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An ancestral interaction module promotes oligomerization in divergent mitochondrial ATP synthases

Author

Listed:
  • Ondřej Gahura

    (Biology Centre, Czech Academy of Sciences)

  • Alexander Mühleip

    (Stockholm University)

  • Carolina Hierro-Yap

    (Biology Centre, Czech Academy of Sciences
    University of South Bohemia)

  • Brian Panicucci

    (Biology Centre, Czech Academy of Sciences)

  • Minal Jain

    (Biology Centre, Czech Academy of Sciences
    University of South Bohemia)

  • David Hollaus

    (University of South Bohemia)

  • Martina Slapničková

    (Biology Centre, Czech Academy of Sciences)

  • Alena Zíková

    (Biology Centre, Czech Academy of Sciences
    University of South Bohemia)

  • Alexey Amunts

    (Stockholm University)

Abstract

Mitochondrial ATP synthase forms stable dimers arranged into oligomeric assemblies that generate the inner-membrane curvature essential for efficient energy conversion. Here, we report cryo-EM structures of the intact ATP synthase dimer from Trypanosoma brucei in ten different rotational states. The model consists of 25 subunits, including nine lineage-specific, as well as 36 lipids. The rotary mechanism is influenced by the divergent peripheral stalk, conferring a greater conformational flexibility. Proton transfer in the lumenal half-channel occurs via a chain of five ordered water molecules. The dimerization interface is formed by subunit-g that is critical for interactions but not for the catalytic activity. Although overall dimer architecture varies among eukaryotes, we find that subunit-g together with subunit-e form an ancestral oligomerization motif, which is shared between the trypanosomal and mammalian lineages. Therefore, our data defines the subunit-g/e module as a structural component determining ATP synthase oligomeric assemblies.

Suggested Citation

  • Ondřej Gahura & Alexander Mühleip & Carolina Hierro-Yap & Brian Panicucci & Minal Jain & David Hollaus & Martina Slapničková & Alena Zíková & Alexey Amunts, 2022. "An ancestral interaction module promotes oligomerization in divergent mitochondrial ATP synthases," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33588-z
    DOI: 10.1038/s41467-022-33588-z
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    1. Kallol Gupta & Joseph A. C. Donlan & Jonathan T. S. Hopper & Povilas Uzdavinys & Michael Landreh & Weston B. Struwe & David Drew & Andrew J. Baldwin & Phillip J. Stansfeld & Carol V. Robinson, 2017. "The role of interfacial lipids in stabilizing membrane protein oligomers," Nature, Nature, vol. 541(7637), pages 421-424, January.
    2. Meghna Sobti & James L. Walshe & Di Wu & Robert Ishmukhametov & Yi C. Zeng & Carol V. Robinson & Richard M. Berry & Alastair G. Stewart, 2020. "Cryo-EM structures provide insight into how E. coli F1Fo ATP synthase accommodates symmetry mismatch," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    3. Rasmus Kock Flygaard & Alexander Mühleip & Victor Tobiasson & Alexey Amunts, 2020. "Type III ATP synthase is a symmetry-deviated dimer that induces membrane curvature through tetramerization," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
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