Microscopic and Molecular Evidence of the First Elasmobranch Adomavirus, the Cause of Skin Disease in a Giant Guitarfish, <named-content content-type="genus-species">Rhynchobatus djiddensis</named-content>

ABSTRACT Only eight families of double-stranded DNA (dsDNA) viruses are known to infect vertebrate animals. During an investigation of papillomatous skin disease in an elasmobranch species, the giant guitarfish (Rhynchobatus djiddensis), a novel virus, distinct from all known viral families in regar...

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Autores principales:	Jennifer A. Dill, Alvin C. Camus, John H. Leary, Terry Fei Fan Ng
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	cartilaginous fish giant guitarfish adomavirus metagenomics pathology skin disease Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d1d89d415855486c99e83f1e26fa80ba
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spelling	oai:doaj.org-article:d1d89d415855486c99e83f1e26fa80ba2021-11-15T16:00:27ZMicroscopic and Molecular Evidence of the First Elasmobranch Adomavirus, the Cause of Skin Disease in a Giant Guitarfish, <named-content content-type="genus-species">Rhynchobatus djiddensis</named-content>10.1128/mBio.00185-182150-7511https://doaj.org/article/d1d89d415855486c99e83f1e26fa80ba2018-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00185-18https://doaj.org/toc/2150-7511ABSTRACT Only eight families of double-stranded DNA (dsDNA) viruses are known to infect vertebrate animals. During an investigation of papillomatous skin disease in an elasmobranch species, the giant guitarfish (Rhynchobatus djiddensis), a novel virus, distinct from all known viral families in regard to particle size, morphology, genome organization, and helicase phylogeny was discovered. Large inclusion bodies containing 75-nm icosahedral viral particles were present within epithelial cell nuclei in the proliferative skin lesions. Deep metagenomic sequencing revealed a 22-kb circular dsDNA viral genome, tentatively named guitarfish “adomavirus” (GAdoV), with only distant homology to two other fish viruses, Japanese eel endothelial cell-infecting virus (JEECV) and a recently reported marbled eel virus. Phylogenetic analysis of the helicase domain places the guitarfish virus in a novel clade that is equidistant between members of the Papillomaviridae and Polyomaviridae families. Specific PCR, quantitative PCR, and in situ hybridization were used to detect, quantify, and confirm that GAdoV DNA was localized to affected epithelial cell nuclei. Changes in the viral titer, as well as the presence of a hybridization signal, coincided with the progression and then final resolution of gross and microscopic lesions. The results indicate that GAdoV is the causative agent of the proliferative skin lesions. IMPORTANCE Cartilaginous fish, including the sharks and rays, evolved from ancestral fish species at least 400 million years ago. Even though they are the descendants of one of the most ancient vertebrate lineages, reports of viral diseases in these species are rare and poorly documented. Deep sequencing revealed a highly divergent virus, tentatively named guitarfish adomavirus, that is distantly related to known papillomaviruses and polyomaviruses. Out of the eight predicted viral genes, only the helicase could be identified as viral by sequence homology searches (BLAST), exemplifying the difficulties of discovering novel viruses within seas of unidentifiable “dark matter” associated with deep sequencing data. The novel adomavirus represents the first viral genome shown to cause clinical disease in a cartilaginous fish species, the giant guitarfish. Our findings demonstrate that emerging fish viruses are fertile ground to expand our understanding of viral evolution in vertebrates.Jennifer A. DillAlvin C. CamusJohn H. LearyTerry Fei Fan NgAmerican Society for Microbiologyarticlecartilaginous fishgiant guitarfishadomavirusmetagenomicspathologyskin diseaseMicrobiologyQR1-502ENmBio, Vol 9, Iss 3 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	cartilaginous fish giant guitarfish adomavirus metagenomics pathology skin disease Microbiology QR1-502
spellingShingle	cartilaginous fish giant guitarfish adomavirus metagenomics pathology skin disease Microbiology QR1-502 Jennifer A. Dill Alvin C. Camus John H. Leary Terry Fei Fan Ng Microscopic and Molecular Evidence of the First Elasmobranch Adomavirus, the Cause of Skin Disease in a Giant Guitarfish, <named-content content-type="genus-species">Rhynchobatus djiddensis</named-content>
description	ABSTRACT Only eight families of double-stranded DNA (dsDNA) viruses are known to infect vertebrate animals. During an investigation of papillomatous skin disease in an elasmobranch species, the giant guitarfish (Rhynchobatus djiddensis), a novel virus, distinct from all known viral families in regard to particle size, morphology, genome organization, and helicase phylogeny was discovered. Large inclusion bodies containing 75-nm icosahedral viral particles were present within epithelial cell nuclei in the proliferative skin lesions. Deep metagenomic sequencing revealed a 22-kb circular dsDNA viral genome, tentatively named guitarfish “adomavirus” (GAdoV), with only distant homology to two other fish viruses, Japanese eel endothelial cell-infecting virus (JEECV) and a recently reported marbled eel virus. Phylogenetic analysis of the helicase domain places the guitarfish virus in a novel clade that is equidistant between members of the Papillomaviridae and Polyomaviridae families. Specific PCR, quantitative PCR, and in situ hybridization were used to detect, quantify, and confirm that GAdoV DNA was localized to affected epithelial cell nuclei. Changes in the viral titer, as well as the presence of a hybridization signal, coincided with the progression and then final resolution of gross and microscopic lesions. The results indicate that GAdoV is the causative agent of the proliferative skin lesions. IMPORTANCE Cartilaginous fish, including the sharks and rays, evolved from ancestral fish species at least 400 million years ago. Even though they are the descendants of one of the most ancient vertebrate lineages, reports of viral diseases in these species are rare and poorly documented. Deep sequencing revealed a highly divergent virus, tentatively named guitarfish adomavirus, that is distantly related to known papillomaviruses and polyomaviruses. Out of the eight predicted viral genes, only the helicase could be identified as viral by sequence homology searches (BLAST), exemplifying the difficulties of discovering novel viruses within seas of unidentifiable “dark matter” associated with deep sequencing data. The novel adomavirus represents the first viral genome shown to cause clinical disease in a cartilaginous fish species, the giant guitarfish. Our findings demonstrate that emerging fish viruses are fertile ground to expand our understanding of viral evolution in vertebrates.
format	article
author	Jennifer A. Dill Alvin C. Camus John H. Leary Terry Fei Fan Ng
author_facet	Jennifer A. Dill Alvin C. Camus John H. Leary Terry Fei Fan Ng
author_sort	Jennifer A. Dill
title	Microscopic and Molecular Evidence of the First Elasmobranch Adomavirus, the Cause of Skin Disease in a Giant Guitarfish, <named-content content-type="genus-species">Rhynchobatus djiddensis</named-content>
title_short	Microscopic and Molecular Evidence of the First Elasmobranch Adomavirus, the Cause of Skin Disease in a Giant Guitarfish, <named-content content-type="genus-species">Rhynchobatus djiddensis</named-content>
title_full	Microscopic and Molecular Evidence of the First Elasmobranch Adomavirus, the Cause of Skin Disease in a Giant Guitarfish, <named-content content-type="genus-species">Rhynchobatus djiddensis</named-content>
title_fullStr	Microscopic and Molecular Evidence of the First Elasmobranch Adomavirus, the Cause of Skin Disease in a Giant Guitarfish, <named-content content-type="genus-species">Rhynchobatus djiddensis</named-content>
title_full_unstemmed	Microscopic and Molecular Evidence of the First Elasmobranch Adomavirus, the Cause of Skin Disease in a Giant Guitarfish, <named-content content-type="genus-species">Rhynchobatus djiddensis</named-content>
title_sort	microscopic and molecular evidence of the first elasmobranch adomavirus, the cause of skin disease in a giant guitarfish, <named-content content-type="genus-species">rhynchobatus djiddensis</named-content>
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/d1d89d415855486c99e83f1e26fa80ba
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Microscopic and Molecular Evidence of the First Elasmobranch Adomavirus, the Cause of Skin Disease in a Giant Guitarfish, <named-content content-type="genus-species">Rhynchobatus djiddensis</named-content>

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