Real Space and Time Imaging of Collective Headgroup Dipole Motions in Zwitterionic Lipid Bilayers
Abstract
Lipid bilayers are supramolecular structures responsible for a range of processes, such as transmembrane transport of ions and solutes, and sorting and replication of genetic materials, to name just a few. Some of these processes are transient and currently, cannot be visualized in real space and time. Here, we developed an approach using 1D, 2D, and 3D Van Hove correlation functions to image collective headgroup dipole motions in zwitterionic phospholipid bilayers. We show that both 2D and 3D spatiotemporal images of headgroup dipoles are consistent with commonly understood dynamic features of fluids. However, analysis of the 1D Van Hove function reveals lateral transient and re-emergent collective dynamics of the headgroup dipoles—occurring at picosecond time scales—that transmit and dissipate heat at longer times, due to relaxation processes. At the same time, the headgroup dipoles also generate membrane surface undulations due a collective tilting of the headgroup dipoles. A continuous intensity band of headgroup dipole spatiotemporal correlations—at nanometer length and nanosecond time scales—indicates that dipoles undergo stretching and squeezing elastic deformations. Importantly, the above mentioned intrinsic headgroup dipole motions can be externally stimulated at GHz-frequency scale, enhancing their flexoelectric and piezoelectric capabilities (i.e., increased conversion efficiency of mechanical energy into electric energy).more »
- Authors:
-
[1];
[2];
[4];
[5]
- Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Shull-Wollan Center
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Nanophase Materials Sciences (CNMS)
- Volgograd State Technical University (Russia)
- Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Shull-Wollan Center; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Materials Science and Technology Division
- Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Shull-Wollan Center; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Neutron Scattering Division
- Publication Date:
- Research Org.:
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Materials Sciences & Engineering Division (MSE); National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF)
- OSTI Identifier:
- 1971016
- Grant/Contract Number:
- AC05-00OR22725; 2219289
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Membranes
- Additional Journal Information:
- Journal Volume: 13; Journal Issue: 4; Journal ID: ISSN 2077-0375
- Publisher:
- MDPI
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; zwitterionic lipid bilayers; POPC; DPPC; headgroup dipoles; collective dipole motions; Van Hove correlation functions; heat transfer; surface undulations; piezoelectricity; flexoelectricity
Citation Formats
Bolmatov, Dima, Collier, Charles Patrick, Zav’yalov, Dmitry, Egami, Takeshi, and Katsaras, John. Real Space and Time Imaging of Collective Headgroup Dipole Motions in Zwitterionic Lipid Bilayers. United States: N. p., 2023.
Web. doi:10.3390/membranes13040442.
Bolmatov, Dima, Collier, Charles Patrick, Zav’yalov, Dmitry, Egami, Takeshi, & Katsaras, John. Real Space and Time Imaging of Collective Headgroup Dipole Motions in Zwitterionic Lipid Bilayers. United States. https://doi.org/10.3390/membranes13040442
Bolmatov, Dima, Collier, Charles Patrick, Zav’yalov, Dmitry, Egami, Takeshi, and Katsaras, John. Tue .
"Real Space and Time Imaging of Collective Headgroup Dipole Motions in Zwitterionic Lipid Bilayers". United States. https://doi.org/10.3390/membranes13040442. https://www.osti.gov/servlets/purl/1971016.
