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

<div class='caption-title'>The supercomplex contains all four ETC components.</div>
<div class='caption-title'>The CI–CIV association and binding of CII.</div>
<div class='caption-title'>An altered CI–CIII2 interface maintains functional symmetry of CIII2.</div>
Mühleip A, Flygaard RK, Baradaran R, Haapanen O, Gruhl T, Tobiasson V, Maréchal A, Sharma V, Amunts A
OpenAccess logo Nature 615 934-938 (2023)
Related entries: 8b6f, 8b6g, 8b6h

Cited: 12 times
EuropePMC logo PMID: 36949187

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.

Reviews citing this publication (7)

  1. The mystery of massive mitochondrial complexes: the apicomplexan respiratory chain. Maclean AE, Hayward JA, Huet D, van Dooren GG, Sheiner L. Trends Parasitol 38 1041-1052 (2022)
  2. The biogenesis and regulation of the plant oxidative phosphorylation system. Ghifari AS, Saha S, Murcha MW. Plant Physiol 192 728-747 (2023)
  3. The functional significance of mitochondrial respiratory chain supercomplexes. Kohler A, Barrientos A, Fontanesi F, Ott M. EMBO Rep 24 e57092 (2023)
  4. An evolving view of complex II-noncanonical complexes, megacomplexes, respiration, signaling, and beyond. Iverson TM, Singh PK, Cecchini G. J Biol Chem 299 104761 (2023)
  5. Mitochondrial Oxidative Phosphorylation in Viral Infections. Purandare N, Ghosalkar E, Grossman LI, Aras S. Viruses 15 2380 (2023)
  6. Mitochondrial proteome research: the road ahead. Baker ZN, Forny P, Pagliarini DJ. Nat Rev Mol Cell Biol (2023)
  7. Six Functions of Respiration: Isn't It Time to Take Control over ROS Production in Mitochondria, and Aging Along with It? Skulachev VP, Vyssokikh MY, Chernyak BV, Mulkidjanian AY, Skulachev MV, Shilovsky GA, Lyamzaev KG, Borisov VB, Severin FF, Sadovnichii VA. Int J Mol Sci 24 12540 (2023)

Articles citing this publication (5)

  1. Mesoscale simulation of biomembranes with FreeDTS. Pezeshkian W, Ipsen JH. Nat Commun 15 548 (2024)
  2. An essential role for an Fe-S cluster protein in the cytochrome c oxidase complex of Toxoplasma parasites. Leonard RA, Tian Y, Tan F, van Dooren GG, Hayward JA. PLoS Pathog 19 e1011430 (2023)
  3. Functional and biochemical characterization of the Toxoplasma gondii succinate dehydrogenase complex. Silva MF, Douglas K, Sandalli S, Maclean AE, Sheiner L. PLoS Pathog 19 e1011867 (2023)
  4. Structures of Tetrahymena thermophila respiratory megacomplexes on the tubular mitochondrial cristae. Han F, Hu Y, Wu M, He Z, Tian H, Zhou L. Nat Commun 14 2542 (2023)
  5. The Ancestral Shape of the Access Proton Path of Mitochondrial ATP Synthases Revealed by a Split Subunit-a. Wong JE, Zíková A, Gahura O. Mol Biol Evol 40 msad146 (2023)


Related citations provided by authors (1)

  1. Structural basis of mitochondrial membrane bending by I-II-III2-IV2 supercomplex. Muhleip A, Flygaard RK, Haapanen O, Baradaran R, Gruhl T, Tobiasson V, Marechal A, Sharma V, Amunts A Biorxiv - (2022)

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