Engineering yeast endosymbionts as a step toward the evolution of mitochondria

Abstract

It has been hypothesized that mitochondria evolved from a bacterial ancestor that initially became established in an archaeal host cell as an endosymbiont. Here we model this first stage of mitochondrial evolution by engineering endosymbiosis betweenEscherichia coliandSaccharomyces cerevisiae. An ADP/ATP translocase-expressingE. coliprovided ATP to a respiration-deficientcox2yeast mutant and enabled growth of a yeast–E. colichimera on a nonfermentable carbon source. In a reciprocal fashion, yeast provided thiamin to an endosymbioticE. colithiamin auxotroph. Expression of several SNARE-like proteins inE. coliwas also required, likely to block lysosomal degradation of intracellular bacteria. This chimeric system was stable for more than 40 doublings, and GFP-expressingE. coliendosymbionts could be observed in the yeast by fluorescence microscopy and X-ray tomography. This readily manipulated system should allow experimental delineation of host–endosymbiont adaptations that occurred during evolution of the current, highly reduced mitochondrial genome.