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Method to extract multiple states in F₁-ATPase rotation experiments from jump distributions

Volkán-Kacsó, Sándor and Le, Luan Q. and Zhu, Kaicheng and Su, Haibin and Marcus, Rudolph A. (2019) Method to extract multiple states in F₁-ATPase rotation experiments from jump distributions. Proceedings of the National Academy of Sciences of the United States of America, 116 (51). pp. 25456-25461. ISSN 0027-8424. https://resolver.caltech.edu/CaltechAUTHORS:20191127-111513039

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Abstract

A method is proposed for analyzing fast (10 μs) single-molecule rotation trajectories in F₁ adenosinetriphosphatase (F₁-ATPase). This method is based on the distribution of jumps in the rotation angle that occur in the transitions during the steps between subsequent catalytic dwells. The method is complementary to the “stalling” technique devised by H. Noji et al. [Biophys. Rev. 9, 103–118, 2017], and can reveal multiple states not directly detectable as steps. A bimodal distribution of jumps is observed at certain angles, due to the system being in either of 2 states at the same rotation angle. In this method, a multistate theory is used that takes into account a viscoelastic fluctuation of the imaging probe. Using an established sequence of 3 specific states, a theoretical profile of angular jumps is predicted, without adjustable parameters, that agrees with experiment for most of the angular range. Agreement can be achieved at all angles by assuming a fourth state with an ∼10 μs lifetime and a dwell angle about 40° after the adenosine 5′-triphosphate (ATP) binding dwell. The latter result suggests that the ATP binding in one β subunit and the adenosine 5′-diphosphate (ADP) release from another β subunit occur via a transient whose lifetime is ∼10 μs and is about 6 orders of magnitude smaller than the lifetime for ADP release from a singly occupied F₁-ATPase. An internal consistency test is given by comparing 2 independent ways of obtaining the relaxation time of the probe. They agree and are ∼15 μs.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1073/pnas.1915314116DOIArticle
https://www.pnas.org/content/suppl/2019/11/26/1915314116.DCSupplementalPublisherSupporting Information
ORCID:
AuthorORCID
Zhu, Kaicheng0000-0003-0218-4985
Su, Haibin0000-0001-9760-6567
Marcus, Rudolph A.0000-0001-6547-1469
Additional Information:© 2019 National Academy of Sciences. Published under the PNAS license. Contributed by Rudolph A. Marcus, October 23, 2019 (sent for review September 4, 2019; reviewed by Hiroyuki Noji and Attila Szabo). PNAS first published November 27, 2019. We thank Drs. Hiroshi Ueno and Hiroyuki Noji for sharing their single-molecule rotation data for use in this analysis. L.Q.L. acknowledges the support from Ian Ferguson Postgraduate Fellowship for his stay at California Institute of Technology. This work was also supported by the Office of the Naval Research, the Army Research Office, the James W. Glanville Foundation, the Society of Interdisciplinary Research, and Hong Kong University of Science and Technology Grants IGN17SC04 and R9418. Data Availability: Computer code (Matlab) for simulations and data analysis is available upon request from the authors. Author contributions: S.V.-K., H.S., and R.A.M. designed research; S.V.-K., L.Q.L., and K.Z. performed research; S.V.-K. and L.Q.L. analyzed data; and S.V.-K., L.Q.L., and R.A.M. wrote the paper. Reviewers: H.N., University of Tokyo; and A.S., NIH. The authors declare no competing interest. This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1915314116/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
CaltechUNSPECIFIED
Office of Naval Research (ONR)UNSPECIFIED
Army Research Office (ARO)UNSPECIFIED
James W. Glanville FoundationUNSPECIFIED
Society of Interdisciplinary ResearchUNSPECIFIED
Hong Kong University of Science and TechnologyIGN17SC04
Hong Kong University of Science and TechnologyR9418
Subject Keywords:F-ATPase; single-molecule imaging; concerted dynamics; 4-state model; ADP release
Issue or Number:51
Record Number:CaltechAUTHORS:20191127-111513039
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20191127-111513039
Official Citation:Method to extract multiple states in F1-ATPase rotation experiments from jump distributions. Sándor Volkán-Kacsó, Luan Q. Le, Kaicheng Zhu, Haibin Su, Rudolph A. Marcus. Proceedings of the National Academy of Sciences Dec 2019, 116 (51) 25456-25461; DOI: 10.1073/pnas.1915314116
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:100103
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:27 Nov 2019 19:26
Last Modified:18 Dec 2019 19:14

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