Lateral proton transport induced by acoustic solitons propagating in lipid membranes
https://doi.org/10.32362/2500-316X-2025-13-2-111-120
EDN: ATOWXW
Abstract
Objectives. The study of proton transport in membrane structures represents a significant technological task in the development of hydrogen energy as well as a fundamental problem in bioenergetics. Investigation in this field aims at finding out the physical mechanisms of fast proton transport in the meso-porous structures in polymer electrolyte membranes, which serve as electrochemical components of hydrogen fuel cells. The objectives of the research in the field of bioenergetics are to elucidate the molecular mechanisms of effective proton transport in transmembrane channel proteins, as well as along the surface proton-conducting structures in biological membranes. To investigate the molecular mechanisms of the direct proton transport along the water-membrane interface, we developed a model of proton movement along quasi-one-dimensional lateral domain structures in multicomponent lipid membranes.
Methods. The developed approach is based on a model of collective excitations spreading along the membranes in the form of acoustic solitons, which represent the regions of local compression of polar groups and structural defects in hydrocarbon chains of lipid molecules.
Results. The results of modeling showed that the interaction between an excess proton on the membrane surface and a soliton of membrane compression leads to the proton being trapped by an acoustic soliton, followed by its transport by moving soliton. The developed model was applied to describe effective proton transport along the inner mitochondrial membrane and its role in the local coupling function of molecular complexes in cell bioenergetics.
Conclusions. The developed soliton model of proton transport demonstrated that collective excitations within lipid membranes can determine one of the factors affecting the efficiency of proton transport along interphase boundaries. Further development of the theoretical approaches, taking into account dynamic properties of polymer and biological proton-conducting membranes, can contribute to the study of a role of surface proton transport in cell bioenergetics, as well as to the investigation of transport characteristics of the proton-exchange polymer membranes developed for the hydrogen energy industry.
Keywords
About the Authors
Vasiliy N. KadantsevRussian Federation
Vasiliy N. Kadantsev, Dr. Sci. (Phys.-Math.), Professor, Department of Biocybernetic Systems and Technologies, Institute of Artificial Intelligence
78, Vernadskogo pr., Moscow, 119454
Scopus Author ID 6602993607
Competing Interests:
The authors declare no conflicts of interest.
Alexey N. Goltsov
Russian Federation
Alexey N. Goltsov, Dr. Sci. (Phys.-Math.), Professor, Department of Biocybernetic Systems and Technologies, Institute of Artificial Intelligence
78, Vernadskogo pr., Moscow, 119454
Scopus Author ID 56234051200
Competing Interests:
The authors declare no conflicts of interest.
References
1. Dobrovolsky Y.A., Chikin A.I., Sanginov E.A., Chub A.V. Proton-exchange membranes based on heteropoly compounds for low temperature fuel cells. Al’ternativnaya energetika i ekologiya = Alternative Energy and Ecology. 2015;4(165):22–45 (in Russ.). https://doi.org/10.15518/isjaee.2015.04.02
2. Lebedeva O.V. Proton conducting membranes for hydrogen-air fuel elements. Izvestiya vuzov. Prikladnaya khimiya i biotekhnologiya = Proceedings of Universities. Applied Chemistry and Biotechnology. 2016;1(16):7–19 (in Russ.).
3. Eremeev S.A., Yaguzhinsky L.S. On local coupling of the electron transport and ATP-synthesis system in mitochondria. Theory and experiment. Biochemistry (Moscow). 2015;80(5):576–581. https://doi.org/10.1134/S0006297915050089 ] [Original Russian Text: Eremeev S.A., Yaguzhinsky L.S. On local coupling of the electron transport and ATP synthesis system in mitochondria. Theory and experiment. Biokhimiya. 2015;80(5):682–688 (in Russ.).]
