Bacterial and fungal symbionts in parasitoid wasp genera Nasonia and Muscidifurax

Abstract

Jewel wasps in the genus of Nasonia are ideal models for insect genetics, genomics, epigenetics, development, and evolution. Wasps in the Muscidifurax genus have a close evolutionary relationship to the model parasitoid genus Nasonia. Muscidifurax raptorellus (M. raptorellus) has received extensive attention for its potential in biological control against filth flies. We reported the first de novo Ng assembly (259 Mbp) and M. raptorellus assembly (314 Mbp) with excellent continuity and completeness using 10× Genomics sequencing and PacBio long-read sequencing technologies. Nasonia has been an excellent model for intracellular bacteria Wolbachia research, with 11 Wolbachia strains identified in four Nasonia species. Phylogenomic analyses with 210 identified core genes indicated that all 33 Wolbachia strains maintained the supergroup relationship determined by multilocus sequence typing (MLST) genes. Fourteen inter-supergroup recombination events (9 A-B events and 5 A-E events) were discovered using an interclade recombination screening method in six genes (2.9%) among 210 single-copy orthologs, which suggested a relatively low frequency of intergroup recombination in Wolbachia. Nosema muscidifuracis (N. muscidifuracis) is a microsporidian parasite in the parasitoid wasps M. zaraptor and M. raptor. We reported a chromosome-level N. muscidifuracis genome (14.4 Mbp) with a novel composite 4-bp (TAGG)n and 5-bp (TTAGG)n telomeric repeat motif discovered at the ends of chromosomes. The genome exhibits extensive gene duplications and rearrangements, with high similarity in duplicated genes. Nosema titers remained high in Nosema-cured parasitoid wasps, suggesting incomplete infection elimination. Comparative phylogenomic analyses revealed incongruency in Nosema and host species trees, indicating a host switch event between parasitoid wasps and bees. A conserved cis-regulatory motif ACCC was identified upstream of the start codon. Cytogenetic analyses revealed a substantial Nosema load in wasp ovaries, suggesting heritable infection and vertical transmission. The tractability of the parasitoid-Nosema system makes it a potential model for the study of Nosemosis. Our study provides novel insights into the genetic architecture, gene regulation, and genome evolution of parasitoid wasps, Wolbachia endosymbionts, and fungal pathogen Nosema, which will build the foundation for the study of comparative genomics and host-parasite interactions in the parasitoid wasp Nasonia/Muscidifurax model system, as well as future biocontrol applications.