An anaerobic mitochondrion that produces hydrogen

Brigitte Boxma, Rob M. de Graaf, Georg W.M. van der Staay, Theo A. van Alen, Guenola Ricard, Toni Gabaldón, Angela H.A.M. van Hoek, Seung Yeo Moon-van der Staay, Werner J.H. Koopman, Jaap J. van Hellemond, Aloysius G.M. Tielens, Thorsten Friedrich, Marten Veenhuis, Martijn A. Huynen, Johannes H.P. Hackstein

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Abstract

Hydrogenosomes are organelles that produce ATP and hydrogen, and are found in various unrelated eukaryotes, such as anaerobic flagellates, chytridiomycete fungi and ciliates. 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 exist. These differences have led to a continuing debate about the evolutionary origin of hydrogenosomes. 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 mitochondria. 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.
Original languageEnglish
Pages (from-to)74 - 79
Number of pages6
JournalNature
Volume434
Issue number7029
DOIs
Publication statusPublished - 2005

Keywords

  • CHYTRID NEOCALLIMASTIX SP
  • PYRUVATE-FORMATE-LYASE
  • COMPLEX-I
  • ORGANELLES
  • GENOME
  • EVOLUTION
  • EUKARYOTE
  • MEMBRANE
  • SEQUENCE
  • ORIGINS

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