A divergent ADP/ATP carrier in the hydrogenosomes of Trichomonas gallinae argues for an independent origin of these organelles

Authors

  • Joachim Tjaden,

    1. Department of Plant Physiology, University of Kaiserslautern, Erwin Schroedinger Strasse, D-67663 Kaiserslautern, Germany.
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  • Ilka Haferkamp,

    1. Department of Plant Physiology, University of Kaiserslautern, Erwin Schroedinger Strasse, D-67663 Kaiserslautern, Germany.
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  • Brigitte Boxma,

    1. Department of Evolutionary Microbiology, Faculty of Science, University of Nijmegen, Toernooiveld 1, NL-6525 ED Nijmegen, the Netherlands.
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  • Aloysius G. M. Tielens,

    1. Department of Biochemistry and Cell Biology, Faculty of Veterinary Medicine, Utrecht University, PO Box 80176, NL-3508 TD Utrecht, the Netherlands.
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  • Martijn Huynen,

    1. Nijmegen Centre for Molecular Life Sciences (NCMLS) and Centre for Molecular and Biomolecular Informatics, Toernooiveld 1, NL- 6525 ED Nijmegen, the Netherlands.
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  • Johannes H. P. Hackstein

    Corresponding author
    1. Department of Evolutionary Microbiology, Faculty of Science, University of Nijmegen, Toernooiveld 1, NL-6525 ED Nijmegen, the Netherlands.
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E-mail hack@sci.kun.nl; Tel. (+31) 24 365 2935; Fax (+31) 24 355 3450.

Summary

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.

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