Atypical subunit composition of the chlorophycean mitochondrial F1FO ATP synthase and role of Asa7 protein in stability and oligomycin resistance of the enzyme.
[en] Background. In yeast, mammals, and land plants, mitochondrial F(1)F(O) ATP synthase (complex V) is a remarkable enzymatic machinery which comprises about 15 conserved subunits. Peculiar among eukaryotes, complex V from Chlamydomonadales algae (order of chlorophycean class) has an atypical subunit composition of its peripheral stator and dimerization module, with 9 subunits of unknown evolutionary origin (Asa subunits). In vitro, this enzyme exhibits an increased stability of its dimeric form, and in vivo, Chlamydomonas reinhardtii cells are insensitive to oligomycins, which are potent inhibitors of proton translocation through the F(O) moiety. Methodology/Principal Findings. In this work, we showed that the atypical features of the Chlamydomonadales complex V enzyme are shared by the other chlorophycean orders. By biochemical and in silico analyses, we detected several atypical Asa subunits in Scenedesmus obliquus (Sphaeropleales) and Chlorococcum ellipsoideum (Chlorococcales). In contrast, Complex V has a canonical subunit composition in other classes of Chlorophytes (Trebouxiophyceae, Prasinophyceae, and Ulvophyceae) as well as in Streptophytes (land plants) and in Rhodophytes (red algae). Growth, respiration and ATP levels in Chlorophyceae were also barely affected by oligomycin concentrations that affect representatives of the other classes of Chlorophytes. We finally studied the function of the Asa7 atypical subunit by using RNA interference in C. reinhardtii. Although the loss of Asa7 subunit has no impact on cell bioenergetics or mitochondrial structures, it destabilizes in vitro the enzyme dimeric form and renders growth, respiration and ATP level sensitive to oligomycins. Conclusions/Significance. Altogether, our results suggest that the loss of canonical components of the Complex V stator happened at the root of chlorophycean lineage and was accompanied by the recruitment of novel polypeptides. Such a massive modification of Complex V stator features might have conferred novel properties, including the stabilization of the enzyme dimeric form and the shielding of the proton channel. In these respects, we discuss an evolutionary scenario for F(1)F(O) ATP synthase in the whole green lineage (i.e. Chlorophyta and Streptophyta).
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Lapaille, Marie
Escobar-Ramirez, Adelma
Degand, Hervé
Baurain, Denis ; Université de Liège - ULiège > Département de productions animales > GIGA-R : Génomique animale
Rodriguez-Salianas, Eizabeth
Coosemans, Nadine ; Université de Liège - ULiège > Département des sciences de la vie > DES en biotechnologie
Boutry, Marc
Gonzalez-Halphen, Diego
Remacle, Claire ; Université de Liège - ULiège > Département des sciences de la vie > Génétique
Cardol, Pierre ; Université de Liège - ULiège > Département des sciences de la vie > Génétique
Language :
English
Title :
Atypical subunit composition of the chlorophycean mitochondrial F1FO ATP synthase and role of Asa7 protein in stability and oligomycin resistance of the enzyme.
Publication date :
July 2010
Journal title :
Molecular Biology and Evolution
ISSN :
0737-4038
eISSN :
1537-1719
Publisher :
Oxford University Press, New York, United States - New York
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