Abstract
The alphaproteobacterium Wolbachia pipientis infects arthropod and nematode species worldwide, making it a key target for host biological control. Wolbachia-driven host reproductive manipulations, such as cytoplasmic incompatibility (CI), are credited for catapulting these intracellular bacteria to high frequencies in host populations. Positive, perhaps mutualistic, reproductive manipulations also increase infection frequencies, but are not well understood. Here, we identify molecular and cellular mechanisms by which Wolbachia influences the molecularly distinct processes of GSC self renewal and differentiation. We demonstrate that wMel infection rescues the fertility of flies lacking the translational regulator mei-P26, and is sufficient to sustain infertile homozygous mei-P26-knockdown stocks indefinitely. Cytology revealed that wMel mitigates the impact of mei-P26 loss through restoring proper pMad, Bam, Sxl, and Orb expression. In OreR files with wild-type fertility, wMel infection elevates lifetime egg hatch rates. Exploring these phenotypes through dual-RNAseq experiments revealed that wMel infection rescues and offsets many gene expression changes induced by mei-P26 loss at the mRNA level. Overall, we show that wMel infection beneficially reinforces host fertility at mRNA, protein, and phenotypic levels, and these mechanisms may promote the emergence of mutualism and the breakdown of host reproductive manipulations.
Graphical Abstract
Highlights
● The wMel strain of Wolbachia restores fertility in females and males deficient for the essential translational regulator meiotic-P26
● Mei-P26’s germline maintenance and oocyte cyst differentiation functions are genetically rescued by wMel infection
● Perturbed pMad, Sxl, Bam, and Orb protein expression are mitigated by wMel infection
● wMel infection elevates lifetime egg lay and hatch rates in OreR flies
● Ovary transcriptomes reveal wMel infection restores or offsets changes in gene expression induced by the loss of functional mei-P26
Significance Statement Wolbachia bacterial symbionts are being harnessed as biological control agents through the use of their costly manipulations to host fertility. Here, we reveal that the wMel strain can have a beneficial impact on fruit fly development in both mutant and wild-type flies. This phenotype is essential to the long-term use of these bacteria for host population control.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
These edits represent the outcome of the first round of revision, following three reviewers' and one editor's comments. The dualRNAseq assay was added to address the reviewer question about the extent of mei-P26 knockdown with our mutant flies. Since much more data were generated than that, we performed a full differential expression analysis.
