Three-color Förster resonance energy transfer within single F₀F₁-ATP synthases: monitoring elastic deformations of the rotary double motor in real time

J Biomed Opt. 2012 Jan;17(1):011004. doi: 10.1117/1.JBO.17.1.011004.

Abstract

Catalytic activities of enzymes are associated with elastic conformational changes of the protein backbone. Förster-type resonance energy transfer, commonly referred to as FRET, is required in order to observe the dynamics of relative movements within the protein. Förster-type resonance energy transfer between two specifically attached fluorophores provides a ruler with subnanometer resolution between 3 and 8 nm, submillisecond time resolution for time trajectories of conformational changes, and single-molecule sensitivity to overcome the need for synchronization of various conformations. F(O)F(1)-ATP synthase is a rotary molecular machine which catalyzes the formation of adenosine triphosphate (ATP). The Escherichia coli enzyme comprises a proton driven 10 stepped rotary F(O) motor connected to a 3-stepped F(1) motor, where ATP is synthesized. This mismatch of step sizes will result in elastic deformations within the rotor parts. We present a new single-molecule FRET approach to observe both rotary motors simultaneously in a single F(O)F(1)-ATP synthase at work. We labeled this enzyme with three fluorophores, specifically at the stator part and at the two rotors. Duty cycle-optimized with alternating laser excitation, referred to as DCO-ALEX, allowed to control enzyme activity and to unravel associated transient twisting within the rotors of a single enzyme during ATP hydrolysis and ATP synthesis. Monte Carlo simulations revealed that the rotor twisting is larger than 36 deg.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / chemistry
  • Adenosine Triphosphate / metabolism
  • Bacterial Proton-Translocating ATPases / chemistry*
  • Bacterial Proton-Translocating ATPases / metabolism
  • Carbocyanines / chemistry
  • Computer Simulation
  • Elasticity
  • Escherichia coli Proteins / chemistry*
  • Escherichia coli Proteins / metabolism
  • Fluorescence Resonance Energy Transfer*
  • Fluorescent Dyes / chemistry*
  • Green Fluorescent Proteins / chemistry
  • Models, Molecular
  • Monte Carlo Method

Substances

  • Carbocyanines
  • Escherichia coli Proteins
  • Fluorescent Dyes
  • cyanine dye 5
  • enhanced green fluorescent protein
  • Green Fluorescent Proteins
  • Adenosine Triphosphate
  • Bacterial Proton-Translocating ATPases
  • Escherichia coli Proton-Translocating ATPase