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Detection of spring viraemia of carp virus in imported amphibians reveals an unanticipated foreign animal disease threat.

ABSTRACT: Global translocation of plants and animals is a well-recognized mechanism for introduction of pathogens into new regions. To mitigate this risk, various tools such as preshipment health certificates, quarantines, screening for specific disease agents and outright bans have been implemented. However, such measures only target known infectious agents and their hosts and may fail to prevent translocation of even well-recognized pathogens if they are carried by novel host species. In a recent example, we screened an imported shipment of Chinese firebelly newts (Cynops orientalis) for Batrachochytrium salamandrivorans, an emergent fungal pathogen of salamanders. All animals tested negative for the fungus. However, a virus was cultured from internal organs from 7 of the 11 individual dead salamanders and from two pools of tissues from four additional dead animals. Sequencing of a portion of the glycoprotein gene from all viral isolates indicated 100% identity and that they were most closely related to spring viraemia of carp virus (SVCV). Subsequently, SVCV-specific PCR testing indicated the presence of virus in internal organs from each of the four animals previously pooled, and whole-genome sequencing of one of the viral isolates confirmed genomic arrangement characteristic of SVCV. SVCV is a rhabdovirus pathogen of cyprinid fish that is listed as notifiable to the Office International des Epizooties. This discovery reveals a novel route for potential spillover of this economically important pathogen as rhabdovirus has not previously been documented in amphibians.

SUBMITTER: Ip HS

PROVIDER: S-EPMC5113056 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Spring viremia of carp virus (SVCV) is a highly pathogenic Vesiculovirus infecting the common carp, yet neither a vaccine nor effective therapies are available to treat spring viremia of carp (SVC). Like all negative-sense viruses, SVCV contains an RNA genome that is encapsidated by the nucleoprotein (N) in the form of a ribonucleoprotein (RNP) complex, which serves as the template for viral replication and transcription. Here, the three-dimensional (3D) structure of SVCV RNP was resolved through cryo-electron microscopy (cryo-EM) at a resolution of 3.7 Å. RNP assembly was stabilized by N and C loops; RNA was wrapped in the groove between the N and C lobes with 9 nt nucleotide per protomer. Combined with mutational analysis, our results elucidated the mechanism of RNP formation. The RNA binding groove of SVCV N was used as a target for drug virtual screening, and it was found suramin had a good antiviral effect. This study provided insights into RNP assembly, and anti-SVCV drug screening was performed on the basis of this structure, providing a theoretical basis and efficient drug screening method for the prevention and treatment of SVC. IMPORTANCE Aquaculture accounts for about 70% of global aquatic products, and viral diseases severely harm the development of aquaculture industry. Spring viremia of carp virus (SVCV) is the pathogen causing highly contagious spring viremia of carp (SVC) disease in cyprinids, especially common carp (Cyprinus carpio), yet neither a vaccine nor effective therapies are available to treat this disease. In this study, we have elucidated the mechanism of SVCV ribonucleoprotein complex (RNP) formation by resolving the 3D structure of SVCV RNP and screened antiviral drugs based on the structure. It is found that suramin could competitively bind to the RNA binding groove and has good antiviral effects both in vivo and in vitro. Our study provides a template for rational drug discovery efforts to treat and prevent SVCV infections.

Project description:Spring viraemia of carp (SVC) is a fatal viral disease for cyprinid fish, which is caused by spring viraemia of carp virus (SVCV). To date, no SVC outbreak has been reported in China. Between 1998 and 2002, outbreaks of SVC were reported in ornamental and wild fish in Europe and America, imported from multiple sources including China. Based on phylogenetic analysis, the viral strain isolated from America was shown to be originated from Asia. These outbreaks not only resulted in huge economic losses, but also raise an interesting question as to whether SVCV really exists in China and if so, is it responsible for SVC outbreaks? From 2002 to 2006, we screened 6700 samples from ornamental fish farms using the cell culture method of the Office International des Epizooties (OIE), and further verified the presence of SVCV by ELISA and real-time quantitative RT-PCR. Two infected samples were found and the complete genome of SVCV was sequenced from one of the isolates, termed SVCV-C1. Several unique hallmarks of SVCV-C1 were identified, including six amino acid (KSLANA) insertion in the viral RNA-dependent RNA polymerase (L) protein and ten nucleotide insertion in the region between glycoprotein (G) and L genes in European SVCV strains. Phylogenetic tree analysis of the full-length G protein of selected SVCV isolates from the United Kingdom and United States revealed that G proteins could be classified into Ia and Id sub genogroups. The Ia sub genogroup can be further divided into newly defined sub genogroups Ia-A and Ia-B. The isolates derived from the United States and China including the SVCV-C1 belongs to in the Ia-A sub genogroup. The SVCV-C1 G protein shares more than 99% homology with the G proteins of the SVCV strains from England and the United States, making it difficult to compare their pathogenicity. Comparison of the predicted three-dimensional structure based on the published G protein sequences from five SVCV strains revealed that the main differences were in the loops of the pleckstrin homology domains. Since SVCV is highly pathogenic, we speculate that SVC may therefore pose a serious threat to farmed cyprinid fish in China.

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Detection of spring viraemia of carp virus in imported amphibians reveals an unanticipated foreign animal disease threat.

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