Dynamic effects of Wolbachia on Drosophila Oogenesis and coordination of infection with stem cell niche morphogenesis
Wolbachia are widespread obligate intracellular bacteria that are maternally transmitted and modulate reproduction of their invertebrate host. Mosquitoes transinfected with Wolbachia have reduced capacity for transmitting vector borne diseases and can replace native populations in the field because of a reproductive advantage. The cellular mechanisms of how reproduction is altered by Wolbachia are poorly understood. In this work Wolbachia-induced reproductive changes in the model organism Drosophila were used to pinpoint underlying cellular processes affected by the bacteria. Specifically, egg production (or fecundity) of Wolbachia-infected Drosophila mauritiana was compared to non-infected flies that had been generated by antibiotic treatment of infected flies. Immediately before the fecundity experiment backcrossing of both fly lines ensured an equivalent nuclear genetic background. Initially egg production in Wolbachia-infected flies was increased by 4-fold but in less than 30 generations this changed to a 0.84 fold decrease with a slight advantage for the non-infected line. Additional backcrossing experiments determined that selection on the host nuclear genome is one of the factors underlying this reversion of fecundity gains. Other non-Mendelian factors, such as the microbiota, may also play a role in this rapid change. Wolbachia alterations in egg production were always linked to Wolbachia induced changes in programmed cell death (PCD) in the germarium during oogenesis and germline stem cell (GSC) division. Germline stem cells are maintained and regulated through their interaction with the germline stem cell niche (GSCN). Interestingly, these cells are both frequently infected with Wolbachia and possess a high bacterial titer. A developmental time course revealed the mechanism of how Wolbachia accumulate in the niche cells. The data suggest that the bacteria actually coordinate their replication with the differentiation of the niche cells. Future work on understanding the cellular and molecular basis of Wolbachia - host interaction will not only give insight into novel mechanisms of host manipulation by a pathogen, but will also expand our current understanding of stem cell niche morphogenesis and modulation of stem cell proliferation.