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Title: Cryo-EM structures provide insight into how E. coli F1Fo ATP synthase accommodates symmetry mismatch

Abstract

F1Fo ATP synthase functions as a biological rotary generator that makes a major contribution to cellular energy production. It comprises two molecular motors coupled together by a central and a peripheral stalk. Proton flow through the Fo motor generates rotation of the central stalk, inducing conformational changes in the F1 motor that catalyzes ATP production. Here we present nine cryo-EM structures of E. coli ATP synthase to 3.1–3.4 Å resolution, in four discrete rotational sub-states, which provide a comprehensive structural model for this widely studied bacterial molecular machine. We observe torsional flexing of the entire complex and a rotational sub-step of Fo associated with long-range conformational changes that indicates how this flexibility accommodates the mismatch between the 3- and 10-fold symmetries of the F1 and Fo motors. We also identify density likely corresponding to lipid molecules that may contribute to the rotor/stator interaction within the Fo motor.

Authors:
 [1]; ORCiD logo [2];  [3];  [4];  [2]; ORCiD logo [3];  [4]; ORCiD logo [5]
+ Show Author Affiliations
  1. The Victor Chang Cardiac Research Inst., Darlinghurst, NSW (Australia). Molecular, Structural and Computational Biology Division; Univ. of New South Wales, Sydney, NSW (Australia). St Vincent’s Clinical School. Faculty of Medicine
  2. The Victor Chang Cardiac Research Inst., Darlinghurst, NSW (Australia). Molecular, Structural and Computational Biology Division
  3. Univ. of Oxford (United Kingdom). Dept. of Chemistry
  4. Univ. of Oxford (United Kingdom). Clarendon Lab.
  5. The Victor Chang Cardiac Research Inst., Darlinghurst, NSW (Australia). Molecular, Structural and Computational Biology Division; Univ. of New South Wales, Sydney, NSW (Australia). St Vincent’s Clinical School. Faculty of Medicine
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division
OSTI Identifier:
1816612
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 11; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Sobti, Meghna, Walshe, James L., Wu, Di, Ishmukhametov, Robert, Zeng, Yi C., Robinson, Carol V., Berry, Richard M., and Stewart, Alastair G. Cryo-EM structures provide insight into how E. coli F1Fo ATP synthase accommodates symmetry mismatch. United States: N. p., 2020. Web. doi:10.1038/s41467-020-16387-2.
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Sobti, Meghna, Walshe, James L., Wu, Di, Ishmukhametov, Robert, Zeng, Yi C., Robinson, Carol V., Berry, Richard M., & Stewart, Alastair G. Cryo-EM structures provide insight into how E. coli F1Fo ATP synthase accommodates symmetry mismatch. United States. https://doi.org/10.1038/s41467-020-16387-2
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Sobti, Meghna, Walshe, James L., Wu, Di, Ishmukhametov, Robert, Zeng, Yi C., Robinson, Carol V., Berry, Richard M., and Stewart, Alastair G. Tue . "Cryo-EM structures provide insight into how E. coli F1Fo ATP synthase accommodates symmetry mismatch". United States. https://doi.org/10.1038/s41467-020-16387-2. https://www.osti.gov/servlets/purl/1816612.
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@article{osti_1816612,
title = {Cryo-EM structures provide insight into how E. coli F1Fo ATP synthase accommodates symmetry mismatch},
author = {Sobti, Meghna and Walshe, James L. and Wu, Di and Ishmukhametov, Robert and Zeng, Yi C. and Robinson, Carol V. and Berry, Richard M. and Stewart, Alastair G.},
abstractNote = {F1Fo ATP synthase functions as a biological rotary generator that makes a major contribution to cellular energy production. It comprises two molecular motors coupled together by a central and a peripheral stalk. Proton flow through the Fo motor generates rotation of the central stalk, inducing conformational changes in the F1 motor that catalyzes ATP production. Here we present nine cryo-EM structures of E. coli ATP synthase to 3.1–3.4 Å resolution, in four discrete rotational sub-states, which provide a comprehensive structural model for this widely studied bacterial molecular machine. We observe torsional flexing of the entire complex and a rotational sub-step of Fo associated with long-range conformational changes that indicates how this flexibility accommodates the mismatch between the 3- and 10-fold symmetries of the F1 and Fo motors. We also identify density likely corresponding to lipid molecules that may contribute to the rotor/stator interaction within the Fo motor.},
doi = {10.1038/s41467-020-16387-2},
journal = {Nature Communications},
number = 1,
volume = 11,
place = {United States},
year = {Tue May 26 00:00:00 EDT 2020},
month = {Tue May 26 00:00:00 EDT 2020}
}
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https://doi.org/10.1038/s41467-020-16387-2
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