Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I

• Published in: Nature 2004-12, Vol.432 (7017), p.618-622
• Main Authors: Tachezy, Jan, Martin Embley, T, Hrdy, Ivan, Hirt, Robert P, Dolezal, Pavel, Bardonová, Lucie, Foster, Peter G
• Format: Article
• Language: English
• Subjects: Aerobiosis; Amino Acid Sequence; Anaerobiosis; Animals; Bacteria; Biological and medical sciences; Biological evolution; Dehydrogenase; Electron Transport Complex I - chemistry; Electron Transport Complex I - metabolism; Electrons; Enzymes; Eukaryotes; Fundamental and applied biological sciences. Psychology; Genetics of eukaryotes. Biological and molecular evolution; Humanities and Social Sciences; Hydrogen - metabolism; Hydrogen production; letter; Malates - metabolism; Mitochondria - enzymology; Mitochondria - metabolism; Models, Biological; Molecular Sequence Data; multidisciplinary; NAD - metabolism; NADH Dehydrogenase - chemistry; NADH Dehydrogenase - metabolism; Organelles - enzymology; Organelles - metabolism; Phylogeny; Protein Subunits - chemistry; Protein Subunits - metabolism; Protozoan Proteins - chemistry; Protozoan Proteins - metabolism; Science; Science (multidisciplinary); Sequence Alignment; Symbiosis; Trichomonas vaginalis; Trichomonas vaginalis - cytology; Trichomonas vaginalis - enzymology; Trichomonas vaginalis - metabolism
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature03149

Hydrogenosomes are double-membraned ATP-producing and hydrogen-producing organelles of diverse anaerobic eukaryotes. In some versions of endosymbiotic theory they are suggested to be homologues of mitochondria, but alternative views suggest they arose from an anaerobic bacterium that was distinct from the mitochondrial endosymbiont. Here we show that the 51-kDa and 24-kDa subunits of the NADH dehydrogenase module in complex I, the first step in the mitochondrial respiratory chain, are active in hydrogenosomes of Trichomonas vaginalis. Like mitochondrial NADH dehydrogenase, the purified Trichomonas enzyme can reduce a variety of electron carriers including ubiquinone, but unlike the mitochondrial enzyme it can also reduce ferredoxin, the electron carrier used for hydrogen production. The presence of NADH dehydrogenase solves the long-standing conundrum of how hydrogenosomes regenerate NAD+ after malate oxidation. Phylogenetic analyses show that the Trichomonas 51-kDa homologue shares common ancestry with the mitochondrial enzyme. Recruitment of complex I subunits into a H2-producing pathway provides evidence that mitochondria and hydrogenosomes are aerobic and anaerobic homologues of the same endosymbiotically derived organelle.