Biology subjects

Ravallec, M.

Publications and source records attributed to Ravallec, M..

4 recordsLinked to original sources

bioRxiv2024

Identification of a viral gene essential for the genome replication of a domesticated endogenous virus in ichneumonid parasitoid wasps

Thousands of endoparasitoid wasp species in the families Braconidae and Ichneumonidae harbor "domesticated endogenous viruses" (DEVs) in their genomes. This study focuses on ichneumonid DEVs, named ichnoviruses (IVs), which derive from an unknown virus and produce virions in ovary calyx cells during the pupal and adult stages of female wasps. Females inject IV virions into host insects when laying eggs. Virions infect cells which express IV genes with functions required for wasp progeny development. IVs have a dispersed genome consisting of two genetic components: proviral segment loci that serve as templates for circular dsDNAs that are packaged into capsids, and genes from an ancestral virus controlling virion production. Because of the lack of homology with known viral genes, the molecular control mechanisms of IV genome are largely uncharacterized. We generated a chromosome-scale genome assembly for Hyposoter didymator and identified a total of 67 H. didymator ichnovirus (HdIV) loci distributed across the 12 wasp chromosomes. By analyzing genomic DNA levels, we found that all HdIV loci were locally amplified in calyx cells during the wasp pupal stage, suggesting the implication of viral proteins in DNA replication. We tested a candidate HdIV gene, U16, encoding a protein with a conserved domain found in primases and which is transcribed in calyx cells during the initial stages of replication. Knockdown of U16 by RNA interference inhibited amplification of all HdIV loci, as well as HdIV gene transcription, circular molecule production and virion morphogenesis in calyx cells. Altogether, our results showed that viral DNA amplification is an early step of IV replication essential for virions production, and demonstrated the implication of the viral gene U16 in this process. Author SummaryParasitoid "domesticated endogenous viruses" (DEVs) provide a fascinating example of eukaryotes acquiring new functions through integration of a virus genome. DEVs consist of multiple loci in the genomes of wasps. Upon activation, these elements collectively orchestrate the production of virions or virus-like particles that are crucial for successful parasitism of host insects. Despite the significance of DEVs for parasitoid biology, the mechanisms regulating key steps in virion morphogenesis are largely unknown. In this study, we focused on the ichneumonid parasitoid Hyposoter didymator, which harbors an ichnovirus consisting of 67 proviral loci. Our findings reveal that all proviral loci are simultaneously amplified in ovary calyx cells of female wasps during the early pupal stage suggesting a hijacking of cellular replication complexes by viral proteins. We tested the implication of such a candidate, U16, encoding a protein with a weakly conserved primase C-terminal domain. Silencing U16 resulted in inhibited viral DNA amplification and virion production, underscoring the key role of this gene for ichnovirus replication. This study provides evidence that genes involved in viral DNA replication have been conserved during the domestication of viruses in the genomes of ichneumonid wasps.

microbiology↗

bioRxiv2019

Conserved and specific genomic features of endogenous polydnaviruses revealed by whole genome sequencing of two ichneumonid wasps

Polydnaviruses (PDVs) are mutualistic endogenous viruses associated with some lineages of parasitoid wasps that allow successful development of the wasps within their hosts. PDVs include two taxa resulting from independent virus acquisitions in braconid (bracoviruses) and ichneumonid wasps (ichnoviruses). PDV genomes are fully incorporated into the wasp genomes and comprise (1) virulence genes located on proviral segments that are packaged into the viral particle, and (2) genes involved in the production of the viral particles, which are not encapsidated. Whereas the genomic organization of bracoviruses within the wasp genome is relatively well known, the architecture of endogenous ichnoviruses remains poorly understood. We sequenced the genome of two ichnovirus-carrying wasp species, Hyposoter didymator and Campoletis sonorensis. Complete assemblies with long scaffold sizes allowed identification of the integrated ichnovirus, highlighting an extreme dispersion within the wasp genomes of the viral loci, i.e. isolated proviral segments and clusters of replication genes. Comparing the two wasp species, proviral segments harbor distinct gene content and variable genomic environment, whereas viral machinery clusters show conserved gene content and order, and can be inserted in collinear wasp genomic regions. This distinct architecture is consistent with the biological properties of the two viral elements: proviral segments producing virulence proteins allowing parasitism success are fine-tuned to the host physiology, while an ancestral viral architecture was likely maintained for the genes involved in virus particle production. Finding a distinct genomic architecture of ichnoviruses and bracoviruses highlights different evolutionary trajectories leading to virus domestication in the two wasp lineages.

