How do Wolbachia modify the Drosophila ovary? New evidences support the “titration-restitution” model for the mechanisms of Wolbachia-induced CI

Abstract

Background Cytoplasmic incompatibility (CI) is the most common phenotype induced by endosymbiont Wolbachia and results in embryonic lethality when Wolbachia -modified sperm fertilize eggs without Wolbachia . However, eggs carrying the same strain of Wolbachia can rescue this embryonic death, thus producing viable Wolbachia -infected offspring. Hence Wolbachia can be transmitted mainly by hosts’ eggs. One of the models explaining CI is “titration-restitution”, which hypothesized that Wolbachia titrated-out some factors from the sperm and the Wolbachia in the egg would restitute the factors after fertilization. However, how infected eggs rescue CI and how hosts’ eggs ensure the proliferation and transmission of Wolbachia are not well understood. Results By RNA-seq analyses, we first compared the transcription profiles of Drosophila melanogaster adult ovaries with and without the w Mel Wolbachia and identified 149 differentially expressed genes (DEGs), of which 116 genes were upregulated and 33 were downregulated by Wolbachia infection. To confirm the results obtained from RNA-seq and to screen genes potentially associated with reproduction, 15 DEGs were selected for quantitative RT-PCR (qRT-PCR). Thirteen genes showed the same changing trend as RNA-seq analyses. To test whether these genes are associated with CI, we also detected their expression levels in testes. Nine of them exhibited different changing trends in testes from those in ovaries. To investigate how these DEGs were regulated, sRNA sequencing was performed and identified seven microRNAs (miRNAs) that were all upregulated in fly ovaries by Wolbachia infection. Matching of miRNA and mRNA data showed that these seven miRNAs regulated 15 DEGs. Wolbachia -responsive genes in fly ovaries were involved in biological processes including metabolism, transportation, oxidation-reduction, immunity, and development. Conclusions Comparisons of mRNA and miRNA data from fly ovaries revealed 149 mRNAs and seven miRNAs that exhibit significant changes in expression due to Wolbachia infection. Notably, most of the DEGs showed variation in opposite directions in ovaries versus testes in the presence of Wolbachia , which generally supports the “titration-restitution” model for CI. Furthermore, genes related to metabolism were upregulated, which may benefit maximum proliferation and transmission of Wolbachia . This provides new insights into the molecular mechanisms of Wolbachia -induced CI and ...

Symbiont-mediated cytoplasmic incompatibility: What have we learned in 50 years?

“…When differential expression is correlated with CI phenotypes, these data can yield valuable insights regarding CI’s mechanism. Significant correlations between Wolbachia symbiont state and host expression have been measured in D. melanogaster ( Biwot et al, 2020 ; He et al, 2019 ; LePage et al, 2014 ; Liu et al, 2014 ; Ote et al, 2016 ; Xi et al, 2008 ; Yuan et al, 2015 ; Zheng et al, 2019b ; Zheng et al, 2011 ), D. simulans ( Brennan et al, 2012 ; Clark et al, 2006 ; Xi et al, 2008 ), La. striatellus ( Huang et al, 2019 ; Ju et al, 2017 ; Liu et al, 2019 ), T. urticae ( Bing et al, 2020a ; Zhang et al, 2015 ) , Cu.…”

Association of Wolbachia with Gene Expression in Drosophila Testes

“…Over the past decade, RNA-seq has become an essential technique in transcriptomic studies, and Gutzwiller et al used RNA-seq to study the dynamic expression of Wolbachia genes during the life cycle of Drosophila melanogaster (D. mel), which provided a rich set of resources to further explore the functional basis of Wolbachia-Drosophila symbiosis [15]. He et al analyze the ovaries of Wolbachiainfected and uninfected Drosophila adults and found that Wolbachia signi cantly affected many metabolic pathways, such as starch and sucrose metabolism, the TGF-β signaling pathway, galactose metabolism, the Wnt signaling pathway, and ubiquitin-mediated proteolysis [16]. RNA-seq is also used to study Wolbachia and host gene expression pro le in other species, such as nematodes and spider mites [17][18][19].…”

Dual proteomics of Drosophila melanogaster hemolymph infected with the heritable endosymbiont Spiroplasma poulsonii

“…It is upregulated in cells harboring intracellular symbionts in weevils, presumably to increase protein turnover and provide free amino-acids to the bacteria (Heddi et al, 2005). In vitro work on cell cultures infected by the facultative endosymbiont Wolbachia also revealed that it induces the host proteasome presumably also to support its own growth (Fallon and Witthuhn, 2009; He et al, 2019; White et al, 2017). Remarkably, one proteasome subunit was detected as enriched upon Spiroplasma infection in the aphid Aphis citricidus when the insect was feeding on a suboptimum but not on an optimum host plant, suggesting an interaction between symbiosis, nutrition and the proteasome-ubiquitin degradation system (Guidolin et al, 2018).…”