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The genome of the nucleopolyhedrosis-causing virus from Tipula oleracea sheds new light on the Nudiviridae family.

ABSTRACT: A large double-stranded DNA (dsDNA) virus that produces occlusion bodies, typical of baculoviruses, has been described to infect crane fly larvae of the genus Tipula (Diptera, Tipulidae). Because of a lack of genomic data, this virus has remained unclassified. Electron microscopy of an archival virus isolated from Tipula oleracea, T. oleracea nudivirus (ToNV), showed irregularly shaped occlusion bodies measuring from 2 to 5 ?m in length and 2 ?m in middiameter, filled with rod-shape virions containing single nucleocapsids within a bilayer envelope. Whole-genome amplification and Roche 454 sequencing revealed a complete circular genome sequence of 145.7 kb, containing five direct repeat regions. We predicted 131 open reading frames, including a homolog of the polyhedrin gene encoding the major occlusion body protein of T. paludosa nucleopolyhedrovirus (NPV). BLAST searches demonstrated that ToNV had 21 of the 37 baculovirus core genes but shared 52 genes with nudiviruses (NVs). Phylogenomic analyses indicated that ToNV clearly belongs to the Nudiviridae family but should probably be assigned to a new genus. Among nudiviruses, ToNV was most closely related to the Penaeus monodon NV and Heliothis zea NV clade but distantly related to Drosophila innubia NV, the other nudivirus infecting a Diptera. Lastly, ToNV was found to be most closely related to the nuvidirus ancestor of bracoviruses. This was also reflected in terms of gene content, as ToNV was the only known exogenous virus harboring homologs of the Cc50C22.6 and 27b (Cc50C22.7) genes found in the nudiviral genomic cluster involved in bracovirus particle production.The Nudiviridae is a family of arthropod dsDNA viruses from which striking cases of endogenization have been reported (i.e., symbiotic bracoviruses deriving from a nudivirus and the endogenous nudivirus of the brown planthopper). Although related to baculoviruses, relatively little is known about the genomic diversity of exogenous nudiviruses. Here, we characterized, morphologically and genetically, an archival sample of the Tipula oleracea nudivirus (ToNV), which has the particularity of forming occlusion bodies. Comparative genomic and phylogenomic analyses showed ToNV to be to date the closest known relative of the exogenous ancestor of bracoviruses and that ToNV should be assigned to a new genus. Moreover, we revised the homology relationships of nudiviral genes and identified a new set of 32 core genes for the Nudiviridae, of which 21 were also baculovirus core genes. These findings provide important insights into the evolutionary history of large arthropod dsDNA viruses.

SUBMITTER: Bezier A

PROVIDER: S-EPMC4337555 | biostudies-literature | 2015 Mar

REPOSITORIES: biostudies-literature

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The genome of the nucleopolyhedrosis-causing virus from Tipula oleracea sheds new light on the Nudiviridae family.

Bézier Annie A Thézé Julien J Gavory Frederick F Gaillard Julien J Poulain Julie J Drezen Jean-Michel JM Herniou Elisabeth A EA

Journal of virology 20141224 6

<h4>Unlabelled</h4>A large double-stranded DNA (dsDNA) virus that produces occlusion bodies, typical of baculoviruses, has been described to infect crane fly larvae of the genus Tipula (Diptera, Tipulidae). Because of a lack of genomic data, this virus has remained unclassified. Electron microscopy of an archival virus isolated from Tipula oleracea, T. oleracea nudivirus (ToNV), showed irregularly shaped occlusion bodies measuring from 2 to 5 μm in length and 2 μm in middiameter, filled with rod ...[more]

PMID: 25540386

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Project description:BackgroundThe New Zealand collembolan genus Holacanthella contains the largest species of springtails (Collembola) in the world. Using Illumina technology we have sequenced and assembled a draft genome and transcriptome from Holacanthella duospinosa (Salmon). We have used this annotated assembly to investigate the genetic basis of a range of traits critical to the evolution of the Hexapoda, the phylogenetic position of H. duospinosa and potential horizontal gene transfer events.ResultsOur genome assembly was ~375 Mbp in size with a scaffold N50 of ~230 Kbp and sequencing coverage of ~180×. DNA elements, LTRs and simple repeats and LINEs formed the largest components and SINEs were very rare. Phylogenomics (370,877 amino acids) placed H. duospinosa within the Neanuridae. We recovered orthologs of the conserved sex determination genes thought to play a role in sex determination. Analysis of CpG content suggested the absence of DNA methylation, and consistent with this we were unable to detect orthologs of the DNA methyltransferase enzymes. The small subunit rRNA gene contained a possible retrotransposon. The Hox gene complex was broken over two scaffolds. For chemosensory ability, at least 15 and 18 ionotropic glutamate and gustatory receptors were identified, respectively. However, we were unable to identify any odorant receptors or their obligate co-receptor Orco. Twenty-three chitinase-like genes were identified from the assembly. Members of this multigene family may play roles in the digestion of fungal cell walls, a common food source for these saproxylic organisms. We also detected 59 and 96 genes that blasted to bacteria and fungi, respectively, but were located on scaffolds that otherwise contained arthropod genes.ConclusionsThe genome of H. duospinosa contains some unusual features including a Hox complex broken over two scaffolds, in a different manner to other arthropod species, a lack of odorant receptor genes and an apparent lack of environmentally responsive DNA methylation, unlike many other arthropods. Our detection of candidate horizontal gene transfer candidates confirms that this phenomenon is occurring across Collembola. These findings allow us to narrow down the regions of the arthropod phylogeny where key innovations have occurred that have facilitated the evolutionary success of Hexapoda.

Project description:BackgroundButterflies and moths are emerging as model organisms in genetics and evolutionary studies. The family Hesperiidae (skippers) was traditionally viewed as a sister to other butterflies based on its moth-like morphology and darting flight habits with fast wing beats. However, DNA studies suggest that the family Papilionidae (swallowtails) may be the sister to other butterflies including skippers. The moth-like features and the controversial position of skippers in Lepidoptera phylogeny make them valuable targets for comparative genomics.ResultsWe obtained the 310 Mb draft genome of the Clouded Skipper (Lerema accius) from a wild-caught specimen using a cost-effective strategy that overcomes the high (1.6 %) heterozygosity problem. Comparative analysis of Lerema accius and the highly heterozygous genome of Papilio glaucus revealed differences in patterns of SNP distribution, but similarities in functions of genes that are enriched in non-synonymous SNPs. Comparison of Lepidoptera genomes revealed possible molecular bases for unique traits of skippers: a duplication of electron transport chain components could result in efficient energy supply for their rapid flight; a diversified family of predicted cellulases might allow them to feed on cellulose-enriched grasses; an expansion of pheromone-binding proteins and enzymes for pheromone synthesis implies a more efficient mate-recognition system, which compensates for the lack of clear visual cues due to the similarities in wing colors and patterns of many species of skippers. Phylogenetic analysis of several Lepidoptera genomes suggested that the position of Hesperiidae remains uncertain as the tree topology varied depending on the evolutionary model.ConclusionCompletion of the first genome from the family Hesperiidae allowed comparative analyses with other Lepidoptera that revealed potential genetic bases for the unique phenotypic traits of skippers. This work lays the foundation for future experimental studies of skippers and provides a rich dataset for comparative genomics and phylogenetic studies of Lepidoptera.

Dataset Information

The genome of the nucleopolyhedrosis-causing virus from Tipula oleracea sheds new light on the Nudiviridae family.

Publications

The genome of the nucleopolyhedrosis-causing virus from Tipula oleracea sheds new light on the Nudiviridae family.

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