Regulation of Aerobic Energy Metabolism in Podospora anserina by Two Paralogous Genes Encoding Structurally Different c-Subunits of ATP Synthase
PLoS Genet. 2016-07-21; 12(7): e1006161
DOI: 10.1371/journal.pgen.1006161
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1. PLoS Genet. 2016 Jul 21;12(7):e1006161. doi: 10.1371/journal.pgen.1006161.
eCollection 2016 Jul.
Regulation of Aerobic Energy Metabolism in Podospora anserina by Two Paralogous
Genes Encoding Structurally Different c-Subunits of ATP Synthase.
Sellem CH(1), di Rago JP(2)(3), Lasserre JP(2)(3), Ackerman SH(4),
Sainsard-Chanet A(1).
Author information:
(1)Institute for Integrative Biology of the Cell (I2BC), CEA-CNRS-Université
Paris-Sud, Gif sur Yvette, France.
(2)CNRS, Institut de Biochimie et Génétique Cellulaires, UMR 5095, Bordeaux,
France.
(3)Université Victor Segalen-Bordeaux 2, IBGC, UMR 5095, Bordeaux, France.
(4)Department of Biochemistry and Molecular Biology, Wayne State University
School of Medicine, Detroit, Michigan, United States of America.
Most of the ATP in living cells is produced by an F-type ATP synthase. This
enzyme uses the energy of a transmembrane electrochemical proton gradient to
synthesize ATP from ADP and inorganic phosphate. Proton movements across the
membrane domain (FO) of the ATP synthase drive the rotation of a ring of 8-15
c-subunits, which induces conformational changes in the catalytic part (F1) of
the enzyme that ultimately promote ATP synthesis. Two paralogous nuclear genes,
called Atp9-5 and Atp9-7, encode structurally different c-subunits in the
filamentous fungus Podospora anserina. We have in this study identified
differences in the expression pattern for the two genes that correlate with the
mitotic activity of cells in vegetative mycelia: Atp9-7 is transcriptionally
active in non-proliferating (stationary) cells while Atp9-5 is expressed in the
cells at the extremity (apex) of filaments that divide and are responsible for
mycelium growth. When active, the Atp9-5 gene sustains a much higher rate of
c-subunit synthesis than Atp9-7. We further show that the ATP9-7 and ATP9-5
proteins have antagonist effects on the longevity of P. anserina. Finally, we
provide evidence that the ATP9-5 protein sustains a higher rate of mitochondrial
ATP synthesis and yield in ATP molecules per electron transferred to oxygen than
the c-subunit encoded by Atp9-7. These findings reveal that the c-subunit genes
play a key role in the modulation of ATP synthase production and activity along
the life cycle of P. anserina. Such a degree of sophistication for regulating
aerobic energy metabolism has not been described before.
DOI: 10.1371/journal.pgen.1006161
PMCID: PMC4956034
PMID: 27442014 [Indexed for MEDLINE]