genomics↗

bioRxiv2018

Sharing cells with Wolbachia: the transovarian vertical transmission of Culex pipiens densovirus

Originality-Significance StatementThis contribution provides a window into the study of a densovirus called CpDV infecting Culex pipiens mosquitoes. The originality of the study lies in the fact that CpDV, a DNA virus, was to date almost unstudied, its interaction with its hosts and its transmission mode were unknown. Considering that all Cx. pipiens are infected with Wolbachia, we studied the influence of this bacterial endosymbiont on CpDV density and transmission. Although Wolbachia-RNA virus interactions, especially in non-native Wolbachia-host associations have been widely studied, Wolbachia-DNA virus interactions were rarely investigated.\n\nIn this natural tripartite Cx. pipiens-Wolbachia-CpDV system: O_LIWe revealed the wide prevalence of CpDV, mostly at low densities, in Cx. pipiens laboratory lines.\nC_LIO_LIWe monitored CpDV presence in several cell types in ovaries including the oocytes where they co-exist with the bacterial endosymbiont Wolbachia.\nC_LIO_LIWe demonstrated that CpDV density in ovaries was influenced by Wolbachia presence and strain variations\nC_LIO_LIWe studied CpDV vertical transmission depending on Wolbachia presence and strain variations\nC_LI\n\nWe report for the first time the occurrence of widely distributed covert CpDV infections in Cx. pipiens laboratory colonies. CpDV is maintained by both vertical and horizontal transmission and under the influence of the vertically transmitted bacterial endosymbiont Wolbachia. Taken together our results suggest that CpDV could be very prevalent in nature putatively influencing natural Cx. pipiens populations dynamics.\n\nSUMMARYCulex pipiens densovirus (CpDV), a single stranded DNA virus, has been isolated from Culex pipiens mosquitoes but differs from other mosquito densoviruses in terms of genome structure and sequence identity. Its transmission from host to host, the nature of its interactions with both its host and hosts endosymbiotic bacteria Wolbachia are not known. Here we report the presence of CpDV in the ovaries and eggs of Cx. pipiens mosquitoes in close encounters with Wolbachia. In the ovaries, CpDV quantity significantly differed between mosquito lines harboring different strains of Wolbachia and these differences were not linked to variations in Wolbachia densities. CpDV was vertically transmitted in all laboratory lines to 17%-20% of the offspring. For some females, however, the vertical transmission reached 90%. Antibiotic treatment that cured the host from Wolbachia also significantly affected both CpDV quantity and vertical transmission suggesting an impact of host microbiota, including Wolbachia, on CpDV transmission. Overall our results show that CpDV is transmitted vertically via transovarian path along with Wolbachia with which it shares the same cells. Our results are primordial to understand the dynamics of densovirus infection, their persistence and spread in populations considering their potential use in the regulation of mosquito vector populations.

microbiology↗

bioRxiv2018

Immuno-suppressive Virus-like particles of Drosophila parasitoids derive from the domestication of a behaviour-manipulating virus relative

To circumvent host immune response, some hymenopteran endo-parasitoids produce virus-like structures in their reproductive apparatus that are injected into the host together with the eggs. These viral-like structures are absolutely necessary for the reproduction of these wasps. The viral evolutionary origin of these viral-like particles has been demonstrated in only a few cases of wasp species all belonging to the Ichneumonoidea superfamily. In addition, the nature of the initial virus-wasp association remains unknown for all. This is either because no closely related descendant infects the wasps, because it has not been sampled yet, or because the virus lineage went extinct. In this paper, we show that the virus-like particles (VLPs) produced by endoparasitoids of Drosophila belonging to the Leptopilina genus (superfamily Cynipoidea) do have a viral origin, solving the debate on their origin. Furthermore, the ancestral donor virus still has close relatives infecting one of the wasp species, thus giving us insights on the ecological interaction that possibly allowed the domestication process. Intriguingly, this contemporary virus is both vertically and horizontally transmitted and has the particularity to manipulate the superparasitism behavior of the wasp. This raises the possibility that behavior manipulation has been instrumental in the birth of such association between wasps and viruses.

evolutionary biology↗