@article{osti_1971016,
title = {Real Space and Time Imaging of Collective Headgroup Dipole Motions in Zwitterionic Lipid Bilayers},
author = {Bolmatov, Dima and Collier, Charles Patrick and Zav’yalov, Dmitry and Egami, Takeshi and Katsaras, John},
abstractNote = {Lipid bilayers are supramolecular structures responsible for a range of processes, such as transmembrane transport of ions and solutes, and sorting and replication of genetic materials, to name just a few. Some of these processes are transient and currently, cannot be visualized in real space and time. Here, we developed an approach using 1D, 2D, and 3D Van Hove correlation functions to image collective headgroup dipole motions in zwitterionic phospholipid bilayers. We show that both 2D and 3D spatiotemporal images of headgroup dipoles are consistent with commonly understood dynamic features of fluids. However, analysis of the 1D Van Hove function reveals lateral transient and re-emergent collective dynamics of the headgroup dipoles—occurring at picosecond time scales—that transmit and dissipate heat at longer times, due to relaxation processes. At the same time, the headgroup dipoles also generate membrane surface undulations due a collective tilting of the headgroup dipoles. A continuous intensity band of headgroup dipole spatiotemporal correlations—at nanometer length and nanosecond time scales—indicates that dipoles undergo stretching and squeezing elastic deformations. Importantly, the above mentioned intrinsic headgroup dipole motions can be externally stimulated at GHz-frequency scale, enhancing their flexoelectric and piezoelectric capabilities (i.e., increased conversion efficiency of mechanical energy into electric energy). In conclusion, we discuss how lipid membranes can provide molecular-level insights about biological learning and memory, and as platforms for the development of the next generation of neuromorphic computers.},
doi = {10.3390/membranes13040442},
journal = {Membranes},
number = 4,
volume = 13,
place = {United States},
year = {Tue Apr 18 00:00:00 EDT 2023},
month = {Tue Apr 18 00:00:00 EDT 2023}
}
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Works referenced in this record:
Low-THz Vibrations of Biological Membranes
journal, January 2023
- Luyet, Chloe; Elvati, Paolo; Vinh, Jordan
- Membranes, Vol. 13, Issue 2
The dynamic face of lipid membranes
journal, January 2021
- Gupta, Sudipta; Ashkar, Rana
- Soft Matter, Vol. 17, Issue 29
Nanoscale Structure and Dynamics of Model Membrane Lipid Raft Systems, Studied by Neutron Scattering Methods
journal, April 2022
- Ahmadi, Delaram; Thompson, Katherine C.; García Sakai, Victoria
- Frontiers in Physics, Vol. 10
Multiple Interacting Collective Modes and Phonon Gap in Phospholipid Membranes
journal, July 2018
- D’Angelo, Giovanna; Nibali, Valeria Conti; Wanderlingh, Ulderico
- The Journal of Physical Chemistry Letters, Vol. 9, Issue 15
Multiscale lipid membrane dynamics as revealed by neutron spectroscopy
journal, July 2022
- Sharma, V. K.; Mamontov, E.
- Progress in Lipid Research, Vol. 87
Dynamic response on a nanometer scale of binary phospholipid-cholesterol vesicles: Low-frequency Raman scattering insight
journal, November 2021
- Surovtsev, N. V.; Adichtchev, S. V.
- Physical Review E, Vol. 104, Issue 5
Functional lipid pairs as building blocks of phase-separated membranes
journal, February 2020
- Soloviov, Dmytro; Cai, Yong Q.; Bolmatov, Dima
- Proceedings of the National Academy of Sciences, Vol. 117, Issue 9
Feeling the hidden mechanical forces in lipid bilayer is an original sense
journal, May 2014
- Anishkin, A.; Loukin, S. H.; Teng, J.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 22
Stress Propagation through Biological Lipid Bilayers in Silico
journal, September 2017
- Aponte-Santamaría, Camilo; Brunken, Jan; Gräter, Frauke
- Journal of the American Chemical Society, Vol. 139, Issue 39
Phonon-mediated lipid raft formation in biological membranes
journal, October 2020
- Bolmatov, Dima; Kinnun, Jacob J.; Katsaras, John
- Chemistry and Physics of Lipids, Vol. 232
Modulation of Membrane Fluidity to Control Interfacial Water Structure and Dynamics in Saturated and Unsaturated Phospholipid Vesicles
journal, October 2020
- Mondal, Dipankar; Malik, Sheeba; Banerjee, Pavel
- Langmuir, Vol. 36, Issue 41
Optimal estimates of self-diffusion coefficients from molecular dynamics simulations
journal, July 2020
- Bullerjahn, Jakob Tómas; von Bülow, Sören; Hummer, Gerhard
- The Journal of Chemical Physics, Vol. 153, Issue 2
Ion-Induced Defect Permeation of Lipid Membranes
journal, February 2014
- Vorobyov, Igor; Olson, Timothy E.; Kim, Jung H.
