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Discovery of a novel nidovirus in cattle with respiratory disease.

ABSTRACT: The family Coronaviridae represents a diverse group of vertebrate RNA viruses, all with genomes greater than 26,000 nt. Here, we report the discovery and genetic characterization of a novel virus present in cattle with respiratory disease. Phylogenetic characterization of this virus revealed that it clusters within the subfamily Torovirinae, in the family Coronaviridae. The complete genome consists of only 20,261 nt and represents the smallest reported coronavirus genome. We identified seven ORFs, including the canonical nidovirus ORF1a and ORF1b. Analysis of polyprotein 1ab revealed that this virus, tentatively named bovine nidovirus (BoNV), shares the highest homology with the recently described python-borne nidoviruses and contains several conserved nidovirus motifs, but does not encode the NendoU or O-MT domains that are present in other viruses within the family Coronaviridae. In concert with its reduced genome, the atypical domain architecture indicates that this virus represents a unique lineage within the order Nidovirales.

SUBMITTER: Tokarz R

PROVIDER: S-EPMC4681066 | biostudies-literature | 2015 Aug

REPOSITORIES: biostudies-literature

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Discovery of a novel nidovirus in cattle with respiratory disease.

Tokarz Rafal R Sameroff Stephen S Hesse Richard A RA Hause Ben M BM Desai Aaloki A Jain Komal K Ian Lipkin W W

The Journal of general virology 20150427 8

The family Coronaviridae represents a diverse group of vertebrate RNA viruses, all with genomes greater than 26,000 nt. Here, we report the discovery and genetic characterization of a novel virus present in cattle with respiratory disease. Phylogenetic characterization of this virus revealed that it clusters within the subfamily Torovirinae, in the family Coronaviridae. The complete genome consists of only 20,261 nt and represents the smallest reported coronavirus genome. We identified seven ORF ...[more]

PMID: 25918239

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Project description:UnlabelledA severe, sometimes fatal respiratory disease has been observed in captive ball pythons (Python regius) since the late 1990s. In order to better understand this disease and its etiology, we collected case and control samples and performed pathological and diagnostic analyses. Electron micrographs revealed filamentous virus-like particles in lung epithelial cells of sick animals. Diagnostic testing for known pathogens did not identify an etiologic agent, so unbiased metagenomic sequencing was performed. Abundant nidovirus-like sequences were identified in cases and were used to assemble the genome of a previously unknown virus in the order Nidovirales. The nidoviruses, which were not previously known to infect nonavian reptiles, are a diverse order that includes important human and veterinary pathogens. The presence of the viral RNA was confirmed in all diseased animals (n = 8) but was not detected in healthy pythons or other snakes (n = 57). Viral RNA levels were generally highest in the lung and other respiratory tract tissues. The 33.5-kb viral genome is the largest RNA genome yet described and shares canonical characteristics with other nidovirus genomes, although several features distinguish this from related viruses. This virus, which we named ball python nidovirus (BPNV), will likely establish a new genus in Torovirinae subfamily. The identification of a novel nidovirus in reptiles contributes to our understanding of the biology and evolution of related viruses, and its association with lung disease in pythons is a promising step toward elucidating an etiology for this long-standing veterinary disease.ImportanceBall pythons are popular pets because of their diverse coloration, generally nonaggressive behavior, and relatively small size. Since the 1990s, veterinarians have been aware of an infectious respiratory disease of unknown cause in ball pythons that can be fatal. We used unbiased shotgun sequencing to discover a novel virus in the order Nidovirales that was present in cases but not controls. While nidoviruses are known to infect a variety of animals, this is the first report of a nidovirus recovered from any reptile. This report will enable diagnostics that will assist in determining the role of this virus in the causation of disease, which would allow control of the disease in zoos and private collections. Given its evolutionary divergence from known nidoviruses and its unique host, the study of reptile nidoviruses may further our understanding of related diseases and the viruses that cause them in humans and other animals.

Project description:BACKGROUND: Among the eutherian mammals, placental architecture varies to a greater extent than any other tissue. The diversity of placental types, even within a single mammalian order suggests that genes expressed in placenta are under strong Darwinian selection. Thus, the ruminant placenta may be a rich source of genes to explore adaptive evolutionary responses in mammals. The aim of our study was to identify novel transcripts expressed in ruminant placenta, and to characterize them with respect to their expression patterns, organization of coding sequences in the genome, and potential functions. RESULTS: A combination of bioinformatics, comparative genomics and transcript profiling was used to identify and characterize 91 novel transcripts (NTs) represented in a cattle placenta cDNA library. These NTs have no significant similarity to any non-ferungulate DNA or RNA sequence. Proteins longer than 100 aa were predicted for 29 NTs, and 21 are candidate non-coding RNAs. Eighty-six NTs were found to be expressed in one or more of 18 different tissues, with 39 (42%) showing tissue-preference, including six that were expressed exclusively in placentome. The authenticity of the NTs was confirmed by their alignment to cattle genome sequence, 42 of which showed evidence of mRNA splicing. Analysis of the genomic context where NT genes reside revealed 61 to be in intergenic regions, whereas 30 are within introns of known genes. The genes encoding the NTs were found to be significantly associated with subtelomeric regions. CONCLUSION: The 91 lineage-specific transcripts are a useful resource for studying adaptive evolutionary responses of the ruminant placenta. The presence of so many genes encoding NTs in cattle but not primates or rodents suggests that gene loss and gain are important mechanisms of genome evolution in mammals. Furthermore, the clustering of NT genes within subtelomeric regions suggests that such regions are highly dynamic and may foster the birth of novel genes. The sequencing of additional vertebrate genomes with defined phylogenetic relationships will permit the search for lineage-specific genes to take on a more evolutionary context that is required to understand their origins and functions.

Dataset Information

Discovery of a novel nidovirus in cattle with respiratory disease.

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Discovery of a novel nidovirus in cattle with respiratory disease.

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