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Molecular and Cellular Biology, April 2000, p. 2488-2497, Vol. 20, No. 7
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Presence of a Member of the Mitochondrial Carrier Family in Hydrogenosomes: Conservation of Membrane-Targeting Pathways between Hydrogenosomes and Mitochondria

Sabrina D. Dyall,1 Carla M. Koehler,2,3 Maria G. Delgadillo-Correa,1 Peter J. Bradley,1 Evelyn Plümper,1 Danielle Leuenberger,2 Christoph W. Turck,4 and Patricia J. Johnson1,3,*

Department of Microbiology and Immunology,1 Department of Chemistry and Biochemistry,2 and Molecular Biology Institute,3 University of California, Los Angeles, California 90095, and Howard Hughes Medical Institute, Department of Medicine and Cardiovascular Research Institute, University of California, San Francisco, California 941434

Received 25 October 1999/Returned for modification 1 December 1999/Accepted 5 January 2000

A number of microaerophilic eukaryotes lack mitochondria but possess another organelle involved in energy metabolism, the hydrogenosome. Limited phylogenetic analyses of nuclear genes support a common origin for these two organelles. We have identified a protein of the mitochondrial carrier family in the hydrogenosome of Trichomonas vaginalis and have shown that this protein, Hmp31, is phylogenetically related to the mitochondrial ADP-ATP carrier (AAC). We demonstrate that the hydrogenosomal AAC can be targeted to the inner membrane of mitochondria isolated from Saccharomyces cerevisiae through the Tim9-Tim10 import pathway used for the assembly of mitochondrial carrier 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 targeting the protein to the organelle. These data indicate that the membrane-targeting signal(s) for hydrogenosomal AAC is internal, similar to that found for mitochondrial carrier proteins. Our findings indicate that the membrane carriers and membrane protein-targeting machinery of hydrogenosomes and mitochondria have a common evolutionary origin. Together, they provide strong evidence that a single endosymbiont evolved into a progenitor organelle in early eukaryotic cells that ultimately give rise to these two distinct organelles and support the hydrogen hypothesis for the origin of the eukaryotic cell.

* Corresponding author. Mailing address: UCLA Department of Microbiology and Immunology, 1602 Molecular Sciences Building, 405 Hilgard Ave., Los Angeles, CA 90095-1489. Phone: (310) 825-4870. Fax: (310) 206-5231. E-mail: johnsonp{at}ucla.edu.

Molecular and Cellular Biology, April 2000, p. 2488-2497, Vol. 20, No. 7
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


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