Restriction of Wolbachia Bacteria in Early Embryogenesis of Neotropical Drosophila Species via Endoplasmic Reticulum-Mediated Autophagy

Wolbachia are maternally transmitted intracellular bacteria that are not only restricted to the reproductive organs but also found in various somatic tissues of their native hosts. The abundance of the endosymbiont in the soma, usually a dead end for vertically transmitted bacteria, causes a multitude of effects on life history traits of their hosts, which are still not well understood. Thus, deciphering the host-symbiont interactions on a cellular level throughout a host’s life cycle is of great importance to understand their homeostatic nature, persistence, and spreading success. Using fluorescent and transmission electron microscopy, we conducted a comprehensive analysis of Wolbachia tropism in soma and germ line of six Drosophila species at the intracellular level during host development. Our data uncovered diagnostic patterns of infections to embryonic primordial germ cells and to particular cells of the soma in three different neotropical Drosophila species that have apparently evolved independently. We further found that restricted patterns of Wolbachia tropism are determined in early embryogenesis via selective autophagy, and their spatially restricted infection patterns are preserved in adult flies. We observed tight interactions of Wolbachia with membranes of the endoplasmic reticulum, which might play a scaffolding role for autophagosome formation and subsequent elimination of the endosymbiont. Finally, by analyzing D. simulans lines transinfected with nonnative Wolbachia, we uncovered that the host genetic background regulates tissue tropism of infection. Our data demonstrate a novel and peculiar mechanism to limit and spatially restrict bacterial infection in the soma during a very early stage of host development.