- Biophysical Journal, Vol. 106, Issue 3
Passive transport of Ca2+ ions through lipid bilayers imaged by widefield second harmonic microscopy
journal, February 2023
- Eremchev, Maksim; Roesel, David; Poojari, Chetan S.
- Biophysical Journal, Vol. 122, Issue 4
Double membrane formation in heterogeneous vesicles
journal, January 2020
- Bolmatov, Dima; Carrillo, Jan-Michael Y.; Sumpter, Bobby G.
- Soft Matter, Vol. 16, Issue 38
Is the tilt of the lipid head group correlated with the number of intermolecular interactions at the bilayer interface?
journal, April 2018
- Baczynski, Krzysztof; Markiewicz, Michal; Pasenkiewicz‐Gierula, Marta
- FEBS Letters, Vol. 592, Issue 9
Probing molecular forces in multi-component physiological membranes
journal, January 2018
- Ray, Arjun; Gräter, Frauke; Thukral, Lipi
- Physical Chemistry Chemical Physics, Vol. 20, Issue 4
Understanding Conformational Dynamics of Complex Lipid Mixtures Relevant to Biology
journal, October 2018
- Friedman, Ran; Khalid, Syma; Aponte-Santamaría, Camilo
- The Journal of Membrane Biology, Vol. 251, Issue 5-6
The push-to-open mechanism of the tethered mechanosensitive ion channel NompC
journal, June 2021
- Wang, Yang; Guo, Yifeng; Li, Guanluan
- eLife, Vol. 10
Lipid–protein forces predict conformational changes in a mechanosensitive channel
journal, December 2020
- Daday, Csaba; de Groot, Bert L.
- European Biophysics Journal, Vol. 50, Issue 2
The Phonon Theory of Liquids and Biological Fluids: Developments and Applications
journal, August 2022
- Bolmatov, Dima
- The Journal of Physical Chemistry Letters, Vol. 13, Issue 31
Unified phonon-based approach to the thermodynamics of solid, liquid and gas states
journal, December 2015
- Bolmatov, Dima; Zav’yalov, Dmitry; Zhernenkov, Mikhail
- Annals of Physics, Vol. 363
Symmetry breaking gives rise to energy spectra of three states of matter
journal, September 2013
- Bolmatov, Dima; Musaev, Edvard T.; Trachenko, K.
- Scientific Reports, Vol. 3, Issue 1
The phonon theory of liquid thermodynamics
journal, May 2012
- Bolmatov, D.; Brazhkin, V. V.; Trachenko, K.
- Scientific Reports, Vol. 2, Issue 1
Two cations, two mechanisms: interactions of sodium and calcium with zwitterionic lipid membranes
journal, January 2017
- Javanainen, Matti; Melcrová, Adéla; Magarkar, Aniket
- Chemical Communications, Vol. 53, Issue 39
Accurate Binding of Sodium and Calcium to a POPC Bilayer by Effective Inclusion of Electronic Polarization
journal, April 2018
- Melcr, Josef; Martinez-Seara, Hector; Nencini, Ricky
- The Journal of Physical Chemistry B, Vol. 122, Issue 16
Heterosynaptic plasticity in biomembrane memristors controlled by pH
journal, August 2022
- McClintic, William T.; Scott, Haden L.; Moore, Nick
- MRS Bulletin, Vol. 48, Issue 1
Calcium Ion Binding at the Lipid–Water Interface Alters the Ion Permeability of Phospholipid Bilayers
journal, November 2021
- Deplazes, Evelyne; Tafalla, Beatriu Domingo; Murphy, Christopher
- Langmuir, Vol. 37, Issue 48
Coexistence of lipid phases in multilayer phospholipid films probed by Raman mapping
journal, January 2022
- Shamaeva, Daria V.; Okotrub, Konstantin A.; Surovtsev, Nikolay V.
