Non-mitochondrial complex I proteins in a hydrogenosomal oxidoreductase complex

• Published in: Nature (London) 2004-10, Vol.431 (7012), p.1103-1107
• Main Authors: Dyall, Sabrina D., Yan, Weihong, Delgadillo-Correa, Maria G., Lunceford, Adam, Loo, Joseph A., Clarke, Catherine F., Johnson, Patricia J.
• Format: Article
• Language: English
• Subjects: Adenosine Triphosphate - metabolism; Amino Acid Sequence; Animals; Biological and medical sciences; Biological Evolution; Carbohydrate Metabolism; Electron Transport Complex I - chemistry; Electron Transport Complex I - metabolism; Fermentation; Fundamental and applied biological sciences. Psychology; Genetics of eukaryotes. Biological and molecular evolution; Humanities and Social Sciences; Hydrogen - metabolism; Hydrogenase - metabolism; Iron-Sulfur Proteins - metabolism; Ketone Oxidoreductases - metabolism; letter; Metabolism; Microbiology; Mitochondrial Proteins - chemistry; Models, Biological; Molecular Sequence Data; multidisciplinary; NADH Dehydrogenase - chemistry; NADH Dehydrogenase - metabolism; Organelles - enzymology; Organelles - metabolism; Oxidation; Oxidation-Reduction; Phosphorylation; Phylogeny; Protein Binding; Proteins; Pyruvate Synthase; Pyruvic Acid - metabolism; Science; Science (multidisciplinary); Symbiosis; Trichomonas vaginalis; Trichomonas vaginalis - cytology; Trichomonas vaginalis - enzymology; Trichomonas vaginalis - metabolism
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature02990

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 mitochondria 1 . PFOR and hydrogenase are found in eubacteria and amitochondriate eukaryotes, but not in typical mitochondria 2 , 3 , 4 . Analyses of mitochondrial genomes indicate that mitochondria have a single endosymbiotic origin from an α-proteobacterial-type progenitor 5 . The absence of a genome in trichomonad hydrogenosomes 6 precludes such comparisons, leaving the endosymbiotic history of this organelle unclear 7 . Although phylogenetic reconstructions of a few proteins indicate that trichomonad hydrogenosomes share a common origin with mitochondria 8 , 9 , 10 , 11 , others do not 2 , 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.