Abstract
The majority of adenosine triphosphate (ATP) powering cellular processes in eukaryotes is produced by the mitochondrial F1Fo ATP synthase. Here, we present the atomic models of the membrane Fo domain and the entire mammalian (ovine) F1Fo, determined by cryo-electron microscopy. Subunits in the membrane domain are arranged in the ‘proton translocation cluster’ attached to the c-ring and a more distant ‘hook apparatus’ holding subunit e. Unexpectedly, this subunit is anchored to a lipid ‘plug’ capping the c-ring. We present a detailed proton translocation pathway in mammalian Fo and key inter-monomer contacts in F1Fo multimers. Cryo-EM maps of F1Fo exposed to calcium reveal a retracted subunit e and a disassembled c-ring, suggesting permeability transition pore opening. We propose a model for the permeability transition pore opening, whereby subunit e pulls the lipid plug out of the c-ring. Our structure will allow the design of drugs for many emerging applications in medicine.
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Acknowledgements
We thank J. Novacek from CEITEC (Brno, Czech Republic) for assistance with collecting the FEI Krios dataset and iNEXT for providing access to CEITEC. We thank the IST Austria EM facility for access and assistance with collecting the FEI Glacios dataset. Data processing was performed at the IST high-performance computing cluster. This work has been supported by iNEXT EM HEDC (proposal 4506), funded by the Horizon 2020 Programme of the European Commission.
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G.P. purified ATP synthase, prepared cryo-EM grids, acquired and processed EM data and built the initial atomic model. L.Z. completed and refined the model. L.A.S. designed and supervised the project, acquired funding, processed data and wrote the manuscript. All authors analyzed data and contributed to the manuscript.
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Extended data
Extended Data Fig. 1 Purification of mammalian ATP synthase and processing chart of the State 1a F1Fo maps.
a, The last step of purification (preparation in LMNG, no divalent cations added) was sucrose gradient with fractions collected using Biocomp Instruments Gradient Station allowing A280 absorbance recording. In the elution profile M indicates monomeric peak used for collection of data on Krios TEM leading to F1Fo monomer structure, D is a dimeric peak and fractions of larger MW were used for collection of data on Glacios TEM leading to multimer structures. The associated Native and SDS-PAGE gels are shown on the right. SDS-PAGE shows expected subunit composition of the mammalian ATP synthase. b, The ‘monomer’ dataset example micrograph and 2D classes examples. c, The ‘multimer’ dataset example micrograph and 2D classes examples. d, The processing strategy for the ‘monomer’ dataset leading to the Fo consensus class map and to the composite state 1a map as described in the Methods section. e, State 1a map from the consensus refinement with F1Fo mask (at 3.8 Å overall resolution, local resolution-filtered in Relion due to lower resolution in the Fo domain) is shown alongside and overlayed with the composite 1a state F1Fo map, to illustrate their global similaritity.
Extended Data Fig. 2 Processing chart of different rotational states of the monomer and of dimers from the ‘monomer’ Krios dataset.
The strategy is described in the Methods section.
Extended Data Fig. 3 Different oligomeric states from the ‘multimer’ Glacios dataset and resolution estimates of State 1a structure determination from the ‘monomer’ Krios dataset.
a, Side-view of the tetramer from the porcine study37 with indicated angles (measured using rotational axes going through the c-ring and F1 of each fitted monomer) and distances (between the IMS side centers of the c-rings) between the protomers. b, Different oligomeric states of ovine F1Fo from the ‘multimer’ dataset (LMNG, no divalent cations) with angles and distances indicated. In the ‘up-down’ dimers the Fo-Fo contacts were tight, with direct interactions between subunits DAPIT and 6.8pl from each monomer (leftmost) or between the c-rings and DAPIT subunits (second from the left). c, Processing chart of different oligomeric states from the ‘multimer’ dataset. d, Gold-standard Fourier shell correlation (FSC) curves for the overall and F1 / Fo-focused refinements of state 1a F1Fo, as well as corresponding local resolution maps estimated with Relion 3.0 implementation. Note that the resolution scale bars differ. e, Gold-standard Fourier shell correlation (FSC) curve for the Fo-focused refinement of the consensus Fo class from all rotational states, as well as corresponding local resolution map. f, The map versus model FSC curves for the consensus Fo and state 1a F1Fo models.
Extended Data Fig. 4 Examples of cryo-EM density of protein and heteroatoms.
Representative densities of subunits α (a), β (b), OSCP (c), γ (d), catalytic ADP (o), and non-catalytic ADP and Mg2+ (p) in the F1-focus refined state 1a map. Densities for ATP8 (e), a (f), c (g), DAPIT (h), e (i), f (j), g (k), and IMS-side lipid (n) are from the Fo consensus class map. Matrix-side lipid density (m) is from the Fo-focus refined 1a state map. In panel (l) the arginine checkpoint is shown from the matrix side (arginine is marked with * here and in panel f). Note the absence of density between E58c and R159a indicating the absence of salt bridge.
