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De novo assembly of Sockeye salmon kidney transcriptomes reveal a limited early response to piscine reovirus with or without infectious hematopoietic necrosis virus superinfection.

ABSTRACT: Piscine reovirus (PRV) has been associated with the serious disease known as Heart and Skeletal Muscle Inflammation (HSMI) in cultured Atlantic salmon Salmo salar in Norway. PRV is also prevalent in wild and farmed salmon without overt disease manifestations, suggesting multifactorial triggers or PRV variant-specific factors are required to initiate disease. In this study, we explore the head kidney transcriptome of Sockeye salmon Oncorhynchus nerka during early PRV infection to identify host responses in the absence of disease in hopes of elucidating mechanisms by which PRV may directly alter host functions and contribute to the development of a disease state. We further investigate the role of PRV as a coinfecting agent following superinfection with infectious hematopoietic necrosis virus (IHNV) - a highly pathogenic rhabdovirus endemic to the west coast of North America.Challenge of Sockeye salmon with PRV resulted in high quantities of viral transcripts to become present in the blood and kidney of infected fish without manifestations of disease. De novo transcriptome assembly of over 2.3 billion paired RNA-seq reads from the head kidneys of 36 fish identified more than 320,000 putative unigenes, of which less than 20 were suggested to be differentially expressed in response to PRV at either 2 or 3 weeks post challenge by DESeq2 and edgeR analysis. Of these, only one, Ependymin, was confirmed to be differentially expressed by qPCR in an expanded sample set. In contrast, IHNV induced substantial transcriptional changes (differential expression of?>?20,000 unigenes) which included transcripts involved in antiviral and inflammatory response pathways. Prior infection with PRV had no significant effect on host responses to superinfecting IHNV, nor did host responses initiated by IHNV exposure influence increasing PRV loads.PRV does not substantially alter the head kidney transcriptome of Sockeye salmon during early (2 to 3 week) infection and dissemination in a period of significant increasing viral load, nor does the presence of PRV change the host transcriptional response to an IHNV superinfection. Further, concurrent infections of PRV and IHNV do not appear to significantly influence the infectivity or severity of IHNV associated disease, or conversely, PRV load.

SUBMITTER: Polinski MP

PROVIDER: S-EPMC5094019 | biostudies-literature | 2016 Nov

REPOSITORIES: biostudies-literature

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De novo assembly of Sockeye salmon kidney transcriptomes reveal a limited early response to piscine reovirus with or without infectious hematopoietic necrosis virus superinfection.

Polinski Mark P MP Bradshaw Julia C JC Inkpen Sabrina M SM Richard Jon J Fritsvold Camilla C Poppe Trygve T TT Rise Matthew L ML Garver Kyle A KA Johnson Stewart C SC

BMC genomics 20161102 1

<h4>Background</h4>Piscine reovirus (PRV) has been associated with the serious disease known as Heart and Skeletal Muscle Inflammation (HSMI) in cultured Atlantic salmon Salmo salar in Norway. PRV is also prevalent in wild and farmed salmon without overt disease manifestations, suggesting multifactorial triggers or PRV variant-specific factors are required to initiate disease. In this study, we explore the head kidney transcriptome of Sockeye salmon Oncorhynchus nerka during early PRV infection ...[more]

PMID: 27806699

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Project description:BackgroundSockeye Salmon are an iconic species widely distributed throughout the North Pacific. A devastating pathogen of Sockeye Salmon is infectious hematopoietic necrosis virus (IHNV, genus Novirhabdovirus, family Rhabdoviridae). It has been postulated that IHNV is maintained in salmon populations by persisting over the life of its host and/or by residing in natural reservoirs other than its susceptible hosts. Herein we demonstrate the presence of IHNV in the brain of Sockeye Salmon that survived an experimentally-induced outbreak, suggesting the presence of viral persistence in this susceptible species. To understand the viral persistent state in Sockeye Salmon we profiled the transcriptome to evaluate the host response in asymptomatic carriers and to determine what effects (if any) IHNV exposure may have on subsequent virus challenges.ResultsA laboratory disease model to simulate a natural IHNV outbreak in Sockeye Salmon resulted in over a third of the population incurring acute IHN disease and mortality during the first four months after initial exposure. Nine months post IHNV exposure, despite the absence of disease and mortality, a small percentage (<4 %) of the surviving population contained IHNV in brain. Transcriptome analysis in brain of asymptomatic virus carriers and survivors without virus exhibited distinct transcriptional profiles in comparison to naïve fish. Characteristic for carriers was the up-regulation of genes involved in antibody production and antigen presentation. In both carriers and survivors a down-regulation of genes related to cholesterol biosynthesis, resembling an antiviral mechanism observed in higher vertebrates was revealed along with differences in nervous system development. Moreover, following challenge with poly(I:C), survivors and carriers displayed an elevated antiviral immune response in comparison to naïve fish.ConclusionsIHN virus persistence was identified in Sockeye Salmon where it elicited a unique brain transcriptome profile suggesting an ongoing adaptive immune response. IHNV carriers remained uncompromised in mounting efficient innate antiviral responses when exposed to a viral mimic. The capacity of IHNV to reside in asymptomatic hosts supports a virus carrier hypothesis and if proven infectious, could have significant epidemiological consequences towards maintaining and spreading IHNV among susceptible host populations.

Project description:Bycatch is a common occurrence in heavily fished areas such as the Fraser River, British Columbia, where fisheries target returning adult Pacific salmon (Oncorhynchus spp.) en route to spawning grounds. The extent to which these encounters reduce fish survival through injury and physiological impairment depends on multiple factors including capture severity, river temperature and infectious agents. In an effort to characterize the mechanisms of post-release mortality and address fishery and managerial concerns regarding specific regulations, wild-caught Early Stuart sockeye salmon (Oncorhynchus nerka) were exposed to either mild (20 s) or severe (20 min) gillnet entanglement and then held at ecologically relevant temperatures throughout their period of river migration (mid-late July) and spawning (early August). Individuals were biopsy sampled immediately after entanglement and at death to measure indicators of stress and immunity, and the infection intensity of 44 potential pathogens. Biopsy alone increased mortality (males: 33%, females: 60%) when compared with non-biopsied controls (males: 7%, females: 15%), indicating high sensitivity to any handling during river migration, especially among females. Mortality did not occur until 5-10 days after entanglement, with severe entanglement resulting in the greatest mortality (males: 62%, females: 90%), followed by mild entanglement (males: 44%, females: 70%). Infection intensities of Flavobacterium psychrophilum and Ceratonova shasta measured at death were greater in fish that died sooner. Physiological indicators of host stress and immunity also differed depending on longevity, and indicated anaerobic metabolism, osmoregulatory failure and altered immune gene regulation in premature mortalities. Together, these results implicate latent effects of entanglement, especially among females, resulting in mortality days or weeks after release. Although any entanglement is potentially detrimental, reducing entanglement durations can improve post-release survival.

Dataset Information

De novo assembly of Sockeye salmon kidney transcriptomes reveal a limited early response to piscine reovirus with or without infectious hematopoietic necrosis virus superinfection.

Publications

De novo assembly of Sockeye salmon kidney transcriptomes reveal a limited early response to piscine reovirus with or without infectious hematopoietic necrosis virus superinfection.

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