Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

An anaerobic mitochondrion that produces hydrogen

Nature volume 434, pages 74–79 (2005)Cite this article

Abstract

Hydrogenosomes are organelles that produce ATP and hydrogen1, and are found in various unrelated eukaryotes, such as anaerobic flagellates, chytridiomycete fungi and ciliates2. Although all of these organelles generate hydrogen, the hydrogenosomes from these organisms are structurally and metabolically quite different, just like mitochondria where large differences also exist3. These differences have led to a continuing debate about the evolutionary origin of hydrogenosomes4,5. Here we show that the hydrogenosomes of the anaerobic ciliate Nyctotherus ovalis, which thrives in the hindgut of cockroaches, have retained a rudimentary genome encoding components of a mitochondrial electron transport chain. Phylogenetic analyses reveal that those proteins cluster with their homologues from aerobic ciliates. In addition, several nucleus-encoded components of the mitochondrial proteome, such as pyruvate dehydrogenase and complex II, were identified. The N. ovalis hydrogenosome is sensitive to inhibitors of mitochondrial complex I and produces succinate as a major metabolic end product—biochemical traits typical of anaerobic mitochondria3. The production of hydrogen, together with the presence of a genome encoding respiratory chain components, and biochemical features characteristic of anaerobic mitochondria, identify the N. ovalis organelle as a missing link between mitochondria and hydrogenosomes.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: A 14,027-bp fragment (mtg 1) of the hydrogenosomal genome of N. ovalis var.
Figure 2: Phylogenetic analysis of hydrogenosomal genes.
Figure 3: Hydrogenosomes of N. ovalis exhibit complex I activity.

References

  1. Müller, M. The hydrogenosome. J. Gen. Microbiol. 39, 2879–2889 (1993)

    Article  Google Scholar 

  2. Roger, A. J. Reconstructing early events in eukaryotic evolution. Am. Nat. 154, S146–S163 (1999)

    Article  CAS  Google Scholar 

  3. Tielens, A. G. M., Rotte, C., van Hellemond, J. J. & Martin, W. Mitochondria as we don't know them. Trends Biochem. Sci. 27, 564–572 (2002)

    Article  CAS  Google Scholar 

  4. Embley, T. M. et al. Hydrogenosomes, mitochondria and early eukaryotic evolution. IUBMB Life 55, 387–395 (2003)

    Article  CAS  Google Scholar 

  5. Dyall, S. D., Brown, M. T. & Johnson, P. J. Ancient invasions: From endosymbionts to organelles. Science 304, 253–257 (2004)

    Article  ADS  CAS  Google Scholar 

  6. van der Giezen, M., Sjollema, K. A., Artz, R. R., Alkema, W. & Prins, R. A. Hydrogenosomes in the anaerobic fungus Neocallimastix frontalis have a double membrane but lack an associated organelle genome. FEBS Lett. 408, 147–150 (1997)

    Article  CAS  Google Scholar 

  7. Clemens, D. L. & Johnson, P. J. Failure to detect DNA in hydrogenosomes of Trichomonas vaginalis by nick translation and immunomicroscopy. Mol. Biochem. Parasitol. 106, 307–313 (2000)

    Article  CAS  Google Scholar 

  8. Leon-Avila, G. & Tovar, J. Mitosomes of Entamoeba histolytica are abundant mitochondrion-related remnant organelles that lack a detectable organellar genome. Microbiol. 150, 1245–1250 (2004)

    Article  CAS  Google Scholar 

  9. Fenchel, T. & Finlay, B. J. Ecology and Evolution in Anoxic Worlds (Oxford University Press, Oxford, UK, 1995)

    Google Scholar 

  10. Embley, T. M., Horner, D. A. & Hirt, R. P. Anaerobic eukaryote evolution: hydrogenosomes as biochemically modified mitochondria? Trends Ecol. Evol. 12, 437–441 (1997)

    Article  CAS  Google Scholar 

  11. Voncken, F. et al. Multiple origins of hydrogenosomes: functional and phylogenetic evidence from the ADP/ATP carrier of the anaerobic chytrid Neocallimastix sp. Mol. Microbiol. 44, 1441–1454 (2002)

