Natural infection of Atlantic salmon (Salmo salar L.) with salmonid alphavirus 3 generates numerous viral deletion mutants

Petterson, Elin; Stormoen, Marit; Evensen, Øystein; Mikalsen, Aase B.; Haugland, Øyvind

doi:10.1099/vir.0.052563-0

Cited by 30 publications

(39 citation statements)

References 46 publications

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“…Virus cultivation was unsuccessful, similar to earlier experiences with primary culture of SAV from infected fish (Christie et al 1998, López-Dóriga et al 2001, Graham et al 2003, Petterson et al 2013. Possible causes as low viral loads, virus neutralizing antibodies and/or defective virus particles in the samples have been suggested (Graham et al 2010, Petterson et al 2013. Challenges associated with primary isolation of SAV are also in accordance with our unpublished data from attempts to cultivate the virus from several outbreaks of PD in Norway.…”

supporting

confidence: 79%

“…Cohorts exposed to lower sea temperatures had significantly longer incubation periods than cohorts infected when the sea temperatures were higher (Stene et al 2014). Virus cultivation was unsuccessful, similar to earlier experiences with primary culture of SAV from infected fish (Christie et al 1998, López-Dóriga et al 2001, Graham et al 2003, Petterson et al 2013. Possible causes as low viral loads, virus neutralizing antibodies and/or defective virus particles in the samples have been suggested (Graham et al 2010, Petterson et al 2013.…”

Section: Discussionsupporting

confidence: 55%

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First outbreak of sleeping disease in Switzerland: disease signs and virus characterization

Schmidt‐Posthaus¹,

Diserens²,

Hjortaas³

et al. 2014

Dis. Aquat. Org.

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Sleeping disease is a contagious disease mainly of freshwater farmed rainbow trout, caused by salmonid alphavirus (SAV) Subtype 2. Here we describe the first case in Switzerland. Pathological changes ranged from acute pancreas necrosis to more chronic lesions with complete loss of exocrine pancreas and simultaneous degenerative, inflammatory and regenerative heart and muscle lesions. The partial sequencing of SAV E2 and nsp3 genes placed the Swiss SAV variant within the Subtype 2 clustering together with freshwater isolates from UK and continental Europe. Although mortality stayed low, growth rates were significantly reduced, making the disease economically relevant.KEY WORDS: Sleeping disease · Salmonid alphavirus · SAV · Subtype 2 · Pathology · Trout · Phylogenetic analysis Resale or republication not permitted without written consent of the publisherDis Aquat Org 111: [165][166][167][168][169][170][171] 2014 The most characteristic sign of the disease is the unusual behaviour of the fish, which stay on their side at the bottom of the tank. Histological examinations of SD-affected fish reveal a chronological appearance of lesions ). Initially, necrosis of exocrine pancreas appears shortly before degeneration of heart muscle fibres. Later, skeletal muscle degeneration, necrosis and inflammation develop. The red muscle damage is particularly severe in the late stage of the disease and is probably responsible for the clinical signs of disease (Boucher et al. 1995, Boucher & Baudin-Laurencin 1996, Kerbart Boscher et al. 2006).Here we report the first case of SD in Switzerland. Clinical and pathological signs are reported. The molecular characterization of the virus is shown, including the relationship with SAV from fish farms in other European countries. MATERIALS AND METHODSIn June 2013, a fish farmer reported rainbow trout lying on their side at the bottom of the tank. The fish originated from imported eggs from a fish farm in Denmark (free of notifiable diseases and sleeping disease). At a weight of about 15 g, fish were moved to a part recirculation system with 90% spring water and 10% creek water. After about 3 wk, the signs mentioned above became obvious. A sample of 10 rainbow trout was sent alive to the Centre for Fish and Wildlife Health for pathological investigation. Time schedule of disease signs and sampling is shown in Fig. 1. Fish were euthanized in buffered 3-aminobenzoic acid ethyl ester (MS-222 ® , Argent Chemical Laboratories). Each trout was measured, followed immediately by a standard necropsy. Fish were examined for changes in external and internal organs. For parasitological examination, a skin scraping, a gill sample and the intestinal content were investigated by light microscopy. On 3 animals a bacteriological examination of liver, spleen and kidney was performed using blood agar plates (Bio Merieux) and bromothymol blue-lactose-agar plates. To examine for Flavobacteria, samples of gill and spleen were cultivated on specific agar plates (Anacker & Ordal 1959). For virological...

