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Non-mitochondrial complex I proteins in a hydrogenosomal oxidoreductase complex

Nature volume 431, pages 1103–1107 (2004)Cite this article

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.

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Figure 1: Complex I proteins.
Figure 2: T. vaginalis Ndh protein–protein interactions.
Figure 3: Hydrogenosomal carbohydrate metabolism.
Figure 4: Analyses of NuoF and NuoE phylogenies with MRBAYES30 show that T. vaginalis Ndh51 and Ndh24 do not belong to the mitochondrial clade.

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Acknowledgements

We thank J. L. Kerwin for mass spectrometric analyses. Preliminary T. vaginalis genome sequence data were obtained from TIGR through the website at http://www.tigr.org. Sequencing of the T. vaginalis genome was accomplished with support from the NIH. This work was supported by National Institute of Health (NIH) grants (P.J.J. and C.F.C.) and a National Aeronautics and Space Administration Astrobiology grant to UCLA. P.J.J. is a Burroughs Wellcome Scholar in Molecular Parasitology. The UCLA Mass Spectrometry and Proteomics Technology Center (J.A.L.) was established with a grant from the W. M. Keck Foundation.

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Authors and Affiliations

  1. Department of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles, 1602 Molecular Sciences Building, 609 Charles E. Young Drive East, Los Angeles, California, 90095-1489, USA

    Sabrina D. Dyall, Weihong Yan, Maria G. Delgadillo-Correa & Patricia J. Johnson

  2. NASA Astrobiology Institute, Center for Astrobiology/IGPP, 3845 Slichter Hall, Los Angeles, California, 90095-1567, USA

    Sabrina D. Dyall & Patricia J. Johnson

  3. Department of Chemistry and Biochemistry, University of California, Los Angeles, 607 Charles E. Young Drive East, Los Angeles, California, 90095-1569, USA

    Weihong Yan, Adam Lunceford & Catherine F. Clarke

  4. Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles, 402 Paul D. Boyer Hall, Los Angeles, California, 90095-1737, USA

    Joseph A. Loo

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Correspondence to Patricia J. Johnson.

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Supplementary information

Supplementary Figure 1

Alignment of T. vaginalis malic enzyme subunits Mae A, B, G, H using CLUSTALW. (DOC 34 kb)

Supplementary Figure 2

Reconstruction of NuoE phylogeny excluding highly divergent sequences. This phylogenetic reconstruction of NuoE sequences shows that the position of T. vaginalis Ndh24 is not due to a long-branch artefact. (JPG 93 kb)

Supplementary Figure 2 Legend (DOC 31 kb)

Supplementary Table 1

Primer sequences used in study. (DOC 27 kb)

Supplementary Table 2

List of sequences used to reconstruct Ndh51 phylogeny, with names and accession numbers. (DOC 61 kb)

Supplementary Table 3

List of sequences used to reconstruct Ndh24 phylogeny, with names and accession numbers. (DOC 53 kb)

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Dyall, S., Yan, W., Delgadillo-Correa, M. et al. Non-mitochondrial complex I proteins in a hydrogenosomal oxidoreductase complex. Nature 431, 1103–1107 (2004). https://doi.org/10.1038/nature02990

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