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Entropy Production and Its Application to the Coupled Nonequilibrium Processes of ATP Synthesis

Department of Biochemical Engineering and Biotechnology, Indian Institute of Technology Delhi, Hauz Khas, New Delhi 110016, India
Entropy 2019, 21(8), 746; https://doi.org/10.3390/e21080746
Received: 29 June 2019 / Revised: 23 July 2019 / Accepted: 27 July 2019 / Published: 30 July 2019
(This article belongs to the Special Issue Entropy Production and Its Applications: From Cosmology to Biology)
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Abstract

Starting from the universal concept of entropy production, a large number of new results are obtained and a wealth of novel thermodynamic, kinetic, and molecular mechanistic insights are provided into the coupling of oxidation and ATP synthesis in the vital process of oxidative phosphorylation (OX PHOS). The total dissipation, Φ , in OX PHOS with succinate as respiratory substrate is quantified from measurements, and the partitioning of Φ into the elementary components of ATP synthesis, leak, slip, and other losses is evaluated for the first time. The thermodynamic efficiency, η , of the coupled process is calculated from the data on Φ and shown to agree well with linear nonequilibrium thermodynamic calculations. Equations for the P/O ratio based on total oxygen consumed and extra oxygen consumed are derived from first principles and the source of basal (state 4) mitochondrial respiration is postulated from molecular mechanistic considerations based on Nath’s two-ion theory of energy coupling within the torsional mechanism of energy transduction and ATP synthesis. The degree of coupling, q , between oxidation and ATP synthesis is determined from the experimental data and the irreversible thermodynamics analysis. The optimality of biological free energy converters is explored in considerable detail based on (i) the standard biothermodynamic approach, and (ii) a new biothermokinetic approach developed in this work, and an effective solution that is shown to arise from consideration of the molecular aspects in Nath’s theory is formulated. New experimental data in state 4 with uncouplers and redox inhibitors of OX PHOS and on respiratory control in the physiological state 3 with ADP and uncouplers are presented. These experimental observations are shown to be incompatible with Mitchell’s chemiosmotic theory. A novel scheme of coupling based on Nath’s two-ion theory of energy coupling within the torsional mechanism is proposed and shown to explain the data and also pass the test of consistency with the thermodynamics, taking us beyond the chemiosmotic theory. It is concluded that, twenty years since its first proposal, Nath’s torsional mechanism of energy transduction and ATP synthesis is now well poised to catalyze the progress of experimental and theoretical research in this interdisciplinary field. View Full-Text
Keywords: free energy dissipation in oxidative phosphorylation (OX PHOS); ATP synthesis by F1FO-ATP synthase; irreversible thermodynamics/nonequilibrium thermodynamics of biological processes; optimization of biological energy converters; variational principle; Mitchell’s chemiosmotic theory; Nath’s torsional mechanism of energy transduction and ATP synthesis; Nath’s two-ion theory of biological energy coupling; succinate as feedback signal and anion uncouplers of OX PHOS; biothermokinetics free energy dissipation in oxidative phosphorylation (OX PHOS); ATP synthesis by F1FO-ATP synthase; irreversible thermodynamics/nonequilibrium thermodynamics of biological processes; optimization of biological energy converters; variational principle; Mitchell’s chemiosmotic theory; Nath’s torsional mechanism of energy transduction and ATP synthesis; Nath’s two-ion theory of biological energy coupling; succinate as feedback signal and anion uncouplers of OX PHOS; biothermokinetics
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Nath, S. Entropy Production and Its Application to the Coupled Nonequilibrium Processes of ATP Synthesis. Entropy 2019, 21, 746.

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