4. Kell D.B. A protet-based model that can account for energy coupling in oxidative and photosynthetic phosphorylation. Biochim. Biophys. Acta Bioenerg. 2024;1865(4):149504. https://doi.org/10.1016/j.bbabio.2024.149504
5. Nesterov S.V., Yaguzhinsky L.S., Vasilov R.G., Kadantsev V.N., Goltsov A.N. Contribution of the Collective Excitations to the Coupled Proton and Energy Transport along Mitochondrial Cristae Membrane in Oxidative Phosphorylation System. Entropy (Basel). 2022;24(12):1813. https://doi.org/10.3390/e24121813
6. Davies K.M., Strauss M., Daum B., Kief J.H., Osiewacz H.D., Rycovska A., et al. Macromolecular organization of ATP synthase and complex I in whole mitochondria. Proc. Natl. Acad. Sci. USA. 2011;108(34):14121–14126. https://doi.org/10.1073/pnas.1103621108
7. Nesterov S., Chesnokov Y., Kamyshinsky R., PanteleevaA., Lyamzaev K., Vasilov R., et al. Ordered Clusters of the Complete Oxidative Phosphorylation System in Cardiac Mitochondria. Int. J. Mol. Sci. 2021;22(3):1462. https://doi.org/10.3390/ijms22031462
8. Mulkidjanian A.Y., Heberle J., Cherepanov D.A. Protons @ interfaces: Implications for biological energy conversion. Biochimica et Biophysica Acta (BBA) – Bioenergetics. 2006;1757(8):913–930. https://doi.org/10.1016/j.bbabio.2006.02.015
9. Weichselbaum E., Österbauer M., Knyazev D.G., Batishchev O.V., Akimov S.A., Nguyen T.H., et al. Origin of proton affinity to membrane/water interfaces. Sci. Rep. 2017;7(1):4553. https://doi.org/10.1038/s41598-017-04675-9
10. Yaguzhinsky L.S., Boguslavsky L.I., Volkov A.G., Rakhmaninova A.B. Synthesis of ATP coupled with action of membrane protonic pumps at the octane-water interface. Nature. 1976;259(5543):494–496. https://doi.org/10.1038/259494a0
11. Kell D.B. On the functional proton current pathway of electron transport phosphorylation. An electrodic view. Biochim. Biophys. Acta. 1979;549(1):55–99. https://doi.org/10.1016/0304-4173(79)90018-1
12. Morelli A.M., Ravera S., Calzia D., Panfoli I. An update of the chemiosmotic theory as suggested by possible proton currents inside the coupling membrane. Open Biol. 2019;9(4):180221. https://doi.org/10.1098/rsob.180221
13. Wraight C.A. Chance and design—Proton transfer in water, channels and bioenergetic proteins. Biochimica et Biophysica Acta (BBA) – Bioenergetics. 2006;1757(8):886–912. https://doi.org/10.1016/j.bbabio.2006.06.017
14. Kreuer K.D. Proton Conductivity: Materials and Applications. Chem. Mater. 1996;8(3):610–641. https://doi.org/10.1021/cm950192a
15. Ludueña G.A., Kühne T.D., Sebastiani D. Mixed Grotthuss and Vehicle Transport Mechanism in Proton Conducting Polymers from Ab initio Molecular Dynamics Simulations. Chem. Mater. 2011;23(6):1424–1429. https://doi.org/10.1021/cm102674u
16. Weichselbaum E., Galimzyanov T., Batishchev O.V., Akimov S.A., Pohl P. Proton Migration on Top of Charged Membranes. Biomolecules. 2023;13(2):352. https://doi.org/10.3390/biom13020352
17. Knyazev D.G., Silverstein T.P., Brescia S., Maznichenko A., Pohl P. A New Theory about Interfacial Proton Diffusion Revisited: The Commonly Accepted Laws of Electrostatics and Diffusion Prevail. Biomolecules. 2023;13(11):1641. https://doi.org/10.3390/biom13111641
18. Antonenko Y.N., Kovbasnjuk O.N., Yaguzhinsky L.S. Evidence in favor of the existence of a kinetic barrier for proton transfer from a surface of bilayer phospholipid membrane to bulk water. Biochimica et Biophysica Acta (BBA) – Biomembranes. 1993;1150(1):45–50. https://doi.org/10.1016/0005-2736(93)90119-k
19. Tashkin V.Yu., Vishnyakova V.E., Shcherbakov A.A., Finogenova O.A., Ermakov Yu.A., Sokolov V.S. Changes of the Capacitance and Boundary Potential of a Bilayer Lipid Membrane Associated with a Fast Release of Protons on Its Surface. Biochem. Moscow Suppl. Ser. A. 2019;13(2):155–160. https://doi.org/10.1134/S1990747819020077
20. Sjöholm J., Bergstrand J., Nilsson T., Šachl R, Ballmoos C., Widengren J., et al. The lateral distance between a proton pump and ATP synthase determines the ATP-synthesis rate. Sci. Rep. 2017;7(1):1–12. http://doi.org/10.1038/s41598-017-02836-4
21. Yaguzhinsky L.S., Boguslavsky L.I., Volkov A.G., Rakhmaninova A.B. Synthesis of ATP coupled with action of membrane protonic pumps at the octane–water interface. Nature. 1976;259(5543):494–496. https://doi.org/10.1038/259494a0
22. Lee J.W. Mitochondrial energetics with transmembrane electrostatically localized protons: do we have a thermotrophic feature? Sci Rep. 2021;11(1):14575. https://doi.org/10.1038/s41598-021-93853-x
23. Medvedev E., Stuchebrukhov A. Mechanism of long-range proton translocation along biological membranes. FEBS Lett. 2012;587(4):345–349. https://doi.org/10.1016/j.febslet.2012.12.010
24. Cherepanov D.A., Junge W., Mulkidjanian A.Y. Proton transfer dynamics at the membrane/water interface: dependence on the fixed and mobile pH buffers, on the size and form of membrane particles, and on the interfacial potential barrier. Biophys J. 2004;86(2):665–80. https://doi.org/10.1016/s0006-3495(04)74146-6
