Genomic Architecture of Endogenous Ichnoviruses Reveals Distinct

Legeai et al. BMC Biology (2020) 18:89 https://doi.org/10.1186/s12915-020-00822-3 RESEARCH ARTICLE Open Access Genomic architecture of endogenous ichnoviruses reveals distinct evolutionary pathways leading to virus domestication in parasitic wasps Fabrice Legeai1,2†, Bernardo F. Santos3†, Stéphanie Robin1,2†, Anthony Bretaudeau1,2, Rebecca B. Dikow3,4, Claire Lemaitre2, Véronique Jouan5, Marc Ravallec5, Jean-Michel Drezen6, Denis Tagu1, Frédéric Baudat7, Gabor Gyapay8, Xin Zhou9, Shanlin Liu9,10, Bruce A. Webb11, Seán G. Brady3 and Anne-Nathalie Volkoff5* Abstract Background: Polydnaviruses (PDVs) are mutualistic endogenous viruses inoculated by some lineages of parasitoid wasps into their hosts, where they facilitate successful wasp development. PDVs include the ichnoviruses and bracoviruses that originate from independent viral acquisitions in ichneumonid and braconid wasps respectively. PDV genomes are fully incorporated into the wasp genomes and consist of (1) genes involved in viral particle production, which derive from the viral ancestor and are not encapsidated, and (2) proviral segments harboring virulence genes, which are packaged into the viral particle. To help elucidating the mechanisms that have facilitated viral domestication in ichneumonid wasps, we analyzed the structure of the viral insertions by sequencing the whole genome of two ichnovirus-carrying wasp species, Hyposoter didymator and Campoletis sonorensis. Results: Assemblies with long scaffold sizes allowed us to unravel the organization of the endogenous ichnovirus and revealed considerable dispersion of the viral loci within the wasp genomes. Proviral segments contained species-specific sets of genes and occupied distinct genomic locations in the two ichneumonid wasps. In contrast, viral machinery genes were organized in clusters showing highly conserved gene content and order, with some loci located in collinear wasp genomic regions. This genomic architecture clearly differs from the organization of PDVs in braconid wasps, in which proviral segments are clustered and viral machinery elements are more dispersed. Conclusions: The contrasting structures of the two types of ichnovirus genomic elements are consistent with their different functions: proviral segments are vehicles for virulence proteins expected to adapt according to different host defense systems, whereas the genes involved in virus particle production in the wasp are likely more stable and may reflect ancestral viral architecture. The distinct genomic architectures seen in ichnoviruses versus bracoviruses reveal different evolutionary trajectories that have led to virus domestication in the two wasp lineages. Keywords: Endogenous virus architecture, Polydnavirus, Parasitoid wasp, Koinobiont, Campopleginae, IVSPERs * Correspondence: [email protected] Fabrice Legeai, Bernardo F. Santos and Stéphanie Robin are Co-first authors. 5DGIMI, INRAE, University of Montpellier, 34095 Montpellier, France Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Legeai et al. BMC Biology (2020) 18:89 Page 2 of 23 Background subfamilies are estimated to carry these mutualistic vi- Parasites and their hosts are involved in a continual co- ruses [18, 19]. Ichnoviruses descend from the integration evolutionary arms race, with hosts evolving defense of a virus of unknown origin [16] and are found in two mechanisms and parasites developing strategies to over- distantly related ichneumonid subfamilies, the Campo- come them [1, 2]. Identifying the genomic basis of such pleginae and the Banchinae [20], which together com- adaptations is crucial to understand the evolutionary dy- prise over 3860 species [21]. Whether ichnoviruses in namics of host-parasite interactions [3], with cycles of these two subfamilies result from a single virus integra- adaptation and counter-adaptation often resulting in tion or two independent events involving related viruses complex biological strategies with far-reaching conse- remains unclear [20]. At least one campoplegine, Ven- quences at the genomic level. The use of endogenous vi- turia canescens, has lost its PDVs and instead produces ruses by parasitoid wasps provides an example of how virus-like particles devoid of DNA deriving from a third complex host-parasite interactions can lead to specific event of virus integration that occurred in this lineage genomic adaptations. [22]. Parasitoid wasps are among the most successful Following integration, viral sequences retained in the groups of parasitic organisms, potentially comprising wasp genome underwent rearrangements leading to the several hundred thousand species and playing major present genomic architecture of bracoviruses and ichno- ecological roles in terrestrial ecosystems [4]. While the viruses. The integrated PDV genomes include two types adult wasps are free-living, during their immature stages of functional components [15, 23, 24]. The first type, they develop as parasites of other arthropods, eventually hereinafter called “proviral segments,” corresponds to se- killing their host. Parasitoid wasps have diverse bio- quences that serve as templates for the PDV segments logical strategies, and many groups develop inside a host packaged within the particles. Proviral segments exhibit that remains active after being parasitized (koinobiont direct repeated sequence at their extremities (“direct re- endoparasitoids). In order to survive within a developing peat junctions,” or DRJs) that allow homologous recom- organism, some lineages of parasitic wasps have evolved bination and generation of the circular molecule [25, strategies to manipulate their host by employing mutual- 26]. The packaged DNA segments of several PDVs have istic viruses from the Polydnaviridae (PDVs) family. PDV been sequenced, revealing that their content differs be- particles are produced exclusively within the calyx re- tween bracoviruses and ichnoviruses (reviewed in [6]). gion of the ovary during female wasp pupation and PDV segments encode virulence genes that will be adulthood. Particles enclose a packaged genome com- expressed in the parasitoid’s host; no typical virus repli- posed of several circular molecules, or “segments,” of cation genes have been identified in PDV packaged ge- double-stranded DNA. Mature virions are secreted into nomes. Although considered as part of the PDV the oviduct and transferred into the host, usually a cater- genome, they probably consist of a mosaic of sequences pillar, during oviposition. Once inside the host, PDVs do from various organismic backgrounds (ancestral virus, not replicate but express genes that induce profound insect host, and others still unknown) [27]. The second physiological alterations in the parasitized host, such as type of PDV endogenous sequences, hereafter “replica- impairment of the immune response or developmental tion genes,” are those involved in the production of the alterations, which are required for successful develop- PDV particles. They are expressed exclusively in the ment of the wasp larva [5–9]. wasp calyx cells during the process of PDV production Two groups of PDVs have been reported, associated [16, 17, 28]), but in contrast with viral segments, are not with the hyperdiverse sister wasp families Braconidae packaged in the viral particles. (bracoviruses) and Ichneumonidae (ichnoviruses) [10, Knowledge on PDV genomic architecture is currently 11]. In both cases, PDVs persist in all cells of the wasp focused on bracoviruses, based on whole genome se- as integrated sequences (provirus), allowing the vertical quencing of PDV-carrying braconid wasps [16, 24]. In transfer of the PDV genetic material [12, 13]. Bracov- braconid genomes, most viral segments are located in iruses and ichnoviruses differ in their morphology and clusters which may comprise up to 18 segments [15, 23, gene content but share the life cycle described above 29] organized in tandem arrays and separated by regions [14]. Each PDV group derives from the genomic integra- of intersegmental DNA that are not encapsidated. This tion of a different virus during the evolution of braconid organization leads to a particular mode of replication of and ichneumonid lineages [15, 16]: the independent ori- the bracovirus segments in the wasp calyx cells. They gin of these two groups of PDVs illustrates an astonish- are first amplified within replication units encompassing ing example of convergent evolution. Bracoviruses, several

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