- The Analyst, Vol. 147, Issue 16
Lipid Vesicles and Other Polymolecular Aggregates—From Basic Studies of Polar Lipids to Innovative Applications
journal, November 2021
- Walde, Peter; Ichikawa, Sosaku
- Applied Sciences, Vol. 11, Issue 21
Deciphering Melatonin-Stabilized Phase Separation in Phospholipid Bilayers
journal, August 2019
- Bolmatov, Dima; McClintic, William T.; Taylor, Graham
- Langmuir, Vol. 35, Issue 37
Role of polyunsaturated phospholipids in liquid-ordered and liquid-disordered phases
journal, January 2021
- Yang, Jing; Jin, Jianyu; Li, Shiben
- RSC Advances, Vol. 11, Issue 44
Role of lipid rafts in persistent Helicobacter pylori infection: a narrative review
journal, March 2022
- Liu, Renjie; Chen, Yuzuo; Yang, Lu
- Annals of Translational Medicine, Vol. 10, Issue 6
Dynamic Water Hydrogen-Bond Networks at the Interface of a Lipid Membrane Containing Palmitoyl-Oleoyl Phosphatidylglycerol
journal, March 2018
- Karathanou, Konstantina; Bondar, Ana-Nicoleta
- The Journal of Membrane Biology, Vol. 251, Issue 3
Hydration dynamics of a lipid membrane: Hydrogen bond networks and lipid-lipid associations
journal, March 2018
- Srivastava, Abhinav; Debnath, Ananya
- The Journal of Chemical Physics, Vol. 148, Issue 9
Intermolecular Hydrogen-Bond Interactions in DPPE and DMPC Phospholipid Membranes Revealed by Far-Infrared Spectroscopy
journal, October 2021
- Conti Nibali, Valeria; Branca, Caterina; Wanderlingh, Ulderico
- Applied Sciences, Vol. 11, Issue 21
X-ray diffraction studies of oriented lipid bilayers
journal, May 1995
- Katsaras, J.
- Biochemistry and Cell Biology, Vol. 73, Issue 5-6
Lipid Bilayer Structure Determined by the Simultaneous Analysis of Neutron and X-Ray Scattering Data
journal, September 2008
- Kučerka, Norbert; Nagle, John F.; Sachs, Jonathan N.
- Biophysical Journal, Vol. 95, Issue 5
Perspective on the Martini model
journal, January 2013
- Marrink, Siewert J.; Tieleman, D. Peter
- Chemical Society Reviews, Vol. 42, Issue 16
CHARMM-GUI: A web-based graphical user interface for CHARMM
journal, March 2008
- Jo, Sunhwan; Kim, Taehoon; Iyer, Vidyashankara G.
- Journal of Computational Chemistry, Vol. 29, Issue 11
CHARMM-GUI Membrane Builder toward realistic biological membrane simulations
journal, August 2014
- Wu, Emilia L.; Cheng, Xi; Jo, Sunhwan
- Journal of Computational Chemistry, Vol. 35, Issue 27
Correlated atomic dynamics in liquid seen in real space and time
journal, November 2020
- Egami, Takeshi; Shinohara, Yuya
- The Journal of Chemical Physics, Vol. 153, Issue 18
Seeing real-space dynamics of liquid water through inelastic x-ray scattering
journal, December 2017
- Iwashita, Takuya; Wu, Bin; Chen, Wei-Ren
- Science Advances, Vol. 3, Issue 12
Split-pulse X-ray photon correlation spectroscopy with seeded X-rays from X-ray laser to study atomic-level dynamics
journal, December 2020
- Shinohara, Yuya; Osaka, Taito; Inoue, Ichiro
- Nature Communications, Vol. 11, Issue 1
Observation of dynamic atom-atom correlation in liquid helium in real space
journal, May 2017
- Dmowski, W.; Diallo, S. O.; Lokshin, K.
