Two Complete Genomes of Male-Killing Wolbachia Infecting Ostrinia Moth Species Illuminate Their Evolutionary Dynamics and Association with Hosts

Abstract

Wolbachia is an extremely widespread intracellular symbiont which causes reproductive manipulation on various arthropod hosts. Male progenies are killed in Wolbachia-infected lineages of the Japanese Ostrinia moth population. While the mechanism of male killing and the evolutionary interaction between host and symbiont are significant concerns for this system, the absence of Wolbachia genomic information has limited approaches to these issues. We determined the complete genome sequences of wFur and wSca, the male-killing Wolbachia of Ostrinia furnacalis and Ostrinia scapulalis. The two genomes shared an extremely high degree of homology, with over 95% of the predicted protein sequences being identical. A comparison of these two genomes revealed nearly minimal genome evolution, with a strong emphasis on the frequent genome rearrangements and the rapid evolution of ankyrin repeat-containing proteins. Additionally, we determined the mitochondrial genomes of both species’ infected lineages and performed phylogenetic analyses to deduce the evolutionary dynamics of Wolbachia infection in the Ostrinia clade. According to the inferred phylogenetic relationship, two possible scenarios were proposed: (1) Wolbachia infection was established in the Ostrinia clade prior to the speciation of related species such as O. furnacalis and O. scapulalis, or (2) Wolbachia infection in these species was introgressively transferred from a currently unidentified relative. Simultaneously, the relatively high homology of mitochondrial genomes suggested recent Wolbachia introgression between infected Ostrinia species. The findings of this study collectively shed light on the host-symbiont interaction from an evolutionary standpoint.

Complete De Novo Assembly of Wolbachia Endosymbiont of Frankliniella intonsa

“…The presence of the irregular GC skew in wFI, meant that there was no obvious GC skew to identify a possible origin of replication, which also suggested that wFI may have undergone frequent rearrangements. This abnormal GC skew pattern has also been observed in other Wolbachia genomes [35][36][37][38][39]. However, it has been observed that Wolbachia with reduced genomes exhibit a strong GC skew [40].…”

Cell-based assays and comparative genomics revealed the conserved and hidden effects ofWolbachiaon insect sex determination

“…wSca] and Ec-Oscar [wCauA]) and Type II Oscar (Hm-Oscar [wHm-t] and Em/Eh-Oscar [wFem]; Figure 2C). Whereas Oscar in the newly sequenced wSca strain was not identical to that in the previously sequenced wSca strain (43), it exhibited high homology to Oscar proteins in the previously sequenced wSca (similarity: 90.4% in 1797 amino acids; bit score: 3241, BLASTp) and wFur (similarity: 94.2% in 1830 amino acids; bit score: 3432) (Table S1). Intriguingly, the Type II Oscar homologs Hm-Oscar and Em-Oscar exhibited higher homology than the wSca strains (similarity: 98.5% in 1181 amino acids; bit score: 2362).…”

Two male-killing Wolbachia from Drosophila birauraia that are closely related but distinct in genome structure

“…For example, the MK Wolbachia strain, w Hm-t, is thought to have evolved from its closely related non-MK strain, w Hm-c, in the tea tortrix, Homona magnanima , by acquiring an MK-associated prophage region [ 18 ]. By contrast, Ostrinia furnacalis and Ostrinia scapulalis harbour closely related MK Wolbachia strains that show an extremely high degree of genomic similarity to several inversions [ 19 ]. The MK Wolbachia strains in Ostrinia moths are thought to have descended from their common ancestral hosts and have maintained a stable genome structure throughout their evolution [ 19 ].…”

“…By contrast, Ostrinia furnacalis and Ostrinia scapulalis harbour closely related MK Wolbachia strains that show an extremely high degree of genomic similarity to several inversions [ 19 ]. The MK Wolbachia strains in Ostrinia moths are thought to have descended from their common ancestral hosts and have maintained a stable genome structure throughout their evolution [ 19 ]. In the highly host-dependent symbiotic bacterium, Wolbachia , substantial changes in the genome structure can disrupt phenotypic expression and intergenic interactions, posing major risks to Wolbachia fitness.…”