Abstract

Mitochondria power the energy production that builds upon the architecture of double membranes and cristae invagination. This paper revealed a novel design of mitochondrial infrastructure to integrate the energetic state of the organelle. To meet high-energy demand, mitochondria of Drosophila muscle developed extensive intra-mitochondrial membrane switches between densely packed lamellar cristae that build spiral-like cristae network and bidirectional matrix confluency. The highly interconnected architecture allows rapid equilibration of membrane potential and biomolecules across integrated regions. Mutant flies with compromised mtDNA replication accumulated mitochondria containing subareas of swirling membrane besides normal cristae, which served as a morphological marker of defective mtDNA. We visualized, at the individual mitochondrial level, the structural and functional alterations of defective mtDNA that impaired local molecular composition and function, and affected fusion/fission dynamics. However, the subarea of normal cristae managed to maintain acceptable function that camouflaged defective mtDNA from quality control elimination.

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