Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I
Abstract
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.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Six-state recoding methods have been endorsed from a theoretical perspective, but their performance has never been extensively tested.
“While these methods have been endorsed from a theoretical perspective, their performance has never been extensively tested.”
From Six-state amino acid recoding is not an effective strategy to offset the effects of compositional heterogeneity and saturation in phylogenetic analyses (2019) · cites this paper as Hrdy et al. 2004
Data-recoding methods reduce compositional heterogeneity in the WhelanD20 and Chang datasets.
“We show that data-recoding methods [13-15] reduce compositional heterogeneity in these datasets”
From Improved Modeling of Compositional Heterogeneity Supports Sponges as Sister to All Other Animals (2017) · cites this paper as [13]
Across-site replacement-pattern heterogeneity and compositional heterogeneity across taxa can both have a misleading effect on phylogenetic reconstruction.
“Across-site replacement-pattern heterogeneity [26] and compositional heterogeneity across taxa [13, 55] can both have a misleading effect on phylogenetic reconstruction.”
From Improved Modeling of Compositional Heterogeneity Supports Sponges as Sister to All Other Animals (2017) · cites this paper as [13]
Amino acid recoding has long been considered a powerful strategy to reduce compositional heterogeneity and saturation in the data.
“Amino acid recoding has long been considered as a powerful strategy to reduce compositional heterogeneity and saturation in the data [7, 13-15, 31-36]”
From Improved Modeling of Compositional Heterogeneity Supports Sponges as Sister to All Other Animals (2017) · cites this paper as [13]
Cites
Whelan, S., & Goldman, N. (2001) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003851 · Cited by 2,849 · see citing works
The Hydrogen Hypothesis for the First Eukaryote
Martin, W., & Müller, M. (1998) · Nature · doi:10.1038/32096 · Cited by 1,282 · see citing works
Modeling compositional heterogeneity
Foster, P. G. (2004) · Systematic Biology · doi:10.1080/10635150490445779 · Cited by 474 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Tunicates and not cephalochordates are the closest living relatives of vertebrates
Delsuc, F., Brinkmann, H., Chourrout, D., & Philippe, H. (2006) · Nature · doi:10.1038/nature04336 · Cited by 1,651 · see citing works
Eukaryotic evolution, changes and challenges
Embley, T. M., & Martin, W. (2006) · Nature · doi:10.1038/nature04546 · Cited by 867 · see citing works
Self-citationBiochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes
Müller, M., Mentel, M., van Hellemond, J. J., Henze, K., Woehle, C., Gould, S. B., Yu, R.-Y., van der Giezen, M., Tielens, A. G. M., & Martin, W. F. (2012) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.05024-11 · Cited by 838 · see citing works
Gray, M. W. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a011403 · Cited by 639 · see citing works
Simion, P., Philippe, H., Baurain, D., Jager, M., Richter, D. J., Di Franco, A., Roure, B., Satoh, N., Quéinnec, É., Ereskovsky, A., et al. (2017) · Current Biology · doi:10.1016/j.cub.2017.02.031 · Cited by 518 · see citing works
Improved Modeling of Compositional Heterogeneity Supports Sponges as Sister to All Other Animals
Feuda, R., Dohrmann, M., Pett, W., Philippe, H., Rota-Stabelli, O., Lartillot, N., Wörheide, G., & Pisani, D. (2017) · Current Biology · doi:10.1016/j.cub.2017.11.008 · Cited by 291 · see citing works
Philippe, H., Delsuc, F., Brinkmann, H., & Lartillot, N. (2005) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev.ecolsys.35.112202.130205 · Cited by 306 · see citing works
