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Non-mitochondrial complex I proteins in a hydrogenosomal oxidoreductase complex

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  • Sabrina D. Dyall

    (University of California, Los Angeles
    NASA Astrobiology Institute, Center for Astrobiology/IGPP)

  • Weihong Yan

    (University of California, Los Angeles
    University of California, Los Angeles)

  • Maria G. Delgadillo-Correa

    (University of California, Los Angeles)

  • Adam Lunceford

    (University of California, Los Angeles)

  • Joseph A. Loo

    (University of California, Los Angeles)

  • Catherine F. Clarke

    (University of California, Los Angeles)

  • Patricia J. Johnson

    (University of California, Los Angeles
    NASA Astrobiology Institute, Center for Astrobiology/IGPP)

Abstract

Trichomonas vaginalis is a unicellular microaerophilic eukaryote that lacks mitochondria yet contains an alternative organelle, the hydrogenosome, involved in pyruvate metabolism. Pathways between the two organelles differ substantially: in hydrogenosomes, pyruvate oxidation is catalysed by pyruvate:ferredoxin oxidoreductase (PFOR), with electrons donated to an [Fe]-hydrogenase which produces hydrogen. ATP is generated exclusively by substrate-level phosphorylation in hydrogenosomes, as opposed to oxidative phosphorylation in mitochondria1. PFOR and hydrogenase are found in eubacteria and amitochondriate eukaryotes, but not in typical mitochondria2,3,4. Analyses of mitochondrial genomes indicate that mitochondria have a single endosymbiotic origin from an α-proteobacterial-type progenitor5. The absence of a genome in trichomonad hydrogenosomes6 precludes such comparisons, leaving the endosymbiotic history of this organelle unclear7. Although phylogenetic reconstructions of a few proteins indicate that trichomonad hydrogenosomes share a common origin with mitochondria8,9,10,11, others do not2,3,4,7. Here we describe a novel NADH dehydrogenase module of respiratory complex I that is coupled to the central hydrogenosomal fermentative pathway to form a hydrogenosomal oxidoreductase complex that seems to function independently of quinones. Phylogenetic analyses of hydrogenosomal complex I-like proteins Ndh51 and Ndh24 reveal that neither has a common origin with mitochondrial homologues. These studies argue against a vertical origin of trichomonad hydrogenosomes from the proto-mitochondrial endosymbiont.

Suggested Citation

  • Sabrina D. Dyall & Weihong Yan & Maria G. Delgadillo-Correa & Adam Lunceford & Joseph A. Loo & Catherine F. Clarke & Patricia J. Johnson, 2004. "Non-mitochondrial complex I proteins in a hydrogenosomal oxidoreductase complex," Nature, Nature, vol. 431(7012), pages 1103-1107, October.
  • Handle: RePEc:nat:nature:v:431:y:2004:i:7012:d:10.1038_nature02990
    DOI: 10.1038/nature02990
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    Cited by:

    1. Pavel Dolezal & Michael J Dagley & Maya Kono & Peter Wolynec & Vladimir A Likić & Jung Hock Foo & Miroslava Sedinová & Jan Tachezy & Anna Bachmann & Iris Bruchhaus & Trevor Lithgow, 2010. "The Essentials of Protein Import in the Degenerate Mitochondrion of Entamoeba histolytica," PLOS Pathogens, Public Library of Science, vol. 6(3), pages 1-13, March.
    2. Vladimir Hampl & Jeffrey D Silberman & Alexandra Stechmann & Sara Diaz-Triviño & Patricia J Johnson & Andrew J Roger, 2008. "Genetic Evidence for a Mitochondriate Ancestry in the ‘Amitochondriate’ Flagellate Trimastix pyriformis," PLOS ONE, Public Library of Science, vol. 3(1), pages 1-9, January.

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