Insights into the mechanism of ATP-driven rotary motors from direct torque measurement

Abstract

Motor proteins are molecular machines that convert chemical energy into mechanical work. In addition to existing studies performed on the linear motors found in eukaryotic cells, researchers in biophysics have also focused on rotary motors such as F 1-ATPase. Detailed studies on the rotary F 1-ATPase motor have correlated all chemical states to specific mechanical events at the single-molecule level. Recent studies showed that there exists another ATP-driven protein motor in life: the rotary machinery that rotates archaeal flagella (archaella). Rotation speed, stepwise movement, and variable directionality of the motor of Halobacterium salinarum were described in previous studies. Here we review recent experimental work discerning the molecular mechanism underlying how the archaellar motor protein FlaI drives rotation by generation of motor torque. In combination, those studies found that rotation slows as the viscous drag of markers increases, but torque remains constant at 160 pN•nm independent of rotation speed. Unexpectedly, the estimated work done in a single rotation is twice the expected energy that would come from hydrolysis of six ATP molecules in the FlaI hexamer. To reconcile the apparent contradiction, a new and general model for the mechanism of ATP-driven rotary motors is discussed.

2019—A year in Biophysical Reviews

“…These opening remarks were complemented by series of excellent Commentaries describing areas of structural biology as diverse as protein production (Owens and Gileadi, 2019), x-ray crystallography (Garman 2019), cryo-electron microscopy (Bhella 2019) and soft x-ray tomography (Pereiro 2019). These Commentaries were followed by an array of equally high-quality review articles as evidenced from the few following examples describing; synchrotron x-ray radiation (Iwamoto 2019); structural studies of protein-protein interaction modulating factors (Mabonga and Kappo, 2019); angiotensin drug discovery (Lubbe and Sturrock 2019); structural analysis of virus capsids (Conley and Bhella 2019); heat shock protein structure and function (Chakafana et al 2019); small wavelength cellular tomography (Groen et al 2019); structural analysis based on combined usage of electron paramagnetic resonance (EPR)/nuclear magnetic resonance techniques (Kachooei et al 2019) and mesoscopic structural analysis and inference based on fluorescence and optical microscopies (Mueller et al 2019;Nishizaka et al 2019). Massimo Vasalli were also responsible for organizing the Meeting.…”

Enzyme Engineering by Force: DNA Springs for the Modulation of Biocatalytic Trajectories

“…11,12 Many proteins can generate or respond to mechanical forces. 13,14 Force-generating proteins include rotary motors like the F1-ATPase, which induces torque generation, 15 and linear motors like myosins, kinesins, and dyneins, which use hydrolysis for linear motion. 16 Mechanosensitive (MS) ion channel proteins, which change conformation upon sensing external forces, 17−19 cytoplasmic proteins, which undergo force-regulated proteolytic cleavage, 20,21 and structural proteins, which modulate cell adhesion properties as a result of force-sensitive localization, are examples of proteins that respond to external mechanical stimuli.…”

Micro-DC rotary-motor working smoothly with neither contact brush nor fixed-axis

“…On the other hand, biological systems use motile micro-machines such as flagella, cilia, and other locomotive apparatus, which work smoothly through the dissipation of chemical energy (e.g., ATP hydrolysis). [5][6][7][8] Generating artificial micromotors under a large viscous effect (Re ≪ 1) is scientifically and technologically important, and several attempts have been reported. Regarding the phenomenon of self-rotation driven by direct current (DC) electrical potential in micro-scale, Quincke rotation is well known.…”