Molecular energy transducers of the living cell. Proton ATP synthase: a rotating molecular motor

Romanovsky, Y.M.; Тихонов, А. Н.

doi:10.3367/ufne.0180.201009b.0931

Cited by 49 publications

(19 citation statements)

References 120 publications

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“…Operation of this pump is similar to the principle of c -ring as ion channel. Many experimental facts agree with the mechanism presented by our model; some of these are listed below: Tributyltin chloride, a special inhibitor of ion access through subunit a , inhibits rotation of F 0 motor (as currently many assume that there is an F 0 electromotor and its rotation occurs due to protons (von Ballmoos et al 2008 , 2009 ; Junge et al 2009 ; Kagawa 2010 ; Romanovsky and Tikhonov 2010 ; Tikhonov 2013a ) by 96 % (Ueno et al 2005 ; see also von Ballmoos et al 2009 ). Transport of anions (for example, chloride and bicarbonate), together with potassium ions, was proved by the following results.…”

Section: Mechano-chemiosmotic Modelsupporting

confidence: 82%

“…The current consensus is, with supporting data, that ATP synthase consists of two motors (mechano-chemical motor—F 1 , working at the expense of energy released during ATP hydrolysis, and H + —managed electric motor—F 0 that utilizes energy of the electrochemical potential—ΔµH + ) (von Ballmoos et al 2008 , 2009 ; Junge et al 2009 ; Kagawa 2010 ; Romanovsky and Tikhonov 2010 ; Tikhonov 2013a ). The rotors of both the motors are constructively linked with each other and rotated jointly in opposite directions; the source of energy is either ATP (when dealing with ATP hydrolysis) or electrochemical potential—ΔµH + (when dealing with ATP synthesis).…”

Section: Current Model Of Action Mechanism Of Atp Synthasementioning

confidence: 99%

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A mechano-chemiosmotic model for the coupling of electron and proton transfer to ATP synthesis in energy-transforming membranes: a personal perspective

Kasumov¹,

Kasumov²,

Kasumova³

2014

Photosynth Res

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ATP is synthesized using ATP synthase by utilizing energy either from the oxidation of organic compounds, or from light, via redox reactions (oxidative- or photo phosphorylation), in energy-transforming membranes of mitochondria, chloroplasts, and bacteria. ATP synthase undergoes several changes during its functioning. The generally accepted model for ATP synthesis is the well-known rotatory model (see e.g., Junge et al., Nature 459:364–370, 2009; Junge and Müller, Science 333:704–705, 2011). Here, we present an alternative modified model for the coupling of electron and proton transfer to ATP synthesis, which was initially developed by Albert Lester Lehninger (1917–1986). Details of the molecular mechanism of ATP synthesis are described here that involves cyclic low-amplitude shrinkage and swelling of mitochondria. A comparison of the well-known current model and the mechano-chemiosmotic model is also presented. Based on structural, and other data, we suggest that ATP synthase is a Ca2+/H+–K+ Cl−–pump–pore–enzyme complex, in which γ-subunit rotates 360° in steps of 30°, and 90° due to the binding of phosphate ions to positively charged amino acid residues in the N-terminal γ-subunit, while in the electric field. The coiled coil b2-subunits are suggested to act as ropes that are shortened by binding of phosphate ions to positively charged lysines or arginines; this process is suggested to pull the α3β3-hexamer to the membrane during the energization process. ATP is then synthesized during the reverse rotation of the γ-subunit by destabilizing the phosphated N-terminal γ-subunit and b2-subunits under the influence of Ca2+ ions, which are pumped over from storage—intermembrane space into the matrix, during swelling of intermembrane space. In the process of ATP synthesis, energy is first, predominantly, used in the delivery of phosphate ions and protons to the α3β3-hexamer against the energy barrier with the help of C-terminal alpha-helix of γ-subunit that acts as a lift; then, in the formation of phosphoryl group; and lastly, in the release of ATP molecules from the active center of the enzyme and the loading of ADP. We are aware that our model is not an accepted model for ATP synthesis, but it is presented here for further examination and test.

