Electron tomographic analysis reveals ultrastructural features of mitochondrial cristae architecture which reflect energetic state and aging

Yi-Fan Jiang,Han-Zen Tsai,Tao-Shih Hsieh,Chi-Yu Fu,Shao-Syuan Lin,Jing-Min Chen

doi:10.1038/srep45474

Abstract

Within mitochondria, the ability to produce energy relies upon the architectural hallmarks of double membranes and cristae invaginations. Herein, we describe novel features of mitochondrial cristae structure, which correspond to the energetic state of the organelle. In concordance with high-energy demand, mitochondria of Drosophila indirect flight muscle exhibited extensive intra-mitochondrial membrane switches between densely packed lamellar cristae that resulted in a spiral-like cristae network and allowed for bidirectional matrix confluency. This highly interconnected architecture is expected to allow rapid equilibration of membrane potential and biomolecules across integrated regions. In addition, mutant flies with mtDNA replication defect and an accelerated aging phenotype accumulated mitochondria that contained subsections of swirling membrane alongside normal cristae. The swirling membrane had impaired energy production capacity as measured by protein composition and function. Furthermore, mitochondrial fusion and fission dynamics were affected in the prematurely aged flies. Interestingly, the normal cristae that remained in the mitochondria with swirling membranes maintained acceptable function that camouflaged them from quality control elimination. Overall, structural features of mitochondrial cristae were described in three-dimension from serial section electron tomographic analysis which reflect energetic state and mtDNA-mediated aging.

Highlights

Deletions and an increased amount of replication related concatamers compared to the Rescue wild-type (RWT) flies[10]
Mitochondria can organize as a reticulated super-structure that undergoes dynamic fusion and fission events to optimize collective cellular function[20]
This process may facilitate the propagation of bioenergetic and apoptotic signaling throughout the mitochondrial reticulum[21]. In addition to these inter-organelle connections, in this paper, we describe intra-mitochondrial membrane switches between lamellar cristae that build spiral-like cristae webs and allow a physical means to achieve bidirectional matrix confluency

Summary

Introduction

Deletions and an increased amount of replication related concatamers compared to the Rescue wild-type (RWT) flies[10]. IFM mitochondria contain outer, inner boundary membranes and cristae invaginations (Fig. 1B,C). Spiral-like cristae switches and bidirectional matrix confluency create robust, physical, intra-organelle connectivity that is expected to facilitate swift equilibration of membrane potential and biomolecules throughout the mitochondrion in response to changing demands or inter-mitochondrial dynamic changes.

Results

Conclusion