    Article  CAS  Google Scholar 

  12. van der Giezen, M. et al. Conserved properties of hydrogenosomal and mitochondrial ADP/ATP carriers: a common origin for both organelles. EMBO J. 21, 572–579 (2002)

    Article  CAS  Google Scholar 

  13. Martin, W., Hoffmeister, M., Rotte, C. & Henze, K. An overview of endosymbiotic models for the origins of eukaryotes, their ATP-producing organelles (mitochondria and hydrogenosomes), and their heterotrophic lifestyle. Biol. Chem. 382, 1521–1539 (2001)

    Article  CAS  Google Scholar 

  14. Martin, W. & Müller, M. The hydrogen hypothesis for the first eukaryote. Nature 392, 37–41 (1998)

    Article  ADS  CAS  Google Scholar 

  15. Akhmanova, A. et al. A hydrogenosome with a genome. Nature 396, 527–528 (1998)

    Article  ADS  CAS  Google Scholar 

  16. Brunk, C. F., Lee, L. C., Tran, A. B. & Li, J. Complete sequence of the mitochondrial genome of Tetrahymena thermophila and comparative methods for identifying highly divergent genes. Nucleic Acids Res. 31, 1673–1682 (2003)

    Article  CAS  Google Scholar 

  17. Burger, G., Gray, M. W. & Lang, B. F. Mitochondrial genomes: anything goes. Trends Genet. 19, 709–716 (2003)

    Article  CAS  Google Scholar 

  18. Dyall, S. D. et al. Non-mitochondrial complex I proteins in a hydrogenosomal oxidoreductase complex. Nature 431, 1103–1107 (2004)

    Article  ADS  CAS  Google Scholar 

  19. Hrdy, I. et al. Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature 432, 618–622 (2004)

    Article  ADS  CAS  Google Scholar 

  20. van Hoek, A. H. A. M. et al. Multiple acquisition of methanogenic archaeal symbionts by anaerobic ciliates. Mol. Biol. Evol. 17, 251–258 (2000)

    Article  CAS  Google Scholar 

  21. Degli Esposti, M. Inhibitors of NADH-ubiquinone reductase: an overview. Biochim. Biophys. Acta 1364, 222–235 (1998)

    Article  CAS  Google Scholar 

  22. Akhmanova, A. et al. A hydrogenosome with pyruvate formate-lyase: anaerobic chytrid fungi use an alternative route for pyruvate catabolism. Mol. Microbiol. 32, 1103–1114 (1999)

    Article  CAS  Google Scholar 

  23. Boxma, B. et al. The anaerobic chytridiomycete fungus Piromyces sp. E2 produces ethanol via pyruvate:formate lyase and an alcohol dehydrogenase E. Mol. Microbiol. 51, 1389–1399 (2004)

    Article  CAS  Google Scholar 

  24. van Hellemond, J. J., Klockiewicz, M., Gaasenbeek, C. P. H., Roos, M. H. & Tielens, A. G. M. Rhodoquinone and complex II of the electron transport chain in anaerobically functioning eukaryotes. J. Biol. Chem. 270, 31065–31070 (1995)

    Article  CAS  Google Scholar 

  25. Sickmann, A. et al. The proteome of Saccharomyces cerevisiae mitochondria. Proc. Natl Acad. Sci. USA 100, 13207–13212 (2003)

    Article  ADS  CAS  Google Scholar 

  26. Cotter, D., Guda, P., Fahy, E. & Subramaniam, S. MitoProteome: mitochondrial protein sequence database and annotation system. Nucleic Acids Res. 32, D463–D467 (2004)

    Article  CAS  Google Scholar 

  27. Voncken, F. G. J. et al. A hydrogenosomal [Fe]-hydrogenase from the anaerobic chytrid Neocallimastix sp L2. Gene 284, 103–112 (2002)

    Article  CAS  Google Scholar 

  28. van Hoek, A. H. A. M. et al. Voltage-dependent reversal of anodic galvanotaxis in Nyctotherus ovalis . J. Eukaryotic Microbiol. 46, 427–433 (1999)

    Article  CAS  Google Scholar 

  29. Koopman, W. J. H. et al. Membrane-initiated Ca2+ signals are reshaped during propagation to subcellular regions. Biophys. J. 81, 57–65 (2001)

