IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-33588-z.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-33588-z
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-33588-z?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. 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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Zhaoxiang He & Mengchen Wu & Hongtao Tian & Liangdong Wang & Yiqi Hu & Fangzhu Han & Jiancang Zhou & Yong Wang & Long Zhou, 2024. "Euglena’s atypical respiratory chain adapts to the discoidal cristae and flexible metabolism," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Fangzhu Han & Yiqi Hu & Mengchen Wu & Zhaoxiang He & Hongtao Tian & Long Zhou, 2023. "Structures of Tetrahymena thermophila respiratory megacomplexes on the tubular mitochondrial cristae," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Vishal Maingi & Zhao Zhang & Chris Thachuk & Namita Sarraf & Edwin R. Chapman & Paul W. K. Rothemund, 2023. "Digital nanoreactors to control absolute stoichiometry and spatiotemporal behavior of DNA receptors within lipid bilayers," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Jixing Lyu & Chang Liu & Tianqi Zhang & Samantha Schrecke & Nicklaus P. Elam & Charles Packianathan & Georg K. A. Hochberg & David Russell & Minglei Zhao & Arthur Laganowsky, 2022. "Structural basis for lipid and copper regulation of the ABC transporter MsbA," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    4. Takaaki A. Kobayashi & Hiroto Shimada & Fumiya K. Sano & Yuzuru Itoh & Sawako Enoki & Yasushi Okada & Tsukasa Kusakizako & Osamu Nureki, 2024. "Dimeric transport mechanism of human vitamin C transporter SVCT1," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    5. Yongchan Lee & Pattama Wiriyasermkul & Pornparn Kongpracha & Satomi Moriyama & Deryck J. Mills & Werner Kühlbrandt & Shushi Nagamori, 2022. "Ca2+-mediated higher-order assembly of heterodimers in amino acid transport system b0,+ biogenesis and cystinuria," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    6. Junke Liu & Hengmin Tang & Chanjuan Xu & Shengnan Zhou & Xunying Zhu & Yuanyuan Li & Laurent Prézeau & Tao Xu & Jean-Philippe Pin & Philippe Rondard & Wei Ji & Jianfeng Liu, 2022. "Biased signaling due to oligomerization of the G protein-coupled platelet-activating factor receptor," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    7. Di Wu & Renhong Yan & Siyuan Song & Andrew K. Swansiger & Yaning Li & James S. Prell & Qiang Zhou & Carol V. Robinson, 2024. "The complete assembly of human LAT1-4F2hc complex provides insights into its regulation, function and localisation," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    8. Tianqi Zhang & Jixing Lyu & Bowei Yang & Sangho D. Yun & Elena Scott & Minglei Zhao & Arthur Laganowsky, 2024. "Native mass spectrometry and structural studies reveal modulation of MsbA–nucleotide interactions by lipids," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    9. Abraham O. Oluwole & Robin A. Corey & Chelsea M. Brown & Victor M. Hernández-Rocamora & Phillip J. Stansfeld & Waldemar Vollmer & Jani R. Bolla & Carol V. Robinson, 2022. "Peptidoglycan biosynthesis is driven by lipid transfer along enzyme-substrate affinity gradients," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    10. Iven Winkelmann & Povilas Uzdavinys & Ian M. Kenney & Joseph Brock & Pascal F. Meier & Lina-Marie Wagner & Florian Gabriel & Sukkyeong Jung & Rei Matsuoka & Christoph Ballmoos & Oliver Beckstein & Dav, 2022. "Crystal structure of the Na+/H+ antiporter NhaA at active pH reveals the mechanistic basis for pH sensing," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    11. Atsushi Yamagata & Yoshiko Murata & Kosuke Namba & Tohru Terada & Shuya Fukai & Mikako Shirouzu, 2022. "Uptake mechanism of iron-phytosiderophore from the soil based on the structure of yellow stripe transporter," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    12. Zhaoxiang He & Mengchen Wu & Hongtao Tian & Liangdong Wang & Yiqi Hu & Fangzhu Han & Jiancang Zhou & Yong Wang & Long Zhou, 2024. "Euglena’s atypical respiratory chain adapts to the discoidal cristae and flexible metabolism," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33588-z. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.