Rapid Viral Symbiogenesis via Changes in Parasitoid Wasp Genome Architecture

Burke, Gaelen R.; Simmonds, Tyler J.; Sharanowski, Barbara J.; Geib, Scott M.

doi:10.1093/molbev/msy148

Cited by 44 publications

(71 citation statements)

References 61 publications

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“…The IVSPERs in H. didymator , G. fumiferanae and now Lissonota (all Banchines) are each located in three compact clusters within wasp genomes, respectively. This level of clustering is similar to the architecture observed for the recently-derived endogenous nudivirus in F. arisanus (nine major clusters) , and lies in contrast to the extensive spread of nudivirus-like genes in the M. demolitor genome representative of the bracovirus-producing microgastrine wasps Burke, Simmonds, et al 2018;Burke, Walden, et al 2018) . As the spread of virus-derived wasp genes throughout wasp genomes is thought to be a relatively neutral process that occurs over evolutionary time , the limited spread of the IVSPERs in wasp genomes indicates that their integration occurred relatively recently.…”

Section: "Ichnoviruses" Represent Two Independent Relatively Recent supporting

confidence: 73%

“…Among parasitoid wasps, Ichneumonoidea are particularly diverse, comprising ~28% of all Hymenoptera, ~3% of all terrestrial, multicellular life (Chapman 2009;Yu et al 2012) and parasitizing a broad range of insects and other arthropods. To facilitate host invasion, ichneumonoid wasps are known to employ novel viral associations in the form of Endogenous Viral Elements (EVEs), in which elements of viral genomes become permanently integrated into the genomes of wasps (Bezier et al 2009;Burke, Simmonds, et al 2018;Pichon et al 2015;Volkoff et al 2010;Béliveau et al 2015) . EVEs produce virions or virus-like particles (VLPs) in ovaries of these wasps, which are injected into hosts during parasitism.…”

Section: Perhaps Some Of the Most Complex Examples Of Viral Endogenizmentioning

confidence: 99%

“…The V. canescens genome lacks the genes required to make a capsid to house viral DNA in virions, preventing delivery of virulence genes but allowing delivery of wasp-derived virulence proteins into hosts within VLPs (Feddersen et al 1986;Pichon et al 2015) . Through wasp genome sequencing, an independent acquisition of viral genes from the alpha-nudiviruses was recently identified in Fopius arisanus (Braconidae), the first recognized incidence of viral genome integration in the subfamily Opiinae (Burke, Simmonds, et al 2018) . Other reports of reproductive gland associated viruses in the Ichneumonoidea have been published (>35), but are limited to the identification of virions in wasp tissues and do not include any genetic analyses (Suzuki & Tanaka 2006;Lawrence 2005) .…”

Section: Perhaps Some Of the Most Complex Examples Of Viral Endogenizmentioning

confidence: 99%

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Endogenization from diverse viral ancestors is common and widespread in parasitoid wasps

Burke

Hines

Sharanowski

2020

Preprint

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The Ichneumonoidea (Ichneumonidae and Braconidae) is an incredibly diverse superfamily of parasitoid wasps that includes species that produce virus-like entities in their reproductive tracts to promote successful parasitism of host insects. Research on these entities has traditionally focused upon two viral genera Bracovirus (in Braconidae) and Ichnovirus (in Ichneumonidae). These viruses are produced using genes known collectively as endogenous viral elements (EVEs) that represent historical, now heritable viral integration events in wasp genomes. Here, new genome sequence assemblies for eleven species and six publicly available genomes from the Ichneumonoidea were screened with the goal of identifying novel EVEs and characterizing the breadth of species in lineages with known EVEs. Exhaustive similarity searches combined with the identification of ancient core genes revealed sequences from both known and novel EVEs. Two species harbored novel, independently derived EVEs related to a divergent large DNA (dsDNA) virus that manipulates behavior in other hymenopteran species. While bracovirus or ichnovirus EVEs were identified as expected in three species, the absence of ichnoviruses in several species suggests that they are independently derived and present in two younger, less widespread lineages than previously thought. Overall, this study presents a novel bioinformatic approach for EVE discovery in genomes and shows that three divergent virus families (nudiviruses, the ancestors of ichnoviruses, and LbFV-like viruses) are recurrently acquired as EVEs in parasitoid wasps. Virus acquisition in the parasitoid wasps is a common process that has occurred in many more than two lineages from a diverse range of arthropod-infecting dsDNA viruses. SignificanceParasitoid wasps are an extremely diverse group of animals that are known to harbor Endogenous Virus Elements (EVEs) that produce virions or virus-like particles of key importance in wasps' parasitism success. However, the prevalence and diversity of independently acquired EVEs in parasitoid wasp lineages has remained largely uncharacterized on a widespread scale. This study represents an important first step and hints at the massive, untapped diversity of EVEs in parasitoid wasps via the identification of several novel virus co-option events from diverse groups of double-stranded DNA virus pathogens.

