A secreted endosymbiont protein essential for colonizing host cells

ABSTRACTIntracellular bacterial symbioses have arisen myriad times in eukaryotes, with dozens known from insects alone1,2. Beginning with Buchnera, the obligate endosymbiont of aphids, genomes of endosymbionts have illuminated their evolutionary origins and metabolic contributions to hosts3,4. However, the mechanisms by which nonculturable endosymbionts enter host cells and suppress cellular immune processes have remained unknown. We show that an uncharacterized Buchnera protein, here designated SyeA, was present in the Buchnera ancestor, is secreted and homologous to secreted effectors of bacterial pathogens and is essential for Buchnera transmission. Buchnera is transmitted via expulsion from specialized maternal cells and uptake by embryos5. Using immunofluorescence microscopy, we found that SyeA levels peak upon colonization, accompanied by actin accumulation at the entry site. SyeA localizes outside the host-derived membrane and actin layer surrounding each Buchnera cell and colocalizes in host cytoplasm with Rho1, which regulates actin polymerization. syeA knockdown disrupts colonization and embryonic development and elevates lysosomal activity, leading to Buchnera destruction6. Our findings provide rare insight into how an anciently associated, mutualistic endosymbiont achieves its intracellular existence. SyeA is a vestige of pathogenic origins followed by evolution of increased host control and erosion of the original, more complex pathogenicity machinery.