Abstract
Mitochondria are ubiquitous organelles of eukaryotic organisms with a number of essential functions, including synthesis of iron-sulfur clusters, amino acids, lipids, and adenosine triphosphate (ATP). During aging of the fungal aging model Podospora anserina, the inner mitochondrial membrane (IMM) undergoes prominent morphological alterations, ultimately resulting in functional impairments. Since phospholipids (PLs) are key components of biological membranes, maintenance of membrane plasticity and integrity via regulation of PL biosynthesis is indispensable. Here, we report results from a lipidomic analysis of isolated mitochondria from P. anserina that revealed an age-related reorganization of the mitochondrial PL profile and the involvement of the i-AAA protease PaIAP in proteolytic regulation of PL metabolism. The absence of PaIAP enhances biosynthesis of characteristic mitochondrial PLs, leads to significant alterations in the acyl composition of the mitochondrial signature PL cardiolipin (CL), and induces mitophagy. These alterations presumably cause the lifespan increase of the PaIap deletion mutant under standard growth conditions. However, PaIAP is required at elevated temperatures and for degradation of superfluous CL synthase PaCRD1 during glycolytic growth. Overall, our study uncovers a prominent role of PaIAP in the regulation of PL homeostasis in order to adapt membrane plasticity to fluctuating environmental conditions as they occur in nature.
Highlights
Aging of biological systems is a complex and, yet, not fully understood process concerning virtually all living beings
Previous studies revealed substantial age-associated changes of mitochondrial morphotypes in P. anserina [42] and massive remodeling of the inner mitochondrial membrane (IMM) leading to a shift from lamellar cristae to a vesiculated ultrastructure [43]
In order to elucidate the impact of mitochondrial lipids on aging in P. anserina, we set out to analyze the membrane composition of the wild type in different age stages
Summary
Aging of biological systems is a complex and, yet, not fully understood process concerning virtually all living beings. The main emphasis of this research was placed on the age-related reorganization of mitochondrial DNA (mtDNA) [7], as well as various proteins participating in essential cellular processes and pathways, ensuring a healthy population of mitochondria over time [8,9,10]. These studies provided a deep insight into molecular mechanisms of organismic aging. We report that this protease is involved in the control of PL homeostasis and is essential for the ability of the fungus to adapt to natural fluctuations of environmental conditions
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