Elastic coupling power stroke mechanism of the F1-ATPase molecular motor

James L. Martin, Robert Ishmukhametov, David Spetzler, Tassilo Hornung, Wayne Frasch

Research output: Contribution to journalArticle

9 Citations (Scopus)

Abstract

The angular velocity profile of the 120° F1-ATPase power stroke was resolved as a function of temperature from 16.3 to 44.6 °C using a ΔμATP = −31.25 kBT at a time resolution of 10 μs. Angular velocities during the first 60° of the power stroke (phase 1) varied inversely with temperature, resulting in negative activation energies with a parabolic dependence. This is direct evidence that phase 1 rotation derives from elastic energy (spring constant, κ = 50 kBT·rad−2). Phase 2 of the power stroke had an enthalpic component indicating that additional energy input occurred to enable the γ-subunit to overcome energy stored by the spring after rotating beyond its 34° equilibrium position. The correlation between the probability distribution of ATP binding to the empty catalytic site and the negative Ea values of the power stroke during phase 1 suggests that this additional energy is derived from the binding of ATP to the empty catalytic site. A second torsion spring (κ = 150 kBT·rad−2; equilibrium position, 90°) was also evident that mitigated the enthalpic cost of phase 2 rotation. The maximum ΔGǂ was 22.6 kBT, and maximum efficiency was 72%. An elastic coupling mechanism is proposed that uses the coiled-coil domain of the γ-subunit rotor as a torsion spring during phase 1, and then as a crankshaft driven by ATP-binding–dependent conformational changes during phase 2 to drive the power stroke.

Original languageEnglish (US)
Pages (from-to)5750-5755
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume115
Issue number22
DOIs
StatePublished - May 29 2018

Fingerprint

Proton-Translocating ATPases
Stroke
Adenosine Triphosphate
Catalytic Domain
Temperature
Costs and Cost Analysis

Keywords

  • F-type ATP synthase
  • F1-ATPase
  • FOF1 ATP synthase
  • Power stroke mechanism
  • Single molecule

ASJC Scopus subject areas

  • General

Cite this

Elastic coupling power stroke mechanism of the F1-ATPase molecular motor. / Martin, James L.; Ishmukhametov, Robert; Spetzler, David; Hornung, Tassilo; Frasch, Wayne.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, No. 22, 29.05.2018, p. 5750-5755.

Research output: Contribution to journalArticle

Martin, James L. ; Ishmukhametov, Robert ; Spetzler, David ; Hornung, Tassilo ; Frasch, Wayne. / Elastic coupling power stroke mechanism of the F1-ATPase molecular motor. In: Proceedings of the National Academy of Sciences of the United States of America. 2018 ; Vol. 115, No. 22. pp. 5750-5755.
@article{99812512859d4010bd05603fc8eb29cc,
title = "Elastic coupling power stroke mechanism of the F1-ATPase molecular motor",
abstract = "The angular velocity profile of the 120° F1-ATPase power stroke was resolved as a function of temperature from 16.3 to 44.6 °C using a ΔμATP = −31.25 kBT at a time resolution of 10 μs. Angular velocities during the first 60° of the power stroke (phase 1) varied inversely with temperature, resulting in negative activation energies with a parabolic dependence. This is direct evidence that phase 1 rotation derives from elastic energy (spring constant, κ = 50 kBT·rad−2). Phase 2 of the power stroke had an enthalpic component indicating that additional energy input occurred to enable the γ-subunit to overcome energy stored by the spring after rotating beyond its 34° equilibrium position. The correlation between the probability distribution of ATP binding to the empty catalytic site and the negative Ea values of the power stroke during phase 1 suggests that this additional energy is derived from the binding of ATP to the empty catalytic site. A second torsion spring (κ = 150 kBT·rad−2; equilibrium position, 90°) was also evident that mitigated the enthalpic cost of phase 2 rotation. The maximum ΔGǂ was 22.6 kBT, and maximum efficiency was 72{\%}. An elastic coupling mechanism is proposed that uses the coiled-coil domain of the γ-subunit rotor as a torsion spring during phase 1, and then as a crankshaft driven by ATP-binding–dependent conformational changes during phase 2 to drive the power stroke.",
keywords = "F-type ATP synthase, F1-ATPase, FOF1 ATP synthase, Power stroke mechanism, Single molecule",
author = "Martin, {James L.} and Robert Ishmukhametov and David Spetzler and Tassilo Hornung and Wayne Frasch",
year = "2018",
month = "5",
day = "29",
doi = "10.1073/pnas.1803147115",
language = "English (US)",
volume = "115",
pages = "5750--5755",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "22",

