application of a Droplet Digital PCR Assay for Virus Quantification in Seawater
by Simon Chioma Weli, Lisa-Victoria Bernhardt, Lars Qviller, Ole Bendik Dale and Atle Lillehaug
Viruses 2021, 13(9), 1770; https://0-doi-org.brum.beds.ac.uk/10.3390/v13091770 - 04 Sep 2021
Cited by 4 | Viewed by 2798
Abstract
Infectious salmon anemia virus (ISAV) infection is currently detected by fish sampling for PCR and immunohistochemistry analysis. As an alternative to sampling fish, we evaluated two different membrane filters in combination with four buffers for elution, concentration, and detection of ISAV in seawater, [...] Read more.
Infectious salmon anemia virus (ISAV) infection is currently detected by fish sampling for PCR and immunohistochemistry analysis. As an alternative to sampling fish, we evaluated two different membrane filters in combination with four buffers for elution, concentration, and detection of ISAV in seawater, during a bath challenge of Atlantic salmon (Salmo salar L.) post-smolts with high and low concentrations of ISAV. Transmission of ISAV in the bath challenge was confirmed by a high mortality, clinical signs associated with ISA disease, and detection of ISAV RNA in organ tissues and seawater samples. The electronegatively charged filter, combined with lysis buffer, gave significantly higher ISAV RNA detection by droplet digital PCR from seawater (5.6 × 104 ISAV RNA copies/L; p < 0.001). Viral shedding in seawater was first detected at two days post-challenge and peaked on day 11 post-challenge, one day before mortalities started in fish challenged with high dose ISAV, demonstrating that a large viral shedding event occurs before death. These data provide important information for ISAV shedding that is relevant for the development of improved surveillance tools based on water samples, transmission models, and management of ISA. Full article
(This article belongs to the Special Issue Viruses Affecting Salmonids)
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16 pages, 2855 KiB  
Article
Emergence of Salmonid Alphavirus Genotype 2 in Norway—Molecular Characterization of Viral Strains Circulating in Norway and Scotland
by Monika J. Hjortaas, Elena Fringuelli, Adérito L. Monjane, Aase B. Mikalsen, Christine M. Jonassen, Paul Savage and Hilde Sindre
Viruses 2021, 13(8), 1556; https://0-doi-org.brum.beds.ac.uk/10.3390/v13081556 - 06 Aug 2021
Cited by 4 | Viewed by 2136
Abstract
Pancreas disease (PD) and sleeping disease (SD), caused by an alphavirus, are endemic in European salmonid aquaculture, causing significant mortality, reduced growth and poor flesh quality. In 2010, a new variant of salmonid alphavirus emerged in Norway, marine salmonid alphavirus genotype 2 (SAV2). [...] Read more.
Pancreas disease (PD) and sleeping disease (SD), caused by an alphavirus, are endemic in European salmonid aquaculture, causing significant mortality, reduced growth and poor flesh quality. In 2010, a new variant of salmonid alphavirus emerged in Norway, marine salmonid alphavirus genotype 2 (SAV2). As this genotype is highly prevalent in Scotland, transmission through well boat traffic was hypothesized as one possible source of infection. In this study, we performed full-length genome sequencing of SAV2 sampled between 2006 and 2012 in Norway and Scotland, and present the first comprehensive full-length characterization of Norwegian marine SAV2 strains. We analyze their relationship with selected Scottish SAV2 strains and explore the genetic diversity of SAV. Our results show that all Norwegian marine SAV2 share a recent last common ancestor with marine SAV2 circulating in Scotland and a higher level of genomic diversity among the Scottish marine SAV2 strains compared to strains from Norway. These findings support the hypothesis of a single introduction of SAV2 to Norway sometime from 2006–2010, followed by horizontal spread along the coast. Full article
(This article belongs to the Special Issue Viruses Affecting Salmonids)
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