Regulation of Wolbachia proliferation by the amplification and deletion of an addictive genomic island
Wolbachia is one of the most prevalent bacterial endosymbionts, infecting approximately 40% of terrestrial arthropod species. Wolbachia is often a reproductive parasite but can also provide fitness benefits to its host, as for example protection against viral pathogens. This protective effect is currently being applied to fight arboviruses transmission by releasing Wolbachia-transinfected mosquitoes. Titre regulation is a crucial aspect of Wolbachia biology.
Higher titres can lead to stronger phenotypes and fidelity of transmission but can have a cost to the host. Since Wolbachia is maternally transmitted, its fitness depends on host fitness, and, therefore, its cost to the host needs to be controlled. Understanding this and other aspects of Wolbachia biology has been hampered by the lack of genetic tools. Here we developed a new forward genetic screen to identify Wolbachia over-proliferative mutant variants.
We characterized in detail two of these new mutants, wMelPop2 and wMelOctoless, and show that the amplification or loss of the Octomom genomic region causes their over-proliferation. These results confirm previous data and expand on the complex role of this genomic region in the control of Wolbachia proliferation. Both new mutants shorten the host lifespan and increase antiviral protection. Moreover, we show that Wolbachia proliferation rate in Drosophila melanogaster depends on the interaction between Octomom copy number, the host developmental stage, and temperature.
Our analysis also suggests that the life shortening phenotype and antiviral protection of Wolbachia are dependent on related, but different, properties of the endosymbiont; the rate of proliferation and the titres at time of infection, respectively. Altogether, we demonstrate the feasibility of a novel and unbiased experimental approach to study Wolbachia biology, which can be further adapted to characterize other genetically intractable bacterial endosymbionts.