Chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization

Abstract

Endogenous viruses form an important proportion of eukaryote genomes and a source of novel functions. How large DNA viruses integrated into a genome evolve when they confer a benefit to their host, however, remains unknown. Bracoviruses are essential for the parasitism success of parasitoid wasps, into whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome at a chromosomal scale, that bracovirus genes colonized all ten chromosomes of Cotesia congregata. Most form clusters of genes involved in particle production or parasitism success. Genomic comparison with another wasp, Microplitis demolitor, revealed that these clusters were already established ~53 mya and thus belong to remarkably stable genomic structures, the architectures of which are evolutionary constrained. Transcriptomic analyses highlight temporal synchronization of viral gene expression without resulting in immune gene induction, suggesting that no conflicts remain between ancient symbiotic partners when benefits to them converge.

Genome-Wide Patterns of Bracovirus Chromosomal Integration into Multiple Host Tissues during Parasitism

“…Polydnavirus genomes within parasitoid wasps (Hymenoptera) are composed of domesticated viral genes and genes of different origins involved in virulence ( 1 – 3 ). The domesticated viruses encode viral particles akin to gene transfer agents, which are injected during oviposition into the lepidopteran hosts of parasitoid wasps and are necessary for successful development of the wasp larvae.…”

“…The products of these genes form viral particles containing virulence genes ( 2 , 16 ). Although the evolutionary origin of virulence genes has in most cases not been uncovered, some are clearly of wasp origin ( 17 , 18 ), while others derive from transposable elements (TEs) ( 3 , 19 ). They are located on so-called proviral segments dispersed in multiple chromosomal regions in the wasp’s genome ( 13 , 20 ); the major one, named the macrolocus, spans 2 Mb and includes two-thirds of the proviral segments.…”

“…They are located on so-called proviral segments dispersed in multiple chromosomal regions in the wasp’s genome ( 13 , 20 ); the major one, named the macrolocus, spans 2 Mb and includes two-thirds of the proviral segments. Chromosome-scale assembly of the genome of Cotesia congregata (Microgastrinae) revealed that it contains 10 proviral loci (PL), each made of 1 to 18 proviral segments (PL2, 18 segments [ 3 ]). Comparisons between Cotesia species and Microplitis demolitor showed that the synteny of these PL is well conserved along the phylogeny of Braconidae in ∼53 million years of evolution, suggesting strong evolutionary constraints associated with the function of the segments.…”

Proteo-Trancriptomic Analyses Reveal a Large Expansion of Metalloprotease-Like Proteins in Atypical Venom Vesicles of the Wasp Meteorus pulchricornis (Braconidae)

“…Finally, we used the TransDecoder.Predict algorithm with the retain.blastp option with the DIAMOND results. Orthologs were identified by OrthoFinder (v2.3.8) [ 96 ] with the -S DIAMOND option and a database already built for previous analyses [ 97 ] and supplemented with the proteomes of C. Congregata [ 13 ], A. ervi and L. fabarum [ 98 ], and with the predicted peptides of M. puchricornis , B. nigricans , L. javana , P. turionellae , and P. concolor (see Table S2 ). Gene functions were obtained after a BLASTp of predicted peptides against NCBI NR (NR.2020-5-29) with DIAMOND (v2.0.6) and the arguments: --evalue 1e-8 --max-target-seqs 10 --masking 0, and InterProScan (v5.42-78) [ 99 ] with the options: -iprlookup -goterms --pathways -f xml -dp.…”

“…Virus-like particles produced in the calyx of female ovaries have been extensively studied in ichneumonid and braconid wasps. In these species, the particles are produced by viral machineries imbedded in wasp chromosomes as a result of virus genome integration events that occurred during wasp evolution [ 8 , 9 , 10 , 11 , 12 , 13 ]. These parasitoid ovarian particles contain either DNA molecules or proteins, and they originate from independent integration events.…”