No 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.

Objectives. Numerous studies of biosystems indicate the distinct role of quasi-one-dimensional molecular structures in the transport of energy, charges, and information. Of particular interest are the studies on the collective dynamics of quasi-one-dimensional lateral structures in liquid crystalline membranes and the possibility of local excitation transfer through such structures. In this paper, we developed a model for the collective dynamics of quasi-one-dimensional domain structures in lipid bilayers interacting with the environment. The objective is to study the mechanisms of the directed energy transport in liquid crystalline lipid membranes.Methods. In this paper, the percolation domain structures formed as a result of phase separation in multicomponent lipid membranes are considered to be quasi-one-dimensional domain structures. The model distinguishes two subsystems interacting with each other and differing in their structural and dynamic properties, i.e., the membrane surface formed by polar groups of lipid molecules and the internal hydrophilic region of the membrane formed by acyl chains of lipids. The acyl chain subsystem is simulated using the Ginzburg-Landau Hamiltonian which considers the dependence of its dynamics on temperature close to the lipid melting phase transition temperature Tc.Results. Analysis of dynamic states has shown that elastic excitations moving at constant rate in the form of solitons may exist near temperatures Tc in the considered quasi-one-dimensional domain structures. In addition, motion of the elastic excitation region (kink) along domain structures in the acyl chain region causes the formation of acoustic soliton, i.e., the compression region in the polar group subsystem moving in concert with the kink displacement. The soliton localization region covers about 10 molecules and depends significantly on the interaction parameter of the polar group and acyl chain subsystems. Soliton moves at a subsonic speed determined, in particular, by the magnitude of an external force.Conclusions. The model developed in this paper shows that liquid crystalline domain structures in lipid membranes exhibit properties of active media, wherein the formation and displacement of localized elastic excitations on macroscopic spatial and temporal scales may occur. The proposed molecular mechanism of the soliton transport along quasi-one-dimensional domain structures may be used for describing the directed energy transfer along lateral domain channels in biomembranes and the cooperative functioning of the membrane bioenergetic and receptor complexes.

A numerical study of the Davydov soliton dynamics in a thermalized cyclic molecular chain is performed. Account is taken of the effect of thermalized molecular vibrations within the scope of the quantum-mechanical theory. It is shown in contrast to results of a number of works, where account of the thermal vibration effect is taken within the framework of the classical model, that using the quantum-mechanical description the thermal vibrations not only don't prevent but also favour autolocalization of intramolecular excitation. nPOBOAEITCR qHCJIeHHOe ElCCJIeAOBaHEIe AEIHaMHKM HaBbIAOBCKOrO COJIHTOHa B TepMaJIH-30RaHHOfi UHKJIHqtXKOfi MOJIeHyJIflpHOfi UeIIOqKe. BnllflHme TenJIOBHX ~o n e 6 a H~f i MOJIe-KYJI yYTeH0 B paMKaX ICBaHTOBO-MeXaHHYeCKOfi MOAeJIEI. nOKa3aH0, YTO B OTJIHqlle OT pe3yJIbTaTOB pHna p a 6 o~, rEe BJIHRHEIe TeIIJIOBLIX ~o n e 6 a~m f i ysHTblBaJlOCb B paMKaX He TOJIbICO He MeIUaIOT, HO H 3HaYEITeJIbHO CIIOCO6CTByIOT aBTOJIOKaJlEI3a411H BHYTPEI-MOJIeEiyJIFIpHOrO BO36YXJIeHHR. maccHYecKoB monenn, n p KBaHToBo-~ieXaHH9ecEo~ o n~c a m m TenJIoBbIe ~o n e 6 a~~f l

V. N. KADAKTSEV et al.: Intramolecular Excitation Dynamics in a Chain (11) 155 phys. stat. sol. (b) 147, 155 (1988) Subject classification: 71.45 Institute for Physico-Technologicul Research, Moscow1) Intramolecular Excitation Dynamics in a Thermalized Chain 11. Formation of Autolocalized States in a Chain with Free Ends2) BY V. N. KADANTSEV, L. N. LUPICHEV, and A. V. SAVINA numerical study of the Davydov soliton dynamics in a thermalized unclosed molecular chain with asymmetric exciton-phonon interaction is carried out. The effect of thermal vibrations in the scope of the quantum-mechanical model is taken into account. When initiating the excitation at the free end of the chain, the soliton transport is shown to be able to occur at temperatures close to 300 K only. In this case the soliton formation is dependent on which of the end molecules in the chain is excited first.