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supporting

confidence: 79%

Section: Discussionsupporting

confidence: 55%

First outbreak of sleeping disease in Switzerland: disease signs and virus characterization

Schmidt‐Posthaus¹,

Diserens²,

Hjortaas³

et al. 2014

Dis. Aquat. Org.

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“…In a previous study on the SAV3 subtype of SPDV, we documented that infectious virus (with full-length genome) is present alongside with numerous RNA deletion mutants in heart of clinically diseased Atlantic salmon, and we hypothesised that recombination of genomes was the explanation for this17. Using reverse genetics, we have shown that infectious virus can be rescued from cell lines transfected with full length SAV3 (FL-SAV3) plasmid18.…”

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confidence: 95%

Experimental piscine alphavirus RNA recombination in vivo yields both viable virus and defective viral RNA

Petterson

Guo

Evensen

et al. 2016

Sci Rep

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RNA recombination in non-segmented RNA viruses is important for viral evolution and documented for several virus species through in vitro studies. Here we confirm viral RNA recombination in vivo using an alphavirus, the SAV3 subtype of Salmon pancreas disease virus. The virus causes pancreas disease in Atlantic salmon and heavy losses in European salmonid aquaculture. Atlantic salmon were injected with a SAV3 6K-gene deleted cDNA plasmid, encoding a non-viable variant of SAV3, together with a helper cDNA plasmid encoding structural proteins and 6K only. Later, SAV3-specific RNA was detected and recombination of viral RNA was confirmed. Virus was grown from plasmid-injected fish and shown to infect and cause pathology in salmon. Subsequent cloning of PCR products confirming recombination, documented imprecise homologous recombination creating RNA deletion variants in fish injected with cDNA plasmid, corresponding with deletion variants previously found in SAV3 from the field. This is the first experimental documentation of alphavirus RNA recombination in an animal model and provides new insight into the production of defective virus RNA.

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“…pancreas disease (PD), heart and skeletal muscle inflammation (HSMI) and cardiomyopathy syndrome (CMS). Viral cause of the diseases, the salmonid alphavirus 3 (SAV3), piscine reovirus (PRV) and piscine myocarditis virus (PMCV), respectively, have been presented [20]–[23], but none of them have shown to be easy to cultivate in cell culture except for a few isolates of SAV3 causing PD [24], [25]. In an attempt to isolate a viral agent from heart samples from farmed Atlantic salmon with HSMI, we obtained a virus isolate not previously found in Atlantic salmon.…”

Section: Introductionmentioning

confidence: 99%

Characterization of a Novel Calicivirus Causing Systemic Infection in Atlantic Salmon (Salmo salar L.): Proposal for a New Genus of Caliciviridae

et al. 2014

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The Caliciviridae is a family of viruses infecting humans, a wide range of animals, birds and marine fish and mammals, resulting in a wide spectrum of diseases. We describe the identification and genetic characterization of a novel calicivirus replicating in Atlantic salmon. The virus has a high prevalence in farmed salmon and is found in fish suffering from several diseases and conditions and also in presumable healthy fish. A challenge and vaccination trial shows that the calicivirus replicates in Atlantic salmon and establishes a systemic infection, which can be reduced by vaccination with formalin-inactivated virus preparation. The virus, named Atlantic salmon calicivirus (ASCV), is found in two genetically distinct variants, a cell culture isolated and a variant sequenced directly from field material. The genomes are 7,4 kb and contain two open reading frames where typical conserved amino acid motifs and domains predict a gene order reminiscent of calicivirus genomes. Phylogenetic analysis performed on extracted capsid amino acid sequences segregated the two ASCV variants in a unique cluster sharing root with the branch of noroviruses infecting humans and the unassigned Tulane virus and St-Valérien like viruses, infecting rhesus monkey and pig, respectively, with relatively large distance to the marine calicivirus subgroup of vesiviruses. Based on the analyses presented, the ASCV is predicted to represent a new genus of Caliciviridae for which we propose the name Salovirus.

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Natural infection of Atlantic salmon (Salmo salar L.) with salmonid alphavirus 3 generates numerous viral deletion mutants

Cited by 30 publications

References 46 publications

First outbreak of sleeping disease in Switzerland: disease signs and virus characterization

First outbreak of sleeping disease in Switzerland: disease signs and virus characterization

Experimental piscine alphavirus RNA recombination in vivo yields both viable virus and defective viral RNA

Characterization of a Novel Calicivirus Causing Systemic Infection in Atlantic Salmon (Salmo salar L.): Proposal for a New Genus of Caliciviridae

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