- Nature Communications, Vol. 8, Issue 1
Real-Space Local Dynamics of Molten Inorganic Salts Using Van Hove Correlation Function
journal, June 2022
- Shinohara, Yuya; Ivanov, Alexander S.; Maltsev, Dmitry
- The Journal of Physical Chemistry Letters, Vol. 13, Issue 25
Clarification of the ripple phase of lecithin bilayers using fully hydrated, aligned samples
journal, May 2000
- Katsaras, J.; Tristram-Nagle, S.; Liu, Y.
- Physical Review E, Vol. 61, Issue 5
Experimental determination of the temperature-dependent Van Hove function in a Zr 80 Pt 20 liquid
journal, February 2020
- Ashcraft, R.; Wang, Z.; Abernathy, D. L.
- The Journal of Chemical Physics, Vol. 152, Issue 7
Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations
journal, May 2016
- Zhernenkov, Mikhail; Bolmatov, Dima; Soloviov, Dmitry
- Nature Communications, Vol. 7, Issue 1
Crossover from picosecond collective to single particle dynamics defines the mechanism of lateral lipid diffusion
journal, November 2018
- Bolmatov, Dima; Cai, Yong Q.; Zav’yalov, Dmitry
- Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1860, Issue 11
Molecular Picture of the Transient Nature of Lipid Rafts
journal, April 2020
- Bolmatov, Dima; Soloviov, Dmytro; Zhernenkov, Mikhail
- Langmuir, Vol. 36, Issue 18
Revealing the Mechanism of the Viscous-to-Elastic Crossover in Liquids
journal, July 2015
- Bolmatov, Dima; Zhernenkov, Mikhail; Zav’yalov, Dmitry
- The Journal of Physical Chemistry Letters, Vol. 6, Issue 15
Thermally triggered phononic gaps in liquids at THz scale
journal, January 2016
- Bolmatov, Dima; Zhernenkov, Mikhail; Zav’yalov, Dmitry
- Scientific Reports, Vol. 6, Issue 1
Disentangling Memristive and Memcapacitive Effects in Droplet Interface Bilayers Using Dynamic Impedance Spectroscopy
journal, April 2022
- Sacci, Robert L.; Scott, Haden L.; Liu, Zening
- Advanced Electronic Materials, Vol. 8, Issue 5
Mesoscopic Undulations and Thickness Fluctuations in Lipid Bilayers from Molecular Dynamics Simulations
journal, July 2000
- Lindahl, Erik; Edholm, Olle
- Biophysical Journal, Vol. 79, Issue 1
Lipid Domain Co-localization Induced by Membrane Undulations
journal, February 2017
- Haataja, Mikko P.
- Biophysical Journal, Vol. 112, Issue 4
Measuring shape fluctuations in biological membranes
journal, May 2016
- Monzel, C.; Sengupta, K.
- Journal of Physics D: Applied Physics, Vol. 49, Issue 24
Curvature–undulation coupling as a basis for curvature sensing and generation in bilayer membranes
journal, August 2016
- Bradley, Ryan P.; Radhakrishnan, Ravi
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 35
Probing lipid membrane bending mechanics using gold nanorod tracking
journal, March 2022
- Molaei, Mehdi; Kandy, Sreeja Kutti; Graber, Zachary T.
- Physical Review Research, Vol. 4, Issue 1
Determination of Elastic Parameters of Lipid Membranes with Molecular Dynamics: A Review of Approaches and Theoretical Aspects
journal, November 2022
- Pinigin, Konstantin V.
