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An anaerobic mitochondrion that produces hydrogen

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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Correspondence to Johannes H. P. Hackstein.

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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)

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Further reading

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.

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