An anaerobic mitochondrion that produces hydrogen

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. 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.