Vertical transmission of a Drosophila endosymbiont via co-option of the yolk transport and internalization machinery. Jeremy K Herren, Juan C Paredes, Fanny Schupfer, Bruno Lemaitre. Global Health Institute, EPFL, Lausanne, Vaud, Switzerland.

   Spiroplasma is a diverse bacterial clade that includes many vertically transmitted insect endosymbionts, including Spiroplasma poulsonii, a natural endosymbiont of Drosophila melanogaster. These bacteria persist in the hemolymph of their adult host and exhibit efficient vertical transmission from mother to offspring. Here, we identify the mechanism that underlies their vertical transmission, showing that these bacteria use the yolk uptake machinery to colonize the germline. We show that Spiroplasma reach the oocyte by passing through the intercellular space surrounding the ovarian follicle cells and are then endocytosed into oocytes within yolk granules during the vitellogenic stages of oogenesis. Mutations that disrupt yolk uptake by oocytes inhibit vertical transmission of Spiroplasma and lead to an accumulation of these bacteria outside of the oocyte. Impairment of yolk secretion by the fat body results in Spiroplasma not reaching the oocyte and a blockage of vertical transmission. We propose a model in which Spiroplasma first interacts with yolk in the hemolymph to gain access to the oocyte and then uses the yolk receptor, Yolkless, to be endocytosed into the oocyte. Co-option of the yolk uptake machinery appears to be a powerful strategy for endosymbionts to target the germline and achieve vertical transmission. This mechanism may apply to other endosymbionts and provides a possible explanation for endosymbiont host specificity.