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Section: "Ichnoviruses" Represent Two Independent Relatively Recent supporting

confidence: 73%

Section: Perhaps Some Of the Most Complex Examples Of Viral Endogenizmentioning

confidence: 99%

Section: Perhaps Some Of the Most Complex Examples Of Viral Endogenizmentioning

confidence: 99%

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Endogenization from diverse viral ancestors is common and widespread in parasitoid wasps

Burke

Hines

Sharanowski

2020

Preprint

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“…At least 25 of the 32 nudivirus core genes involved in essential viral functions 27 have been retained in the wasp genome, with the notable absence of the nudiviral DNA polymerase (Supplementary Table 8). The loss of this major replication gene may have prevented viral escape 10,25,28 . The fen genes, generally involved in DNA replication, form a gene family with six tandem copies that is found specifically in the Cotesia lineage (Fig.…”

Section: Resultsmentioning

confidence: 99%

Chromosomal resolution reveals symbiotic virus colonization of parasitic wasp genomes

Gauthier

Boulain

Vugt

et al. 2020

Preprint

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17Most endogenous viruses, an important proportion of eukaryote genomes, are doomed to slowly 18 decay. Little is known, however, on how they evolve when they confer a benefit to their host. 19Bracoviruses are essential for the parasitism success of parasitoid wasps, whose genomes they 20 integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp 21 genome, for the first time at a chromosomal scale, that symbiotic bracovirus genes spread to 22 and colonized all the chromosomes. Moreover, large viral clusters are stably maintained 23 suggesting strong evolutionary constraints. Genomic comparison with another wasps revealed 24 that this organization was already established ~53 mya. Transcriptomic analyses highlight 25 temporal synchronization of viral gene expression, leading to particle production. Immune 26 genes are not induced, however, indicating the virus is not perceived as foreign by the wasp. 27This recognition suggests that no conflicts remain between symbiotic partners when benefits to 28 them converge. 29 30 31 32 33 Main 34 Cotesia wasps (Hymenoptera, Braconidae) are parasitoids of Lepidoptera. Female 35 wasps lay their eggs into caterpillars and larvae develop feeding on the host hemolymph. 36Several Cotesia species are famous for their use as biological control agents to control insect 37 pests, such as Cotesia flavipes which is massively released over several million hectares of 38 sugarcane fields in Brazil 1,2 . Parasitoid wasps evolved several strategies that increase parasitic 39 success, including a sensitive olfactory apparatus to locate their hosts 3,4 and detoxification 40 mechanisms against plant toxic compounds accumulating in their host (Fig. 1). But the most 41 original strategy is the domestication of a bracovirus (BV) shared by over 46,000 braconid wasp 42 species 5 . Bracoviruses originate from a single integration event ~103 million years ago (mya) 43 of a nudivirus in the genome of the last common ancestor of this group 6-9 . Virus domestication 44 nowadays confers a benefit to the wasps that use BVs as virulence gene delivery systems 10 . 45

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“…and transfer virulence proteins into host cells (Pichon et al 2015;Burke et al 2018). Viral genes encoding VLP proteins are either dispersed in the wasp genome (as in VcVLP) or present in discrete genomic areas (as in FaENV).…”

mentioning

confidence: 99%

Immune Suppressive Extracellular Vesicle Proteins ofLeptopilina heterotomaAre Encoded in the Wasp Genome

Wey

Heavner

Wittmeyer

et al. 2020

G3 Genes|Genomes|Genetics

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Leptopilina heterotoma are obligate parasitoid wasps that develop in the body of their Drosophila hosts. During oviposition, female wasps introduce venom into the larval hosts’ body cavity. The venom contains discrete, 300 nm-wide, mixed-strategy extracellular vesicles (MSEVs), until recently referred to as virus-like particles. While the crucial immune suppressive functions of L. heterotoma MSEVs have remained undisputed, their biotic nature and origin still remain controversial. In recent proteomics analyses of L. heterotoma MSEVs, we identified 161 proteins in three classes: conserved eukaryotic proteins, infection and immunity related proteins, and proteins without clear annotation. Here we report 246 additional proteins from the L. heterotoma MSEV proteome. An enrichment analysis of the entire proteome supports vesicular nature of these structures. Sequences for more than 90% of these proteins are present in the whole-body transcriptome. Sequencing and de novo assembly of the 460 Mb-sized L. heterotoma genome revealed 90% of MSEV proteins have coding regions within the genomic scaffolds. Altogether, these results explain the stable association of MSEVs with their wasps, and like other wasp structures, their vertical inheritance. While our results do not rule out a viral origin of MSEVs, they suggest that a similar strategy for co-opting cellular machinery for immune suppression may be shared by other wasps to gain advantage over their hosts. These results are relevant to our understanding of the evolution of figitid and related wasp species.

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Rapid Viral Symbiogenesis via Changes in Parasitoid Wasp Genome Architecture

Cited by 44 publications

References 61 publications

Endogenization from diverse viral ancestors is common and widespread in parasitoid wasps

Endogenization from diverse viral ancestors is common and widespread in parasitoid wasps

Chromosomal resolution reveals symbiotic virus colonization of parasitic wasp genomes

Immune Suppressive Extracellular Vesicle Proteins ofLeptopilina heterotomaAre Encoded in the Wasp Genome

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