Multiple origins of hydrogenosomes: functional and phylogenetic evidence from the ADP/ATP carrier of the anaerobic chytrid Neocallimastix sp.
A mitochondrial-type ADP/ATP carrier (AAC) has been identified in the hydrogenosomes of the anaerobic chytridiomycete fungus Neocallimastix sp. L2. Biochemical and immunocytochemical studies revealed that this ADP/ATP carrier is an integral component of hydrogenosomal membranes. Expression of the corresponding cDNA in Escherichia coli confers the ability on the bacterial host to incorporate ADP at significantly higher rates than ATP--similar to isolated mitochondria of yeast and animals. Phylogenetic analysis of this AAC gene (hdgaac) confirmed with high statistical support that the hydrogenosomal ADP/ATP carrier of Neocallimastix sp. L2 belongs to the family of veritable mitochondrial-type AACs. Hydrogenosome-bearing anaerobic ciliates possess clearly distinct mitochondrial-type AACs, whereas the potential hydrogenosomal carrier Hmp31 of the anaerobic flagellate Trichomonas vaginalis and its homologue from Trichomonas gallinae do not belong to this family of proteins. Also, phylogenetic analysis of genes encoding mitochondrial-type chaperonin 60 proteins (HSP 60) supports the conclusion that the hydrogenosomes of anaerobic chytrids and anaerobic ciliates had independent origins, although both of them arose from mitochondria.
Voncken
Frank
F
Department of Evolutionary Microbiology, University of Nijmegen, Toernooiveld 1, NL-6525 ED Nijmegen, The Netherlands.
Boxma
Brigitte
B
Tjaden
Joachim
J
Akhmanova
Anna
A
Huynen
Martijn
M
Verbeek
Fons
F
Tielens
Aloysius G M
AG
Haferkamp
Ilka
I
Neuhaus
H Ekkehard
HE
Vogels
Godfried
G
Veenhuis
Marten
M
Hackstein
Johannes H P
JH
D000244:Adenosine Diphosphate / Q000378:metabolism*; D000255:Adenosine Triphosphate / Q000378:metabolism*; D000595:Amino Acid Sequence; D000818:Animals; D015153:Blotting, Western; D004926:Escherichia coli / Q000235:genetics; D006859:Hydrogen / Q000378:metabolism*; D007150:Immunohistochemistry; D008928:Mitochondria / Q000378:metabolism*; D000226:Mitochondrial ADP, ATP Translocases / Q000737:chemistry / Q000145:classification / Q000235:genetics / Q000378:metabolism*; D008969:Molecular Sequence Data; D020088:Neocallimastix / Q000145:classification / Q000201:enzymology* / Q000235:genetics / Q000378:metabolism; D010802:Phylogeny; D017386:Sequence Homology, Amino Acid; D014244:Trichomonas / Q000235:genetics
D000244:Adenosine Diphosphate; D006859:Hydrogen; D000255:Adenosine Triphosphate; D000226:Mitochondrial ADP, ATP Translocases