An anaerobic mitochondrion that produces hydrogen (original) (raw)

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.

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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..

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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
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  2. Rob M. de Graaf
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  3. Georg W. M. van der Staay
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  4. Theo A. van Alen
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  7. Angela H. A. M. van Hoek
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  8. Seung Yeo Moon-van der Staay
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  9. Werner J. H. Koopman
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  10. Jaap J. van Hellemond
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  11. Aloysius G. M. Tielens
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  13. Marten Veenhuis
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Correspondence toJohannes H. P. Hackstein.

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Supplementary Notes

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

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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

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Editorial Summary

Change in the air

Hydrogenosomes are simple organelles found in anaerobic protists and fungi. They are double-membraned and produce ATP and hydrogen, hence suggestions that they are anaerobic derivatives of mitochondria. An alternative view suggests that mitochondria and hydrogenosomes arose from a common ancestor, a facultatively anaerobic bacterium. The discovery of a novel hydrogenosome in Nyctotherus ovalis, a ciliate that lives in the gut of cockroaches, further complicates this debate. It is unique among known hydrogenosomes because, just like a mitochondrion, it retains its own genome. This ‘missing link’ between hydrogenosomes and mitochondria also has remnants of an electron transport chain characteristic of an aerobic lifestyle.

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