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Geography and host species shape the evolutionary dynamics of U genogroup infectious hematopoietic necrosis virus.

ABSTRACT: Infectious hematopoietic necrosis virus (IHNV) is a negative-sense RNA virus that infects wild and cultured salmonids throughout the Pacific Coastal United States and Canada, from California to Alaska. Although infection of adult fish is usually asymptomatic, juvenile infections can result in high mortality events that impact salmon hatchery programs and commercial aquaculture. We used epidemiological case data and genetic sequence data from a 303?nt portion of the viral glycoprotein gene to study the evolutionary dynamics of U genogroup IHNV in the Pacific Northwestern United States from 1971 to 2013. We identified 114 unique genotypes among 1,219?U genogroup IHNV isolates representing 619 virus detection events. We found evidence for two previously unidentified, broad subgroups within the U genogroup, which we designated 'UC' and 'UP'. Epidemiologic records indicated that UP viruses were detected more frequently in sockeye salmon (Oncorhynchus nerka) and in coastal waters of Washington and Oregon, whereas UC viruses were detected primarily in Chinook salmon (Oncorhynchus tshawytscha) and steelhead trout (Oncorhynchus mykiss) in the Columbia River Basin, which is a large, complex watershed extending throughout much of interior Washington, Oregon, and Idaho. These findings were supported by phylogenetic analysis and by FST. Ancestral state reconstruction indicated that early UC viruses in the Columbia River Basin initially infected sockeye salmon but then emerged via host shifts into Chinook salmon and steelhead trout sometime during the 1980s. We postulate that the development of these subgroups within U genogroup was driven by selection pressure for viral adaptation to Chinook salmon and steelhead trout within the Columbia River Basin.

SUBMITTER: Black A

PROVIDER: S-EPMC5822886 | biostudies-literature | 2016 Jul

REPOSITORIES: biostudies-literature

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Geography and host species shape the evolutionary dynamics of U genogroup infectious hematopoietic necrosis virus.

Black Allison A Breyta Rachel R Bedford Trevor T Kurath Gael G

Virus evolution 20160701 2

Infectious hematopoietic necrosis virus (IHNV) is a negative-sense RNA virus that infects wild and cultured salmonids throughout the Pacific Coastal United States and Canada, from California to Alaska. Although infection of adult fish is usually asymptomatic, juvenile infections can result in high mortality events that impact salmon hatchery programs and commercial aquaculture. We used epidemiological case data and genetic sequence data from a 303 nt portion of the viral glycoprotein gene to stu ...[more]

PMID: 29492278

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Project description:Many pathogens interact and evolve in communities where more than one host species is present, yet our understanding of host-pathogen specialization is mostly informed by laboratory studies with single species. Managing diseases in the wild, however, requires understanding how host-pathogen specialization affects hosts in diverse communities. Juvenile salmonid mortality in hatcheries caused by infectious hematopoietic necrosis virus (IHNV) has important implications for salmonid conservation programs. Here, we evaluate evidence for IHNV specialization on three salmonid hosts and assess how this influences intra- and interspecific transmission in hatchery-reared salmonids. We expect that while more generalist viral lineages should pose an equal risk of infection across host types, viral specialization will increase intraspecific transmission. We used Bayesian models and data from 24 hatcheries in the Columbia River Basin to reconstruct the exposure history of hatcheries with two IHNV lineages, MD and UC, allowing us to estimate the probability of juvenile infection with these lineages in three salmonid host types. Our results show that lineage MD is specialized on steelhead trout and perhaps rainbow trout (both Oncorhynchus mykiss), whereas lineage UC displayed a generalist phenotype across steelhead trout, rainbow trout, and Chinook salmon. Furthermore, our results suggest the presence of specialist-generalist trade-offs because, while lineage UC had moderate probabilities of infection across host types, lineage MD had a small probability of infection in its nonadapted host type, Chinook salmon. Thus, in addition to quantifying probabilities of infection of socially and economically important salmonid hosts with different IHNV lineages, our results provide insights into the trade-offs that viral lineages incur in multihost communities. Our results suggest that knowledge of the specialist/generalist strategies of circulating viral lineages could be useful in salmonid conservation programs to control disease.

Project description:The genome of infectious hematopoietic necrosis virus (IHNV), a salmonid novirhabdovirus, has been engineered to modify the gene order and to evaluate the impact on a possible attenuation of the virus in vitro and in vivo By reverse genetics, eight recombinant IHNVs (rIHNVs), termed NxGy according to the respective positions of the nucleoprotein (N) and glycoprotein (G) genes along the genome, have been recovered. All rIHNVs have been fully characterized in vitro for their cytopathic effects, kinetics of replication, and profiles of viral gene transcription. These rIHNVs are stable through up to 10 passages in cell culture. Following bath immersion administration of the various rIHNVs to juvenile trout, some of the rIHNVs were clearly attenuated (N2G3, N2G4, N3G4, and N4G1). The position of the N gene seems to be one of the most critical features correlated to the level of viral attenuation. The induced immune response potential in fish was evaluated by enzyme-linked immunosorbent spot assay (ELISPOT) and seroneutralization assays. The recombinant virus N2G3 induced a strong antibody response in immunized fish and conferred 86% of protection against wild-type IHNV challenge in trout, thus representing a promising starting point for the development of a live attenuated vaccine candidate.In Europe, no vaccines are available against infectious hematopoietic necrosis virus (IHNV), one of the major economic threats in fish aquaculture. Live attenuated vaccines are conditioned by a sensible balance between attenuation and pathogenicity. Moreover, nonsegmented negative-strain RNA viruses (NNSV) are subject to a transcription gradient dictated by the order of the genes in their genomes. With the perspective of developing a vaccine against IHNV, we engineered various recombinant IHNVs with reordered genomes in order to artificially attenuate the virus. Our results validate the gene rearrangement approach as a potent and stable attenuation strategy for fish novirhabdovirus and open a new perspective for design of vaccines against other NNSV.

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Geography and host species shape the evolutionary dynamics of U genogroup infectious hematopoietic necrosis virus.

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Geography and host species shape the evolutionary dynamics of U genogroup infectious hematopoietic necrosis virus.

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