- Membranes, Vol. 12, Issue 11
Dynamical nonlinear memory capacitance in biomimetic membranes
journal, July 2019
- Najem, Joseph S.; Hasan, Md Sakib; Williams, R. Stanley
- Nature Communications, Vol. 10, Issue 1
Neuromorphic functions with a polyelectrolyte-confined fluidic memristor
journal, January 2023
- Xiong, Tianyi; Li, Changwei; He, Xiulan
- Science, Vol. 379, Issue 6628
Long-term memory and synapse-like dynamics in two-dimensional nanofluidic channels
journal, January 2023
- Robin, P.; Emmerich, T.; Ismail, A.
- Science, Vol. 379, Issue 6628
A Brief History of Long-Term Potentiation
journal, January 2017
- Nicoll, Roger A.
- Neuron, Vol. 93, Issue 2
Evidence for long-term potentiation in phospholipid membranes
journal, December 2022
- Scott, Haden L.; Bolmatov, Dima; Podar, Peter T.
- Proceedings of the National Academy of Sciences, Vol. 119, Issue 50
Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path
journal, July 1973
- Bliss, T. V. P.; Lømo, T.
- The Journal of Physiology, Vol. 232, Issue 2
Chirality of lipids makes fluid lamellar phases piezoelectric
journal, January 2009
- Harden, John; Diorio, Nicholas; Petrov, Alexander G.
- Physical Review E, Vol. 79, Issue 1
Piezoelectricity of phospholipids: a possible mechanism for mechanoreception and magnetoreception in biology
journal, April 2008
- Jákli, A.; Harden, J.; Notz, C.
- Liquid Crystals, Vol. 35, Issue 4
Remote control of ion channels and neurons through magnetic-field heating of nanoparticles
journal, June 2010
- Huang, Heng; Delikanli, Savas; Zeng, Hao
- Nature Nanotechnology, Vol. 5, Issue 8
Mechano-capacitive properties of polarized membranes
journal, January 2015
- Mosgaard, Lars D.; Zecchi, Karis A.; Heimburg, Thomas
- Soft Matter, Vol. 11, Issue 40
Wireless magnetothermal deep brain stimulation
journal, March 2015
- Chen, R.; Romero, G.; Christiansen, M. G.
- Science, Vol. 347, Issue 6229
Infrared light excites cells by changing their electrical capacitance
journal, January 2012
- Shapiro, Mikhail G.; Homma, Kazuaki; Villarreal, Sebastian
- Nature Communications, Vol. 3, Issue 1
The mechanoelectrical response of droplet interface bilayer membranes
journal, January 2016
- Freeman, E. C.; Najem, J. S.; Sukharev, S.
- Soft Matter, Vol. 12, Issue 12
Emergent Optical Phononic Modes upon Nanoscale Mesogenic Phase Transitions
journal, May 2017
- Bolmatov, Dima; Zhernenkov, Mikhail; Sharpnack, Lewis
- Nano Letters, Vol. 17, Issue 6
Anomalous Nanoscale Optoacoustic Phonon Mixing in Nematic Mesogens
journal, April 2018
- Bolmatov, Dima; Soloviov, Dmytro; Zav’yalov, Dmitry
- The Journal of Physical Chemistry Letters, Vol. 9, Issue 10
Quantification of in-plane flexoelectricity in lipid bilayers
journal, June 2021
- Thomas, Nidhin; Agrawal, Ashutosh
- EPL (Europhysics Letters), Vol. 134, Issue 6
Thermal effects on neurons during stimulation of the brain
journal, October 2022
- Kim, TaeKen; Kadji, Herve; Whalen, Andrew J.
- Journal of Neural Engineering, Vol. 19, Issue 5
A lateral electric field inhibits gel-to-fluid transition in lipid bilayers
journal, January 2022
- Thomas, Nidhin; Agrawal, Ashutosh
- Soft Matter, Vol. 18, Issue 34
The excitable fluid mosaic
journal, March 2023
- Heimburg, Thomas
- Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1865, Issue 3