Distinct epigenomic and transcriptomic modifications associated with Wolbachia-mediated asexuality

Abstract

Wolbachia are maternally transmitted intracellular bacteria that induce a range of pathogenic and fitness-altering effects on insect and nematode hosts. In parasitoid wasps of the genus Trichogramma, Wolbachia infection induces asexual production of females, thus increasing transmission of Wolbachia. It has been hypothesized that Wolbachia infection accompanies a modification of the host epigenome. However, to date, data on genomewide epigenomic changes associated with Wolbachia are limited, and are often confounded by background genetic differences. Here, we took sexually reproducing Trichogramma free of Wolbachia and introgressed their genome into a Wolbachia-infected cytoplasm, converting them to Wolbachia-mediated asexuality. Wolbachia was then cured from replicates of these introgressed lines, allowing us to examine the genome-wide effects of wasps newly converted to asexual reproduction while controlling for genetic background. We thus identified gene expression and DNA methylation changes associated with Wolbachia-infection. We found no overlaps between differentially expressed genes and differentially methylated genes, indicating that Wolbachia-infection associated DNA methylation change does not directly modulate levels of gene expression. Furthermore, genes affected by these mechanisms exhibit distinct evolutionary histories. Genes differentially methylated due to the infection tended to be evolutionarily conserved. In contrast, differentially expressed genes were significantly more likely to be unique to the Trichogramma lineage, suggesting host-specific transcriptomic responses to infection. Nevertheless, we identified several novel aspects of Wolbachia-associated DNA methylation changes. Differentially methylated genes included those involved in oocyte development and chromosome segregation. Interestingly, Wolbachia-infection was associated with higher levels of DNA methylation. Additionally, Wolbachia infection reduced overall variability in gene expression, even after accounting for the effect of DNA methylation. We also identified specific cases where alternative exon usage was associated with DNA methylation changes due to Wolbachia infection. These results

Dnmt1a is essential for gene body methylation and the regulation of zygotic genome activation in the wasp

“…The strong correlation of methylated genes with down-regulation after Nv-Dnmt1a pRNAi fits well with previous observations that methylated genes are more highly and stably expressed than non-methylated genes in insects 19,36,45 .…”

Wolbachia and Sirtuin-4 interaction is associated with alterations in host glucose metabolism and bacterial titer

“…Another potential explanation is that the observed differences are due to epigenetic changes. Recent work in parasitoid wasps observed a series of host genes that were differently methylated in the presence of Wolbachia [ 64 ], similarly to what has been reported in Aedes aegypti mosquitoes infected with the w MelPop strain [ 65 ] and the reproductive tissues of male Drosophila infected with w Mel [ 66 ]. Both represent intriguing hypotheses to be tested in future studies.…”

Wolbachiaand virus alter the host transcriptome at the interface of nucleotide metabolism pathways

“…One of the major findings across our analyses is the significant amount of differential isoform usage due to Wolbachia, virus, and the combination of the two. The first evidence of Wolbachia having effects on host splicing and/or isoform usage was recently reported in a parasitoid wasp (Wu et al, 2020), and splicing is becoming increasingly appreciated as an important component (which was not certified by peer review) is the author/funder. All rights reserved.…”