Comparative Genomics of Two Closely RelatedWolbachiawith Different Reproductive Effects on Hosts

Abstract

Wolbachia pipientis are obligate intracellular bacteria commonly found in many arthropods. They can induce various reproductive alterations in hosts, including cytoplasmic incompatibility, male-killing, feminization, and parthenogenetic development, and can provide host protection against some viruses and other pathogens. Wolbachia differ from many other primary endosymbionts in arthropods because they undergo frequent horizontal transmission between hosts and are well known for an abundance of mobile elements and relatively high recombination rates. Here, we compare the genomes of two closely related Wolbachia (with 0.57% genome-wide synonymous divergence) that differ in their reproductive effects on hosts. wVitA induces a sperm–egg incompatibility (also known as cytoplasmic incompatibility) in the parasitoid insect Nasonia vitripennis, whereas wUni causes parthenogenetic development in a different parasitoid, Muscidifurax uniraptor. Although these bacteria are closely related, the genomic comparison reveals rampant rearrangements, protein truncations (particularly in proteins predicted to be secreted), and elevated substitution rates. These changes occur predominantly in the wUni lineage, and may be due in part to adaptations by wUni to a new host environment, or its phenotypic shift to parthenogenesis induction. However, we conclude that the approximately 8-fold elevated synonymous substitution rate in wUni is due to a either an elevated mutation rate or a greater number of generations per year in wUni, which occurs in semitropical host species. We identify a set of genes whose loss or pseudogenization in the wUni lineage implicates them in the phenotypic shift from cytoplasmic incompatibility to parthenogenesis induction. Finally, comparison of these closely related strains allows us to determine the fine-scale mutation patterns in Wolbachia. Although Wolbachia are AT rich, mutation probabilities estimated from 4-fold degenerate sites are not AT biased, and predict an equilibrium AT content much less biased than observed (57–50% AT predicted vs. 76% current content at degenerate sites genome wide). The contrast suggests selection for increased AT content within Wolbachia genomes.

Uncovering the hidden players in Lepidoptera biology: the heritable microbial endosymbionts

“…The genomes of many arthropod heritable endosymbionts have now been assembled, however very few of those sequenced are associated with Lepidoptera hosts. A comparative genomics approach can be used to elucidate endosymbiont evolution and function in its host including identifying candidate genes involved in reproductive manipulations such as CI (as in Drosophila (Sutton et al, 2014;LePage et al, 2017)), and parthenogenesis induction (in parasitoid wasps (Newton et al, 2016;Lindsey et al, 2016)). A recent comparison of 16 Wolbachia genomes identified a core Wolbachia genome of 496 sets of orthologous genes, 14 of which were unique to Wolbachia among the Rickettsiales bacteria, of which it is a member (Lindsey et al, 2016).…”

Transcriptome of Tetranychus urticae embryos reveals insights into Wolbachia‐induced cytoplasmic incompatibility

“…The mechanism by which Wolbachia induces CI has attracted considerable attention including multiple genomic comparisons and many elegant cytogenetic studies (Tram and Sullivan, 2002;Serbus et al, 2008;Newton et al, 2016). Recent studies have suggested that two adjacent Wolbachia genes (cidA/cifA and cidB/cifB) are involved in Wolbachia-mediated CI (Beckmann et al, 2017;LePage et al, 2017).…”

The Association of Wolbachia on the Gene Expression in Drosophila Adult Testis

“…For example, Wolbachia is necessary for nematode growth and development, as the adult worms were retarded, ovaries degenerated, and embryos could not form when Wolbachia was remove from nematodes by antibiotics [6]. In insect hosts, Wolbachia can increase the host's fertility [7][8][9][10][11], and enhance the insect host's resistance to many pathogens (such as RNA virus) [12][13][14]. Wolbachia can also provide vitamins to the host and give the host a clear growth advantage in the face of adversity [1,15].…”