    Article  ADS  CAS  Google Scholar 

  30. Curtis, E. A. & Landweber, L. F. Evolution of gene scrambling in ciliate micronuclear genes. Ann. NY Acad. Sci. 870, 349–350 (1999)

    Article  ADS  CAS  Google Scholar 

Download references

Acknowledgements

We thank L. Landweber, J. Wong and W.-J. Chang for advice on the cloning of complete minichromosomes and for sharing the first sequence of a PDH gene in N. ovalis; S. van Weelden and H. de Roock for help in the metabolic studies; J. Brouwers for analysis of the quinones; G. Cremers, L. de Brouwer, A. Ederveen, A. Grootemaat, M. Hachmang, S. Huver, S. Jannink, N. Jansse, R. Janssen, M. Kwantes, B. Penders, G. Schilders, R. Talens, D. van Maassen, H. van Zoggel, M. Veugelink and P. Wijnhoven for help with the isolation of various N. ovalis sequences; and K. Sjollema for electron microscopy. G.W.M.v.d.S., S.Y.M.-v.d.S. and G.R. were supported by the European Union 5th framework grant ‘CIMES’. This work was also supported by equipment grants from ZON (Netherlands Organisation for Health Research and Development), NWO (Netherlands Organisation for Scientific Research), and the European Union 6th framework programme for research, priority 1 “Life sciences, genomics and biotechnology for health” to W.J.H.K..

Author information

Author notes

  1. Angela H. A. M. van Hoek

    Present address: RIKILT, Institute of Food Safety, Bornsesteeg 45, NL-6708 PD, Wageningen, The Netherlands

  2. Brigitte Boxma, Rob M. de Graaf and Georg W. M. van der Staay: These authors contributed equally to this work

Authors and Affiliations

  1. Department of Evolutionary Microbiology, Faculty of Science, Radboud University Nijmegen, Toernooiveld 1, NL-6525 ED, Nijmegen, The Netherlands

    Brigitte Boxma, Rob M. de Graaf, Georg W. M. van der Staay, Theo A. van Alen, Angela H. A. M. van Hoek, Seung Yeo Moon-van der Staay & Johannes H. P. Hackstein

  2. Centre for Molecular and Biomolecular Informatics,

    Guenola Ricard, Toni Gabaldón & Martijn A. Huynen

  3. Microscopical Imaging Centre and Department of Biochemistry, Nijmegen Centre of Molecular Life Sciences (NCMLS), Radboud University Nijmegen Medical Centre, NL-6500 HB, Nijmegen, The Netherlands

    Werner J. H. Koopman

  4. Department of Biochemistry and Cell Biology, Faculty of Veterinary Medicine, Utrecht University, PO Box 80176, NL-3508 TD, Utrecht, The Netherlands

    Jaap J. van Hellemond & Aloysius G. M. Tielens

  5. Albert-Ludwigs-Universität, Institut für Organische Chemie und Biochemie, Albertstrasse 21, D-79104 i. Br., Freiburg, Germany

    Thorsten Friedrich

  6. Department of Eukaryotic Microbiology, Groningen University, PO Box 14, NL-9750 AA, Haren, The Netherlands

    Marten Veenhuis

Authors
  1. Brigitte Boxma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rob M. de Graaf
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Georg W. M. van der Staay
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Theo A. van Alen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Guenola Ricard
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Toni Gabaldón
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Angela H. A. M. van Hoek
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Seung Yeo Moon-van der Staay
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Werner J. H. Koopman
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jaap J. van Hellemond
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Aloysius G. M. Tielens
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Thorsten Friedrich
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Marten Veenhuis
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Martijn A. Huynen
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Johannes H. P. Hackstein
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Johannes H. P. Hackstein.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Notes

This file contains the Supplementary Methods, Supplementary Figures S1-S16 and a Supplementary Table for the study. (PDF 1898 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Boxma, B., de Graaf, R., van der Staay, G. et al. An anaerobic mitochondrion that produces hydrogen. Nature 434, 74–79 (2005). https://doi.org/10.1038/nature03343

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature03343

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing