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New insights into Sauropsid Papillomaviridae evolution and epizootiology: discovery of two novel papillomaviruses in native and invasive Island geckos.

ABSTRACT: Papillomaviruses cause persistent infections in skin and mucosal membranes and, in at least one species, are also be able to infect a tissue of mesenchymal origin. Infections may either be subclinical or induce proliferative lesions. Of the known papillomaviruses, the majority that have been characterized are from humans and other mammals. Currently, only fifteen complete bird and reptile papillomavirus genomes have been described, and they have been found in birds (n?=?11), turtles (n?=?2), and snakes (n?=?2). Using next-generation sequencing technologies and virus-specific PCR, we have identified two novel papillomavirus genomes, Hemidactylus frenatus Papillomavirus 1 and 2 (HfrePV1, HfrePV2), in the widely distributed and highly invasive Asian house gecko (H.frenatus) and mute gecko (Gehyra mutilata) on Christmas Island and Cocos (Keeling) Islands. HfrePV1 was also detected in critically endangered Lister's geckos (Lepidodactylus listeri) in their captive breeding colony on Christmas Island. Tissue-containing virus included epidermis, oral mucosa, and liver (HfrePV1) and epidermis, liver, and colon (HfrePV2). Concurrent infections were found in both H.frenatus and G.mutilata. Invasive mourning geckos (Lepidodactylus lugubris) (n?=?4), Sri Lankan house geckos (Hemidactylus parvimaculatus) (n?=?3), flat-tailed house geckos (Hemidactylus platyurus) (n?=?4) from the Cocos Islands, and blue-tailed skinks (Cryptoblepharus egeriae) (n?=?10) from Christmas Island were also screened but were not found to be infected. The novel HfrePV1 and HfrePV2 genomes were 7,378?bp and 7,380?bp in length, respectively, and each contained the early (E1, E2, and E7), and late (L1 and L2) open-reading frames. Phylogenetic analysis of the concatenated E1, E2, and L1 proteins from both papillomaviruses revealed that they clustered with, but were basal to, the Sauropsida clade containing bird and reptile viruses. This study sheds light on the evolution of papillomaviruses and the distribution of pathogens in a highly invasive species impacting endangered populations of geckos.

SUBMITTER: Agius JE

PROVIDER: S-EPMC6874027 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

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New insights into Sauropsid Papillomaviridae evolution and epizootiology: discovery of two novel papillomaviruses in native and invasive Island geckos.

Agius Jessica E JE Phalen David N DN Rose Karrie K Eden John-Sebastian JS

Virus evolution 20190701 2

Papillomaviruses cause persistent infections in skin and mucosal membranes and, in at least one species, are also be able to infect a tissue of mesenchymal origin. Infections may either be subclinical or induce proliferative lesions. Of the known papillomaviruses, the majority that have been characterized are from humans and other mammals. Currently, only fifteen complete bird and reptile papillomavirus genomes have been described, and they have been found in birds (n = 11), turtles (n ...[more]

PMID: 31798966

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Project description:The family Papillomaviridae contains more than 320 papillomavirus types, with most having been identified as infecting skin and mucosal epithelium in mammalian hosts. To date, only nine non-mammalian papillomaviruses have been described from birds (n?=?5), a fish (n?=?1), a snake (n?=?1), and turtles (n?=?2). The identification of papillomaviruses in sauropsids and a sparid fish suggests that early ancestors of papillomaviruses were already infecting the earliest Euteleostomi. The Euteleostomi clade includes more than 90 per cent of the living vertebrate species, and progeny virus could have been passed on to all members of this clade, inhabiting virtually every habitat on the planet. As part of this study, we isolated a novel papillomavirus from a 16-year-old female Adélie penguin (Pygoscelis adeliae) from Cape Crozier, Ross Island (Antarctica). The new papillomavirus shares ?64 per cent genome-wide identity to a previously described Adélie penguin papillomavirus. Phylogenetic analyses show that the non-mammalian viruses (expect the python, Morelia spilota, associated papillomavirus) cluster near the base of the papillomavirus evolutionary tree. A papillomavirus isolated from an avian host (Northern fulmar; Fulmarus glacialis), like the two turtle papillomaviruses, lacks a putative E9 protein that is found in all other avian papillomaviruses. Furthermore, the Northern fulmar papillomavirus has an E7 more similar to the mammalian viruses than the other avian papillomaviruses. Typical E6 proteins of mammalian papillomaviruses have two Zinc finger motifs, whereas the sauropsid papillomaviruses only have one such motif. Furthermore, this motif is absent in the fish papillomavirus. Thus, it is highly likely that the most recent common ancestor of the mammalian and sauropsid papillomaviruses had a single motif E6. It appears that a motif duplication resulted in mammalian papillomaviruses having a double Zinc finger motif in E6. We estimated the divergence time between Northern fulmar-associated papillomavirus and the other Sauropsid papillomaviruses be to around 250 million years ago, during the Paleozoic-Mesozoic transition and our analysis dates the root of the papillomavirus tree between 400 and 600 million years ago. Our analysis shows evidence for niche adaptation and that these non-mammalian viruses have highly divergent E6 and E7 proteins, providing insights into the evolution of the early viral (onco-)proteins.

Project description:Genes encoded in vertebrate mitochondrial DNAs are transcribed as a polycistronic transcript for both strands, which is later processed into individual mRNAs, rRNAs and tRNAs, followed by modifications, such as polyadenylation at the 3' end of mRNAs. Although mechanisms of the mitochondrial transcription and RNA processing have been extensively studied using some model organisms, structural variability of mitochondrial mRNAs across different groups of vertebrates is poorly understood. We conducted the high-throughput RNA sequencing to identify major polyadenylation sites for mitochondrial mRNAs in the Japanese grass lizard, Takydromus tachydromoides and compared the polyadenylation profiles with those identified similarly for 23 tetrapod species, featuring sauropsid taxa (reptiles and birds).As compared to the human, a major polyadenylation site for the NADH dehydrogenase subunit 5 mRNA of the grass lizard was located much closer to its stop codon, resulting in considerable truncation of the 3' untranslated region for the mRNA. Among the other sauropsid taxa, several distinct polyadenylation profiles from the human counterpart were found for different mRNAs. They included various truncations of the 3' untranslated region for NADH dehydrogenase subunit 5 mRNA in four taxa, bird-specific polyadenylation of the light-strand-transcribed NADH dehydrogenase subunit 6 mRNA, and the combination of the ATP synthase subunit 8/6 mRNA with a neighboring mRNA into a tricistronic mRNA in the side-necked turtle Pelusios castaneus. In the last case of P. castaneus, as well as another example for NADH dehydrogenase subunit 1 mRNAs of some birds, the association between the polyadenylation site change and the gene overlap was highlighted. The variations in the polyadenylation profile were suggested to have arisen repeatedly in diverse sauropsid lineages. Some of them likely occurred in response to gene rearrangements in the mitochondrial DNA but the others not.These results demonstrate structural variability of mitochondrial mRNAs in sauropsids. The efficient and comprehensive characterization of the mitochondrial mRNAs will contribute to broaden our understanding of their structural and functional evolution.

Dataset Information

New insights into Sauropsid Papillomaviridae evolution and epizootiology: discovery of two novel papillomaviruses in native and invasive Island geckos.

Publications

New insights into Sauropsid <i>Papillomaviridae</i> evolution and epizootiology: discovery of two novel papillomaviruses in native and invasive Island geckos.

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