Extended Data Fig. 5 Catalytic cycle and different rotational states of the mammalian F1Fo.
a, A scheme of 360° catalytic cycle with dwell angles, catalytic events and nucleotide occupancies indicated, discussed in the Supplementary Note 1. Different conformations of the three catalytic β subunits (gray, salmon and yellow) are color-coded in the circumference as green for βDP, magenta for βTP and blue for βE. Note that during one 120° rotation between the two ATP binding dwells, starting from top and moving anti-clockwise, the ATP binding, Pi release and ATP hydrolysis generate 65°, 25° and 30° rotations respectively, while ADP is released before Pi. b, Scheme 1 for MgADP inhibition, discussed in the Supplementary Note 1. c, Scheme 2 for MgADP inhibition. d, Different rotational states of ovine F1Fo and their distribution (% of particles in the class), with the degree of subunit γ rotation shown. Subunits α and β of in-between states (1_2, 2_3 and 3_1) are transparent to indicate an ambiguous fit of some of these subunits into the density. The degree of subunit γ rotation from in-between to the main states is roughly consistent with angles between dwells in a.
Extended Data Fig. 6 Comparison of different species, sequence conservation in F1Fo and surface properties of Fo.
a, Gradual flattening of the joint end of the key helix hairpin in subunit a of different ATPases. Stuctures are aligned by the c subunit that directly interacts with the arginine checkpoint in subunit a. Subunits DAPIT/k of the mitochondrial enzymes are also shown to illustrate their roles in bending helices towards the c-ring. b, Complementary surface charges of the c-ring (bottom) and the interacting surface of the central stalk (top) are shown on the right. Solvent-accessible surface is shown colored red for negative, white for neutral and blue for positive surface charges. State 1a model is shown on the left for orientation. c, Comparison of the Fo interactions in the mammalian (top) and yeast (bottom) dimers. Note the extensive contacts of subunits a and i(6.8pl) in yeast (circled). d, Mammalian ATP synthase model (in two views rotated for clarity) colored according to residue conservation from blue (most conserved) to red (least conserved). Most conserved areas are indicated. e, Side views of the dimeric Fo region with the approximate membrane position indicated according to exposed hydrophobic areas. (Left) Solvent-accessible surface charge distribution. (Right) Protein surface colored according to the Eisenberg hydrophobicity scale from white (hydrophobic) to red (hydrophilic). From both representations it is clear that the membrane has to be highly curved to accommodate a dimer (or even a monomer).
Extended Data Fig. 7 Lipids and interactions in the c-ring.
a, b, Lipid occupancies. a, Fo density of the consensus class from all the rotational states combined (3.8 Å resolution) shows clear density of the IMS-side lipid (ISL) while the matrix-side (MSL) lipid density (circled area) is blurred/averaged due to MSL rotation with the c-ring (matrix side is on top). b, In the Fo density of state 1a only (4.2 Å resolution) the MSL is better resolved due to its fixed position in one state. Density for ISL at the bottom is visible in both cases since ISL is attached to subunit e and does not rotate with the ring. c, Surface charge distribution shows that the c-ring cavity is highly hydrophobic, with lipids inside shown as spheres. The ring of V16c, indicated with green sticks, serves as a bottleneck in the 310 helix section of subunit c. d, e, Cryo-EM density straight from Fo-focused auto-refinement (no post-processing, that is B-factor is not applied) for the consensus Fo class (d) and for state 1a only (e), showing that subunit e remains helical till the C-terminus, where it is connected (arrow) to the density in the center of the c-ring. f, g, CryoEM analysis of the enzyme purified in the presence of Ca2+ (or Mg2+) ions. f, Typical 2D classes from Mg and Ca datasets. g, Slices through the Fo domain density (between two yellow lines in the Overview) viewed in the projection along the vertical axis. In the Mg monomer, the fitted model is shown as a cartoon in magenta, with yellow arrow indicating c-ring and blue arrow subunit a. At similar resolution in the Mg monomer the c-ring is clearly seen as a circular density, while it is considerably distorted in Step0 and Step1 classes and absent in Step2 and Step3. All maps of Mg and Ca monomers were pre-aligned, so the slices show identical orientation.
Extended Data Fig. 8 Purification and cryoEM data processing of ATP synthase in the presence of Mg2+ or Ca2+.
These preparations were in digitonin and started from the addition of divalent cations (5 mM of either Mg or Ca) to the intact mitochondria. a-b, The last step of purification was sucrose gradient: for the Mg dataset collected fractions included mostly tetramers (a) while for the Ca dataset mostly monomeric fractions were included (b), although these species would overlap in elution. The associated Native gels are shown below, with SDS-PAGE of selected fractions on the left. SDS-PAGE shows expected subunit composition of the mammalian ATP synthase, with α/β subunits band marked. Both tetramer and monomer fractions are dominated by ATP synthase, although some amounts of CIII and CIV co-elute with monomers. These contaminants are separated out during cryo-EM data processing. Examples of micrographs and 2D classes are shown in (c) for the Mg dataset and in (d) for the Ca dataset. Processing chart for the Mg dataset is in (e) and for the Ca dataset in (f), with details in Methods.
Supplementary information
Supplementary Information
Supplementary Note 1, Tables 1–3 and Fig. 1.
Supplementary Video 1
Catalytic cycle of the ovine ATP synthase.
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Pinke, G., Zhou, L. & Sazanov, L.A. Cryo-EM structure of the entire mammalian F-type ATP synthase. Nat Struct Mol Biol 27, 1077–1085 (2020). https://doi.org/10.1038/s41594-020-0503-8
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DOI: https://doi.org/10.1038/s41594-020-0503-8
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