25. Amdursky N., Lin Y., Aho N., Groenhof G. Exploring fast proton transfer events associated with lateral proton diffusion on the surface of membranes. Proc. Natl. Acad. Sci. USA. 2019;116(7):2443–2451. https://doi.org/10.1073/pnas.1812351116
26. Golovnev A., Eikerling M. Theory of collective proton motion at interfaces with densely packed protogenic surface groups. J. Phys.: Condens. Matter. 2012;25(4):045010. https://doi.org/10.1088/0953-8984/25/4/045010
27. Kadantsev V.N., Goltsov A.N. Collective dynamics of domain structures in liquid crystalline lipid bilayers. Russian Technological Journal . 2022;10(4):44–54 https://doi.org/10.32362/2500-316X-2022-10-4-44-54
28. Shrivastava S., Schneider M.F. Evidence for two-dimensional solitary sound waves in a lipid controlled interface and its implications for biological signalling. J. Royal Soc. Interface. 2014;11(97):20140098. https://doi.org/10.1098/rsif.2014.0098
29. Gonzalez-Perez A., Budvytyte R., Mosgaard L.D., Nissen S., Heimburg T. Penetration of Action Potentials During Collision in the Median and Lateral Giant Axons of Invertebrates. Phys. Rev. X. 2014;4(3):031047. http://doi.org/10.1103/PhysRevX.4.031047
30. Lupichev L.N., Savin A.V., Kadantsev V.N. Synergetics of Molecular Systems. Series: Springer Series in Synergetics. Cham: Springer; 2015. 332 p. https://doi.org/10.1007/978-3-319-08195-3
31. Kadantsev V.N., Goltsov A.N., Kondakov M.A. Electrosoliton dynamics in a thermalized molecular chain. Rossiiskii tekhnologicheskii zhurnal. 2020;8(1):43–57 (in Russ.). https://doi.org/10.32362/2500-316X-2020-8-1-43-57
32. Bolterauer H., Tuszyński J.A., Satarić M.V. Fröhlich and Davydov regimes in the dynamics of dipolar oscillations of biological membranes. Phys. Rev. A. 1991;44(2):1366–1381. https://doi.org/10.1103/physreva.44.1366
33. Landau L.D., Lifshits E.M. Teoreticheskaya fizika (Theoretical Physics): in 10 v. V. 3. Kvantovaya mekhanika (nerelyativistskaya teoriya) (Quantum Mechanics (Non-Relativistic Theory)). Moscow: Fizmatlit; 2024. 800 p. (in Russ.). ISBN 5-9221-0057-2, 978-5-9221-0530-9
34. Wack D.C., Webb W.W. Synchrotron X-ray study of the modulated lamellar phase in the lecithin-water system. Phys. Rev. A. 1989;40(5):2712–2730. https://doi.org/10.1103/PhysRevA.40.2712
35. Goltsov A.N. Formation of quasilinear structure in lipid membranes. Biofizika. 1997;42(1):174–181.
36. Joubert F., Puff N. Mitochondrial Cristae Architecture and Functions: Lessons from Minimal Model Systems. Membranes (Basel). 2021;11(7):465. https://doi.org/10.3390/membranes11070465
37. Toth A., Meyrat A., Stoldt S., Santiago R., Wenzel D., Jakobs S., et al. Kinetic coupling of the respiratory chain with ATP synthase, but not proton gradients, drives ATP production in cristae membranes. Proc. Natl. Acad. Sci. USA. 2020;117(5): 2412–2421. https://doi.org/10.1073/pnas.1917968117
38. Patil N., Bonneau S., Joubert F., Bitbol A.F., Berthoumieux H. Mitochondrial cristae modeled as an out-of-equilibrium membrane driven by a proton field. Phys. Rev. E. 2020;102(2):022401. https://doi.org/10.1103/physreve.102.022401
39. Johnson A.S., Winlow W. The Soliton and the Action Potential – Primary Elements Underlying Sentience. Front. Physiol. 2018;9:779. https://doi.org/10.3389/fphys.2018.00779
40. Li S., Yan Z., Huang F., Zhang X., Yue T. How a lipid bilayer membrane responds to an oscillating nanoparticle: Promoted membrane undulation and directional wave propagation. Colloids Surf. B. Biointerfaces. 2020;187:110651. https://doi.org/10.1016/j.colsurfb.2019.110651
Supplementary files
|
1. Wave function of the ground state of proton (solid line) in the potential well generated by soliton of compression (dashed line) of lipid molecule polar groups in a quasi-one-dimensional lipid domain structure | |
Subject | ||
Type | Исследовательские инструменты | |
View
(21KB)
|
Indexing metadata ▾ |
- To investigate the molecular mechanisms of the direct proton transport along the water-membrane interface, we developed a model of proton movement along quasi-one-dimensional lateral domain structures in multicomponent lipid membranes.
- The results of modeling showed that the interaction between an excess proton on the membrane surface and a soliton of membrane compression leads to the proton being trapped by an acoustic soliton, followed by its transport by moving soliton.
- The developed model was applied to describe effective proton transport along the inner mitochondrial membrane and its role in the local coupling function of molecular complexes in cell bioenergetics.
Review
For citations:
Kadantsev V.N., Goltsov A.N. Lateral proton transport induced by acoustic solitons propagating in lipid membranes. Russian Technological Journal. 2025;13(2):111-120. https://doi.org/10.32362/2500-316X-2025-13-2-111-120. EDN: ATOWXW