A divergent ADP/ATP carrier in the hydrogenosomes of Trichomonas gallinae argues for an independent origin of these organelles.
The evolution of mitochondrial ADP and ATP exchanging proteins (AACs) highlights a key event in the evolution of the eukaryotic cell, as ATP exporting carriers were indispensable in establishing the role of mitochondria as ATP-generating cellular organelles. Hydrogenosomes, i.e. ATP- and hydrogen-generating organelles of certain anaerobic unicellular eukaryotes, are believed to have evolved from the same ancestral endosymbiont that gave rise to present day mitochondria. Notably, the hydrogenosomes of the parasitic anaerobic flagellate Trichomonas seemed to be deficient in mitochondrial-type AACs. Instead, HMP 31, a different member of the mitochondrial carrier family (MCF) with a hitherto unknown function, is abundant in the hydrogenosomal membranes of Trichomonas vaginalis. Here we show that the homologous HMP 31 of closely related Trichomonas gallinae specifically transports ADP and ATP with high efficiency, as do genuine mitochondrial AACs. However, phylogenetic analysis and its resistance against bongkrekic acid (BKA, an efficient inhibitor of mitochondrial-type AACs) identify HMP 31 as a member of the mitochondrial carrier family that is distinct from all mitochondrial and hydrogenosomal AACs studied so far. Thus, our data support the hypothesis that the various hydrogenosomes evolved repeatedly and independently.
Tjaden
Joachim
J
Department of Plant Physiology, University of Kaiserslautern, Erwin Schroedinger Strasse, D-67663 Kaiserslautern, Germany.
Haferkamp
Ilka
I
Boxma
Brigitte
B
Tielens
Aloysius G M
AG
Huynen
Martijn
M
Hackstein
Johannes H P
JH
D000244:Adenosine Diphosphate / Q000378:metabolism; D000255:Adenosine Triphosphate / Q000378:metabolism; D000818:Animals; D000900:Anti-Bacterial Agents / Q000378:metabolism; D001865:Bongkrekic Acid / Q000378:metabolism; D004926:Escherichia coli / Q000235:genetics / Q000378:metabolism; D019143:Evolution, Molecular; D006859:Hydrogen / Q000378:metabolism; D000226:Mitochondrial ADP, ATP Translocases / Q000145:classification / Q000235:genetics / Q000378:metabolism*; D008969:Molecular Sequence Data; D015388:Organelles / Q000378:metabolism*; D010802:Phylogeny; D010940:Plant Proteins / Q000378:metabolism; D015800:Protozoan Proteins / Q000145:classification / Q000235:genetics / Q000378:metabolism*; D014244:Trichomonas / Q000166:cytology* / Q000378:metabolism*
D000900:Anti-Bacterial Agents; D010940:Plant Proteins; D015800:Protozoan Proteins; D001865:Bongkrekic Acid; D000244:Adenosine Diphosphate; D006859:Hydrogen; D000255:Adenosine Triphosphate; D000226:Mitochondrial ADP, ATP Translocases