Distinct epigenomic and transcriptomic modifications associated with Wolbachiamediated asexuality

Xin Wu, Amelia R.I. Lindsey, Paramita Chatterjee, John H. Werren, Richard Stouthamer, Soojin V. Yi

Research output: Contribution to journalArticlepeer-review

2 Scopus citations

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 begin to reveal distinct genes and molecular pathways subject to Wolbachia induced epigenetic modification and/or host responses to Wolbachia-infection.

Original languageEnglish (US)
Article numbere1008397
JournalPLoS pathogens
Volume16
Issue number3
DOIs
StatePublished - 2020
Externally publishedYes

Bibliographical note

Funding Information:
This work was supported by the National Science Foundation (DEB 1501227 to ARIL, and MCB 1615664 to SVY) the United States Department of Agriculture (NIFA 194617 to RS and NIFA 2016-67011-24778 to ARIL); and Robert and Peggy van den Bosch Memorial Scholarships to ARIL. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

PubMed: MeSH publication types

  • Journal Article
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

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