Structural basis of mitochondrial membrane bending by the I–II–III2–IV2 supercomplex

Alexander Mühleip, Rasmus Kock Flygaard, Rozbeh Baradaran, Outi Haapanen, Thomas Gruhl, Victor Tobiasson, Amandine Maréchal, Vivek Sharma and Alexey Amunts ()
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Alexander Mühleip: Stockholm University
Rasmus Kock Flygaard: Stockholm University
Rozbeh Baradaran: Stockholm University
Outi Haapanen: University of Helsinki
Thomas Gruhl: Birkbeck College
Victor Tobiasson: Stockholm University
Amandine Maréchal: Birkbeck College
Vivek Sharma: University of Helsinki
Alexey Amunts: Stockholm University

Nature, 2023, vol. 615, issue 7954, 934-938

Abstract: Abstract Mitochondrial energy conversion requires an intricate architecture of the inner mitochondrial membrane1. Here we show that a supercomplex containing all four respiratory chain components contributes to membrane curvature induction in ciliates. We report cryo-electron microscopy and cryo-tomography structures of the supercomplex that comprises 150 different proteins and 311 bound lipids, forming a stable 5.8-MDa assembly. Owing to subunit acquisition and extension, complex I associates with a complex IV dimer, generating a wedge-shaped gap that serves as a binding site for complex II. Together with a tilted complex III dimer association, it results in a curved membrane region. Using molecular dynamics simulations, we demonstrate that the divergent supercomplex actively contributes to the membrane curvature induction and tubulation of cristae. Our findings highlight how the evolution of protein subunits of respiratory complexes has led to the I–II–III2–IV2 supercomplex that contributes to the shaping of the bioenergetic membrane, thereby enabling its functional specialization.

Date: 2023
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DOI: 10.1038/s41586-023-05817-y

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