Presence of a member of the mitochondrial carrier family in hydrogenosomes: Conservation of membrane-targeting pathways between hydrogenosomes and mitochondria

A number of microaerophilic eukaryotes lack mitochondria but possess anothe r organelle involved in energy metabolism, the hydrogenosome. Limited phylo genetic analyses of nuclear genes support a common origin for these two org anelles. We have identified a protein of the mitochondrial carrier family i n the hydrogenosome of Trichomonas vaginalis and have shown that this prote in, Hmp31, is phylogenetically related to the mitochondrial ADP-ATP carrier (AAC). We demonstrate that the hydrogenosomal AAC can be targeted to the i nner membrane of mitochondria isolated from Saccharomyces cerevisiae throug h the Tim9-Tim10 import pathway used for the assembly of mitochondrial carr ier proteins. Conversely, yeast mitochondrial AAC can be targeted into the membranes of hydrogenosomes. The hydrogenosomal AAC contains a cleavable, N -terminal presequence; however, this sequence is not necessary for targetin g the protein to the organelle. These data indicate that the membrane-targe ting signal(s) for hydrogenosomal AAC is internal, similar to that found fo r mitochondrial carrier proteins. Our findings indicate that the membrane c arriers and membrane protein-targeting machinery of hydrogenosomes and mito chondria have a common evolutionary origin. Together, they provide strong e vidence that a single endosymbiont evolved into a progenitor organelle in e arly eukaryotic cells that ultimately give rise to these two distinct organ elles and support the hydrogen hypothesis for the origin of the eukaryotic cell.