Table 1.
A comparison of Boyer’s model with mechano-chemiosmotic model
| Boyer’s model (Skulachev 1989; Boyer 1997; Tikhonov 2013a; Walker 2013) | Mechano-chemiosmotic model | |
|---|---|---|
| Proton delivery | Proton is not delivered to the active center | Three protons are delivered to the active centers at C-terminal part of γ-subunit |
| What is the purpose of protons? | Protons are necessary for rotation of a rotor—c-ring, and c-ring rotates together with γ-subunit | Protons are necessary to change pH value in the matrix, stroma, or cytosol to pH 7.0 to provide negative and positive groups in the proteins |
| What is the major force that drives ATP synthesis in the ATP synthase functioning? | pmf is what drives ATP synthase. The force that causes a movement of the «rotor» of ATP synthase arises as a result of difference of potentials between outer and inner sides of the membrane (>220 mV) and is provided by proton flow, passing through a special channel in F0 located between subunits a and c | The major force for ATP synthase functioning is a proton gradient and membrane potential as is the case for the other model. Proton flow, passing through proton channel in F0 located at the border between a-, c- and b 2-subunits, change pH of matrix, stroma, or cytosol to pH 7.0, and three protons are delivered to active centers. At the expense of proton gradient, transport of cations, and change of volumes of organelles take place. Membrane potential causes rotation of γ-subunit and twisting of b 2-subunits. At the expense of membrane potential, three protons, three phosphate ions are delivered to active centers. Due to electrostatic interactions nucleophilic substitution takes place, phosphoryl groups are formed, three molecules of ATP are synthesized, ATPs are released from the enzyme, and ADP molecules are loaded to active centers |
| Does ATP synthesis require energy? | Energy is not required for ATP synthesis, but for its release (see below) | Energy is required for the production of phosphoryl groups |
| Does delivery of ADP and Pi to active center require energy? | Energy is required for delivery of ADP and Pi from the water phase to the active center. This is provided by mechanical movement of the side surface of α- and β-subunits during rotation of a «rotor»—γ-subunit, where conformational changes take place in catalytic centers | Energy is necessary to deliver ADP and Pi from the water phase to active center. ADP enters through the apical part of the hexamer during opening of the «lid-cap» of the hexamer—δ-subunit. Three Pi together with three protons are delivered to active centers at C-terminal part of γ-subunit |
| Does ATP release from the enzyme require energy? | Energy is required for the release of ATP from the enzyme. This is achieved by mechanical movement of the side surface of α- and β-subunits during rotation of the «rotor»—γ-subunit, where conformational changes take place in catalytic centers | Energy is required for ATP release from the enzyme. Under energization of membrane, γ-subunit rotates counterclockwise direction and negatively charged phosphate ions electrostatically repulse negatively charged ATP molecules to the apical apart of the hexamer. In case of full energization of the membrane, the «lid-cap» of the hexamer—δ-subunit opens and ATP molecules from the apical part of the hexamer are exchanged for external molecules of ADP with participation of sodium ions |
| H+/ATP ratio | H+/ATP ratio is linked to the amount of c-monomers in the c-ring | H+/ATP ratio is linked to the amount of protons (3 protons) required for the synthesis of ATP molecules and pH changes to neutral pH of 7.0 |
| Low-amplitude changes of volumes of organelles | Low-amplitude changes of organelle volume are consequences and do not carry any function | Low-amplitude changes of volumes of organelles proceed as a result of membrane protonation and transport of cations. During shrinkage of the intermembrane space or thylakoids, electron transfer from ISP protein to cytochrome c 1 or f takes place |
| Transport of ions—cations and anions | Transport of cations or anions is not meaningful and it is a consequence of a response to protonation of the membrane | Transport of cations and anions is active part of the mechanism, energy-dependent process at the expense of proton gradient. It changes the buffer capacity of matrix, stroma, or cytosol. Monovalent cations together with polyvalent anions participate in stabilization, but polyvalent cations (calcium), on the contrary, cause destabilization of protein molecules |
| Opening of active center of enzyme | Active center of the enzyme is opened by mechanical movement of the side surface of α- and β-subunits with the assistance of γ-subunit | Active center of the enzyme is opened by deprotonation of alpha-helical loops of α- and β-subunits by γ-subunit |
| Rotation of γ-subunit | γ-Subunit rotates due to rotation of the c-ring or in ATP hydrolysis | γ-Subunit rotates in the case of protonation and binding of phosphate ions to N-terminal subunit in the electric field |
| Role of δ-subunit | δ-subunit is a part of stator | δ-Subunit is a “lid-cap” of hexamer through which ADP is imported and ATP is exported |
| Role of c-ring | c-ring together with γ-subunit and ε-subunit constitutes a rotor of electromotor | c-ring is non-selective ion channel |
| Role of b 2-subunit | b 2-Subunit is a part of stator together with a-subunit | b 2-Subunits represent cords that are in a twisted state and, which twists more during binding of phosphate ions; the membrane potential allows the hexamer to be dragged to the membrane |
| Role of ε-subunit | ε-Subunit regulates ATPase activity | ε-Subunit is a mechanical «stopper» of the proton channel in contracted conformation. It protonates β-subunit and also regulates ATPase activity in extended conformation |
| Role of γ-subunit | γ-Subunit represents an axis of the rotor—c-ring and rotates clockwise direction during ATP hydrolysis and counterclockwise direction in ATP synthesis | γ-Subunit is the rotor. It rotates counterclockwise direction 360° during energization, and then it rotates clockwise direction 360° back during the synthesis of ATP. Three Pi together with three protons are delivered to active centers at C-terminal part of γ-subunit |
| Role of α 3 β 3-hexamer | α 3 β 3-Hexamer has three catalytic and three non-catalytic centers; it represents a part of stator of electromotor | α 3 β 3-Hexamer has three catalytic and three non-catalytic centers; it is moved (dragged by b 2-subunits) to the membrane during the energization process and is moved from the membrane during the deenergization process |
| Regulation of electron transport and proton transfer | Electron transport and proton transfer are regulated by pH changes | Electron transport through cytochrome bc 1 and proton passage through proton channel in ATP synthase are regulated by pH changes and mechanically |
| Evidence for the model | Currently there is no working model | The direct proof of this model is the acting nanomotor of carbon nanotube which operates on the same principles |