Phylogenomics provides robust support for a two-domains tree of life
Williams, T. A., Cox, C. J., Foster, P. G., Szöllősi, G. J., & Embley, T. M. (2019) · Nature Ecology & Evolution · doi:10.1038/s41559-019-1040-x · Cited by 274 · see citing works
Self-citationIntegrative modeling of gene and genome evolution roots the archaeal tree of life
Williams, T. A., Szöllősi, G. J., Spang, A., Foster, P. G., Heaps, S. E., Boussau, B., Ettema, T. J. G., & Embley, T. M. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1618463114 · Cited by 233 · see citing works
Self-citationGenomic diversity, lifestyles and evolutionary origins of DPANN archaea
Dombrowski, N., Lee, J.-H., Williams, T. A., Offre, P., & Spang, A. (2019) · FEMS Microbiology Letters · doi:10.1093/femsle/fnz008 · Cited by 230 · see citing works
On Reduced Amino Acid Alphabets for Phylogenetic Inference
Susko, E., & Roger, A. J. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm144 · Cited by 177 · see citing works
Redmond, A. K., & McLysaght, A. (2021) · Nature Communications · doi:10.1038/s41467-021-22074-7 · Cited by 139 · see citing works
Multiple secondary origins of the anaerobic lifestyle in eukaryotes
Martin Embley, T. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1844 · Cited by 124 · see citing works
Heterogeneous Models Place the Root of the Placental Mammal Phylogeny
Morgan, C. C., Foster, P. G., Webb, A. E., Pisani, D., McInerney, J. O., & O’Connell, M. J. (2013) · Molecular Biology and Evolution · doi:10.1093/molbev/mst117 · Cited by 123 · see citing works
Self-citationEnergy metabolism among eukaryotic anaerobes in light of Proterozoic ocean chemistry
Mentel, M., & Martin, W. (2008) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2008.0031 · Cited by 92 · see citing works
Plastid establishment did not require a chlamydial partner
Domman, D., Horn, M., Embley, T. M., & Williams, T. A. (2015) · Nature Communications · doi:10.1038/ncomms7421 · Cited by 51 · see citing works
Self-citationHernandez, A. M., & Ryan, J. F. (2019) · doi:10.1101/729103 · Cited by 52 · see citing works
Signal Conflicts in the Phylogeny of the Primary Photosynthetic Eukaryotes
Deschamps, P., & Moreira, D. (2009) · Molecular Biology and Evolution · doi:10.1093/molbev/msp189 · Cited by 50 · see citing works
- Authors
- Hrdy, I., Hirt, R. P., Dolezal, P., Bardonová, L., Foster, P. G., Tachezy, J., & Martin Embley, T.
- Affiliations
- Newcastle University (GB)
- Charles University (CZ)
- Natural History Museum (GB)
- Corresponding author
- Tachezy, Jan
- Venue
- Nature
- Published
- 2004-12
- Volume
- 432
- Issue
- 7017
- Pages
- 618-622
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2062899499
- Cited by
- 262
- References
- 3
- Citations by year
- 2026: 7 · 2025: 2 · 2024: 8 · 2023: 3 · 2022: 12 · 2021: 13 · 2020: 6 · 2019: 17 · 2018: 4 · 2017: 12 · 2016: 11 · 2015: 5 · 2014: 10 · 2013: 9 · 2012: 18
- FWCI
- 7.22
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases
- Fogarty International Center
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Metalloenzymes and iron-sulfur proteins
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
- Keywords
- hydrogenosomes, Trichomonas vaginalis, NADH dehydrogenase, mitochondrial complex I, endosymbiotic theory, hydrogen production, ferredoxin, NAD+ regeneration, malate oxidation, ubiquinone reduction, mitochondrial evolution, anaerobic eukaryotes, phylogenetic analysis
- MeSH terms
- Aerobiosis, Amino Acid Sequence, Anaerobiosis, Animals, Hydrogen, Malates, Mitochondria, Models, Biological, Molecular Sequence Data, NAD, NADH Dehydrogenase, Phylogeny, Symbiosis, Trichomonas vaginalis, Organelles, Protozoan Proteins, Sequence Alignment, Protein Subunits, Electron Transport Complex I
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
