An anaerobic mitochondrion that produces hydrogen.
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.
Boxma
Brigitte
B
Department of Evolutionary Microbiology, Faculty of Science, Radboud University Nijmegen, Toernooiveld 1, NL-6525 ED Nijmegen, The Netherlands.
de Graaf
Rob M
RM
van der Staay
Georg W M
GW
van Alen
Theo A
TA
Ricard
Guenola
G
Gabaldón
Toni
T
van Hoek
Angela H A M
AH
Moon-van der Staay
Seung Yeo
SY
Koopman
Werner J H
WJ
van Hellemond
Jaap J
JJ
Tielens
Aloysius G M
AG
Friedrich
Thorsten
T
Veenhuis
Marten
M
Huynen
Martijn A
MA
Hackstein
Johannes H P
JH
D000693:Anaerobiosis; D000818:Animals; D016798:Ciliophora / Q000166:cytology* / Q000235:genetics / Q000378:metabolism* / Q000648:ultrastructure; D003058:Cockroaches / Q000469:parasitology; D004272:DNA, Mitochondrial / Q000235:genetics; D004579:Electron Transport; D042967:Electron Transport Complex I / Q000037:antagonists & inhibitors / Q000378:metabolism; D016678:Genome; D005947:Glucose / Q000378:metabolism; D006859:Hydrogen / Q000378:metabolism*; D008928:Mitochondria / Q000201:enzymology / Q000235:genetics / Q000378:metabolism* / Q000648:ultrastructure; D008969:Molecular Sequence Data; D016366:Open Reading Frames / Q000235:genetics; D015388:Organelles / Q000187:drug effects / Q000235:genetics / Q000378:metabolism / Q000648:ultrastructure; D010802:Phylogeny; D020543:Proteome
D004272:DNA, Mitochondrial; D020543:Proteome; D006859:Hydrogen; D042967:Electron Transport Complex I; D005947:Glucose