}

TY - JOUR

T1 - Elastic coupling power stroke mechanism of the F1-ATPase molecular motor

AU - Martin, James L.

AU - Ishmukhametov, Robert

AU - Spetzler, David

AU - Hornung, Tassilo

AU - Frasch, Wayne

PY - 2018/5/29

Y1 - 2018/5/29

N2 - The angular velocity profile of the 120° F1-ATPase power stroke was resolved as a function of temperature from 16.3 to 44.6 °C using a ΔμATP = −31.25 kBT at a time resolution of 10 μs. Angular velocities during the first 60° of the power stroke (phase 1) varied inversely with temperature, resulting in negative activation energies with a parabolic dependence. This is direct evidence that phase 1 rotation derives from elastic energy (spring constant, κ = 50 kBT·rad−2). Phase 2 of the power stroke had an enthalpic component indicating that additional energy input occurred to enable the γ-subunit to overcome energy stored by the spring after rotating beyond its 34° equilibrium position. The correlation between the probability distribution of ATP binding to the empty catalytic site and the negative Ea values of the power stroke during phase 1 suggests that this additional energy is derived from the binding of ATP to the empty catalytic site. A second torsion spring (κ = 150 kBT·rad−2; equilibrium position, 90°) was also evident that mitigated the enthalpic cost of phase 2 rotation. The maximum ΔGǂ was 22.6 kBT, and maximum efficiency was 72%. An elastic coupling mechanism is proposed that uses the coiled-coil domain of the γ-subunit rotor as a torsion spring during phase 1, and then as a crankshaft driven by ATP-binding–dependent conformational changes during phase 2 to drive the power stroke.

AB - The angular velocity profile of the 120° F1-ATPase power stroke was resolved as a function of temperature from 16.3 to 44.6 °C using a ΔμATP = −31.25 kBT at a time resolution of 10 μs. Angular velocities during the first 60° of the power stroke (phase 1) varied inversely with temperature, resulting in negative activation energies with a parabolic dependence. This is direct evidence that phase 1 rotation derives from elastic energy (spring constant, κ = 50 kBT·rad−2). Phase 2 of the power stroke had an enthalpic component indicating that additional energy input occurred to enable the γ-subunit to overcome energy stored by the spring after rotating beyond its 34° equilibrium position. The correlation between the probability distribution of ATP binding to the empty catalytic site and the negative Ea values of the power stroke during phase 1 suggests that this additional energy is derived from the binding of ATP to the empty catalytic site. A second torsion spring (κ = 150 kBT·rad−2; equilibrium position, 90°) was also evident that mitigated the enthalpic cost of phase 2 rotation. The maximum ΔGǂ was 22.6 kBT, and maximum efficiency was 72%. An elastic coupling mechanism is proposed that uses the coiled-coil domain of the γ-subunit rotor as a torsion spring during phase 1, and then as a crankshaft driven by ATP-binding–dependent conformational changes during phase 2 to drive the power stroke.

KW - F-type ATP synthase

KW - F1-ATPase

KW - FOF1 ATP synthase

KW - Power stroke mechanism

KW - Single molecule

UR - http://www.scopus.com/inward/record.url?scp=85047895615&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85047895615&partnerID=8YFLogxK

U2 - 10.1073/pnas.1803147115

DO - 10.1073/pnas.1803147115

M3 - Article

VL - 115

SP - 5750

EP - 5755

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 22

ER -