Osmomechanics of the Propionigenium modestum Fo Motor (original) (raw)
Related papers
Energy transduction in the sodium F-ATPase of Propionigenium modestum
Proceedings of the National Academy of Sciences, 1999
The F-ATPase of the bacterium Propionigenium modestum is driven by an electrochemical sodium gradient between the cell interior and its environment. Here we present a mechanochemical model for the transduction of transmembrane sodium-motive force into rotary torque. The same mechanism is likely to operate in other F-ATPases, including the proton-driven F-ATPases of Escherichia coli.
Torque generation by the Fo motor of the sodium ATPase
Biophysical journal, 2004
Based on recent structural and functional findings, we have constructed a mathematical model for the sodiumdriven F o motor of the F 1 F o -ATPase from the anaerobic bacterium Propionigenium modestum. The model reveals the mechanochemical principles underlying the F o motor's operation, and explains all of the existing experimental data on wild-type and mutant F o motors. In particular, the model predicts a nonmonotonic dependence of the ATP hydrolysis activity on the sodium concentration, a prediction confirmed by new experiments. To explain experimental observations, the positively charged stator residue (R227) must assume different positions in the ATP synthesis and hydrolysis directions. This work also illustrates how to extract a motor mechanism from dynamical experimental observations in the absence of complete structural information.
Biochimica et Biophysica Acta (BBA) - Bioenergetics, 2000
The mechanism of converting an electrochemical gradient of protons or Na ions across the membrane into rotational torque by the F o motor of the ATP synthase has been described by a two-channel model or by a one-channel model. Experimental evidence obtained with the F o motor from the Propionigenium modestum ATP synthase is described which is in accordance with the one-channel model, but not with the two-channel model. This evidence includes the ATP-dependent occlusion of one 22 Na per ATP synthase with a mutated Na-impermeable a subunit or the Na in / 22 Na out exchange which is not affected by modifying part of the c subunit sites with dicyclohexylcarbodiimide.
Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1998
A model is presented in which ion translocation through the F 0 part of the ATP synthase drives the rotation of the ring of c subunits (rotor) versus the a subunit (stator). The coupling ion binding sites on the rotor are accessible from the cytoplasm of a bacterial cell except for the c subunit at the interface to the stator. Here, the binding site is accessible from the periplasm through a channel formed by subunit a. In the ATP synthesis mode, a coupling ion is anticipated to pass through the stator channel into the binding site of the adjacent rotor subunit, following the electrical potential. Occupation of this site triggers, probably by electrostatic forces, the rotation of the ring. This makes the binding site accessible to the cytoplasm, where the coupling ion dissociates. Simultaneously, this rotation moves again an empty rotor subunit into the contact site with the stator, where its binding site becomes loaded and rotation continues.
Voltage-generated torque drives the motor of the ATP synthase
The EMBO Journal, 1998
The mechanism by which ion-flux through the membrane-bound motor module (F 0) induces rotational torque, driving the rotation of the γ subunit, was probed with a Na ⍣-translocating hybrid ATP synthase. The ATP-dependent occlusion of 1 22 Na ⍣ per ATP synthase persisted after modification of the c subunit ring with dicyclohexylcarbodiimide (DCCD), when 22 Na ⍣ was added first and ATP second, but not if the order of addition was reversed. These results support the model of ATP-driven rotation of the c subunit oligomer (rotor) versus subunit a (stator) that stops when either a 22 Na ⍣-loaded or a DCCD-modified rotor subunit reaches the Na ⍣-impermeable stator. The ATP synthase with a Na ⍣-permeable stator catalyzed 22 Na ⍣ out /Na ⍣ in-exchange after reconstitution into proteoliposomes, which was not significantly affected by DCCD modification of the c subunit oligomer, but was abolished by the additional presence of ATP or by a membrane potential (∆Ψ) of 90 mV. We propose that in the idling mode of the motor, Na ⍣ ions are shuttled across the membrane by limited back and forth movements of the rotor against the stator. This motional flexibility is arrested if either ATP or ∆Ψ induces the switch from idling into a directed rotation. The Propionigenium modestum ATP synthase catalyzed ATP formation with ∆Ψ of 60-125 mV but not with ∆pNa ⍣ of 195 mV. These results demonstrate that electric forces are essential for ATP synthesis and lead to a new concept of rotary-torque generation in the ATP synthase motor.
ATP Synthase Motor Components: Proposal and Animation of Two Dynamic Models for Stator Function
Biochemical and Biophysical Research Communications, 2001
Recent research indicates that ATP synthases (F 0 F 1 ) contain two distinct nanomotors, one an electrochemically driven proton motor contained within F 0 that drives an ATP hydrolysis-driven motor (F 1 ) in reverse during ATP synthesis. This is depicted in recent models as involving a series of events in which each of the three ␣ pairs comprising F 1 is induced via a centrally rotating subunit (␥) to undergo the sequential binding changes necessary to synthesize ATP (binding change mechanism). Stabilization of this rotary process (i.e., to minimize "wobble" of F 1 ) is provided in current models by a peripheral stalk or "stator" that has recently been shown to extend from near the bottom of the ATP synthase molecule to the very top of F 1 . Although quite elegant, these models envision the stator as fixed during ATP synthesis, i.e., bound to only a single ␣ pair. This is despite the fact that the binding change mechanism views each ␣ pair as going through the same sequential order of conformational changes which demonstrate a chemical equivalency among them. For this reason, we propose here two different dynamic models for stator function during ATP synthesis. Both models have been designed to maintain chemical equivalency among the three ␣ pairs during ATP synthesis and both have been animated.
Energy transduction in the F1 motor of ATP synthase
ATP synthase is the universal enzyme that manufactures ATP from ADP and phosphate by using the energy derived from a transmembrane protonmotive gradient. It can also reverse itself and hydrolyse ATP to pump protons against an electrochemical gradient. ATP synthase carries out both its synthetic and hydrolytic cycles by a rotary mechanism 1±4 . This has been con®rmed in the direction of hydrolysis 5,6 after isolation of the soluble F 1 portion of the protein and visualization of the actual rotation of the central`shaft' of the enzyme with respect to the rest of the molecule, making ATP synthase the world's smallest rotary engine. Here we present a model for this engine that accounts for its mechanochemical behaviour in both the hydrolysing and synthesizing directions. We conclude that the F 1 motor achieves its high mechanical torque and almost 100% ef®ciency because it converts the free energy of ATP binding into elastic strain, which is then released by a coordinated kinetic and tightly coupled conformational mechanism to create a rotary torque.