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Section: Mechano-chemiosmotic Modelsupporting

confidence: 82%

Section: Current Model Of Action Mechanism Of Atp Synthasementioning

confidence: 99%

A mechano-chemiosmotic model for the coupling of electron and proton transfer to ATP synthesis in energy-transforming membranes: a personal perspective

Kasumov¹,

Kasumov²,

Kasumova³

2014

Photosynth Res

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“…The synthesis of ATP is catalyzed by ATP synthases using the energy from external sources. One type of ATP synthase complexes catalyzes both reactions, ATP synthesis and ATP hydrolysis (Romanovsky and Tikhonov, 2010). As one of ATP synthase complexes performs synthesis of the majority of ATP molecules in the cell (Skulachev, 1988;Feldkamp et al, 2005;Nelson and Cox, 2004) and the phenotype of both camel species are clearly different, the great amino acid substitutions of ATP6 gene may be correlated to its major role in energy synthesis.…”

Section: Discussionmentioning

confidence: 99%

“…One type of ATP synthase protein complexes performs synthesis of the overwhelming majority of ATP molecules in the cell (Skulachev, 1988;Nicholls, 2002;Nelson and Cox, 2004). These molecules are the smallest macromolecular electric motors in nature (Romanovsky and Tikhonov, 2010).…”

Section: Ajbbmentioning

confidence: 99%

Molecular Study of Energy Related Mitochondrial Genes in Arabian and Bactrian Camels

Ahmed¹,

El-Shazly²,

Sayed³

2013

American Journal of Biochemistry and Biotechnology

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The single-humped camel, Camelus dromedaries inhabiting Afro-Arabia and the double-humped camel, Camelus bactrianus inhabiting central Asia are the only species in their genus. The present study aimed to amplify and partially sequence the mitochondrial DNA genes encoding for NADH dehydrogenase subunit 1, cytochrome c oxidase subunit 1, ATP synthase subunit 6 (ATP6), cytochrome b and displacement region (d-loop) in the single-humped camel and compare it to their counterparts already sequenced for the doublehumped camel. These energy-related genes showed amino acid substitutions gradually increased according to their locations among macromolecular energy transducers. Both ATP synthase 6 in the central core and cytochrome b in the inner mitochondrial membrane acquired the greatest substitutions of 5 and 7 amino acids, respectively. Cytochrome c oxidase is the terminal complex of the electron transport chain of the inner mitochondrial membrane and it showed no substitutions. These substitutions seemed to be correlated with the energy metabolism in both camel phenotypes. The d-loop showed tandem repeats of six nucleotides at its 3` end with polymorphism between both species without any evidence relates such variation to energy production.

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“…The efficiency of Brownian motors is therefore maximized when they are operating mostly close to the thermal equilibrium, to minimize the heat losses. Theoretically, efficiency can reach value of one (if to operate very slowly at almost zero power), and some biological molecular motors can indeed be very efficient, by operating in multiple small steps [44,46,47]. This is a textbook wisdom [24].…”

Section: Load and Efficiencymentioning

confidence: 99%

Subdiffusive rocking ratchets in viscoelastic media: Transport optimization and thermodynamic efficiency in overdamped regime

Kharchenko

Goychuk

2013

Phys. Rev. E

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We study subdiffusive overdamped Brownian ratchets periodically rocked by an external zero-mean force in viscoelastic media within the framework of a non-Markovian generalized Langevin equation approach and associated multidimensional Markovian embedding dynamics. Viscoelastic deformations of the medium caused by the transport particle are modeled by a set of auxiliary Brownian quasiparticles elastically coupled to the transport particle and characterized by a hierarchy of relaxation times which obey a fractal scaling. The most slowly relaxing deformations which cannot immediately follow to the moving particle imprint long-range memory about its previous positions and cause subdiffusion and anomalous transport on a sufficiently long time scale. This anomalous behavior is combined with normal diffusion and transport on an initial time scale of overdamped motion. Anomalously slow directed transport in a periodic ratchet potential with broken space inversion symmetry emerges due to a violation of the thermal detailed balance by a zero-mean periodic driving and is optimized with frequency of driving, its amplitude, and temperature. Such optimized anomalous transport can be low dispersive and characterized by a large generalized Peclet number. Moreover, we show that overdamped subdiffusive ratchets can sustain a substantial load and do useful work. The corresponding thermodynamic efficiency decays algebraically in time since the useful work done against a load scales sublinearly with time following to the transport particle position, but the energy pumped by an external force scales with time linearly. Nevertheless, it can be transiently appreciably high and compare well with the thermodynamical efficiency of the normal diffusion overdamped ratchets on sufficiently long temporal and spatial scales.

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Molecular energy transducers of the living cell. Proton ATP synthase: a rotating molecular motor

Cited by 49 publications

References 120 publications

A mechano-chemiosmotic model for the coupling of electron and proton transfer to ATP synthesis in energy-transforming membranes: a personal perspective

A mechano-chemiosmotic model for the coupling of electron and proton transfer to ATP synthesis in energy-transforming membranes: a personal perspective

Molecular Study of Energy Related Mitochondrial Genes in Arabian and Bactrian Camels

Subdiffusive rocking ratchets in viscoelastic media: Transport optimization and thermodynamic efficiency in overdamped regime

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