Contribution of the Collective Excitations to the Coupled Proton and Energy Transport along Mitochondrial Cristae Membrane in Oxidative Phosphorylation System

Semen V Nesterov; Lev S Yaguzhinsky; Raif G Vasilov; Vasiliy N Kadantsev; Alexey N Goltsov

doi:10.3390/e24121813

Contribution of the Collective Excitations to the Coupled Proton and Energy Transport along Mitochondrial Cristae Membrane in Oxidative Phosphorylation System

Entropy (Basel). 2022 Dec 13;24(12):1813. doi: 10.3390/e24121813.

Authors

Semen V Nesterov^{1

2}, Lev S Yaguzhinsky^{2

3

4}, Raif G Vasilov¹, Vasiliy N Kadantsev⁵, Alexey N Goltsov⁵

Affiliations

¹ Kurchatov Complex of NBICS-Technologies, National Research Center Kurchatov Institute, 123182 Moscow, Russia.
² Research Center for Molecular Mechanisms of Aging and Age-Related Diseases, Moscow Institute of Physics and Technology, 141701 Dolgoprudny, Russia.
³ Department of Bioenergetics, Institute of Cytochemistry and Molecular Pharmacology, 115404 Moscow, Russia.
⁴ Belozersky Research Institute for Physico-Chemical Biology, Lomonosov Moscow State University, 119992 Moscow, Russia.
⁵ Institute for Artificial Intelligence, Russian Technological University (MIREA), 119454 Moscow, Russia.

Abstract

The results of many experimental and theoretical works indicate that after transport of protons across the mitochondrial inner membrane (MIM) in the oxidative phosphorylation (OXPHOS) system, they are retained on the membrane-water interface in nonequilibrium state with free energy excess due to low proton surface-to-bulk release. This well-established phenomenon suggests that proton trapping on the membrane interface ensures vectorial lateral transport of protons from proton pumps to ATP synthases (proton acceptors). Despite the key role of the proton transport in bioenergetics, the molecular mechanism of proton transfer in the OXPHOS system is not yet completely established. Here, we developed a dynamics model of long-range transport of energized protons along the MIM accompanied by collective excitation of localized waves propagating on the membrane surface. Our model is based on the new data on the macromolecular organization of the OXPHOS system showing the well-ordered structure of respirasomes and ATP synthases on the cristae membrane folds. We developed a two-component dynamics model of the proton transport considering two coupled subsystems: the ordered hydrogen bond (HB) chain of water molecules and lipid headgroups of MIM. We analytically obtained a two-component soliton solution in this model, which describes the motion of the proton kink, corresponding to successive proton hops in the HB chain, and coherent motion of a compression soliton in the chain of lipid headgroups. The local deformation in a soliton range facilitates proton jumps due to water molecules approaching each other in the HB chain. We suggested that the proton-conducting structures formed along the cristae membrane surface promote direct lateral proton transfer in the OXPHOS system. Collective excitations at the water-membrane interface in a form of two-component soliton ensure the coupled non-dissipative transport of charge carriers and elastic energy of MIM deformation to ATP synthases that may be utilized in ATP synthesis providing maximal efficiency in mitochondrial bioenergetics.

Keywords: collective excitations; mitochondrial cristae membrane; oxidative phosphorylation system; proton conducting networks; proton transport; soliton dynamics.

Grants and funding

This work was partly supported (S.V.N. and R.G.V.) by the Kurchatov National Research Center, Moscow, Russia (Research Project “Investigation of generation, transfer, and distribution of energy in live organisms”).