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Molecular and Cellular Biology, April 2000, p. 2488-2497, Vol. 20, No. 7
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.
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
*
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.
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