Piezoelectricity of phospholipids : A possible mechanism for mechano-, and magneto-receptions in biology

Classically, the phospholipid bilayer within the cell membrane has been considered as a flexible and self-healing barrier between the inside and outside of the cell, as well as a structural unit to support functional proteins. Here we show that the phospholipids may not play just a passive role, but may act as active transducers. By periodically shearing and compressing films of hydrated L-α-Phosphatidylcholine, we induced tilt of the molecules with respect to the bilayer’s normal and produced electric current perpendicular to the tilt plane. This effect occurs due to the spontaneous assembly of the chiral phospholipid molecules to stack in bilayers, corresponding to a SmA* liquid crystal phase with D∞ symmetry. Tilting the molecules with respect to these layers induces a transition to a ferroelectric SmC* phase with C2 polar symmetry where the polarization is normal to the tilt plane. We find that a 5 degree tilt yields a polarization of 300 nC/cm and propose that this piezoelectric effect can couple with functional units and create new ways to convert mechanical stimuli into electric signals within the membrane. We suggest that this coupling allows for a wide variety of sensory possibilities such as mechano-reception (the sensing of mechanical distortions). We also hypothesize that rotation of magnetic particles found in migratory animals can induce local reorientation of the lipid molecules, which via this piezoelectric effect can produce electric signals that may trigger firing of nerve cells, thus allowing navigation based on magnetic information. We demonstrate this hypothesis by generating electric currents in hydrated phospholipids doped with 0.5wt% of ferrofluid of magnetite (Fe3O4) nanoparticles when less than a 100G alternating magnetic field. Introduction Lipids are important components in biological systems, specifically when dealing with the structure of cellular membranes. The cellular membrane fulfills the following functions critical to cellular survival; it acts as a flexible, self-healing barrier between the cell and its environment and it also acts as a structural unit for functional proteins. The membrane, however, does not have a purely passive role. There is now recognition of the importance that lipid organization within the cell membranes plays in controlling protein function and many disease states have been associated with aberrations of these lipid/protein interactions. A number of these interactions occur via electric signals. For example some membranes swell or become birefringent in response to voltage changes, which was interpreted as a converse piezoelectric or electroclinic effect, respectively. Ion channels sensitive to membrane stretch have been observed in muscle cells and piezoelectric models of the outer hair cell composite membranes have been considered. These latter models are based on the flexoelectric properties of the lipid bilayers, which are related to membrane curvature resulting in polarization normal to the lipid bilayers as discussed extensively by Petrov. Using liquid crystal terminology, a lipid bilayer can electronic-Liquid Crystal Communications April 10, 2007 http://www.e-lc.org/docs/2007_04_09_12_01_56 2 be considered as a SmA* phase (Sm stands for smectic, which indicates layered structure; A means that the average molecular orientation (director) is normal to the layers, and * indicates that the constituent molecules are chiral). Such a phase has D∞ symmetry and therefore must be piezoelectric, because by tilting the molecules, induced by shear and/or layer compression, one induces a SmC* phase, which has polar C2 symmetry with the polar axis normal to the tilt plane. In this paper we concentrate on this piezoelectric property of bare lipid bilayers. We show that piezoelectricity of lipid bilayers might explain previously observed ferroelectric-like behavior of ion channels and may have consequences in various sensory mechanisms. As opposed to the flexoelectric polarization, here the tilt induced polarization occurs within the insulating chains of the bilayers and therefore cannot be screened out by free ions of the surrounding aqueous plasma. We studied these properties using a hydrated phospholipid extract of egg yolk from Avanti Inc., which forms a stable SmA* liquid crystal phase in bulk over a wide temperature range including the room temperature. The pictorial representation of the physical mechanism of the piezoelectricity, and the molecular structure of the major phospholipid component of the mixture, L-α-Phosphatidylcholine, are illustrated in Figure 1. Figure 1: Illustration of the molecular structure of phospholipid L-α-Phosphatidylcholine and of the piezoelectricity of a lipid bilayer. A tilt of the average molecular orientation (director) with respect to the layer normal, induced by mechanical shear and/or layer compression, leads to a SmC* configuration with polarization normal to the tilt (shear) plane. We assert that the lipid bilayers of cell membranes have this local SmA* structure, suggesting that real biological membranes are piezoelectric and electric charges are generated along the membrane when the lipids become tilted due to mechanical stimuli. Furthermore, we believe that cell membrane piezoelectricity may have numerous applications in biological processes. For example, it could explain communication between proteins embedded in cell membranes, or allow the conversion of external stimuli to electric signals within sensory proteins. One specific sensory mechanism that we suspect might be possible is magneto-reception, where animals use ferromagnetic particles to sense local changes in magnetic fields. Homing pigeons, as well as many other animals have the ability to travel long distances without landmarks and arrive at their destinations with very high accuracy. For example, salmon, having spent most of their life in electronic-Liquid Crystal Communications April 10, 2007 http://www.e-lc.org/docs/2007_04_09_12_01_56 3 the ocean will one day return to their place of birth in a mountain stream far away. The artic tern travels 20,000km one way from Antarctica to their breeding grounds in the Artic. The fact that magnetite (Fe3O4) is found within all of these animals, indicate that the Earth’s magnetic fields might play some role in their ability to navigate (magnetoreception). Magnetoreception can provide an animal with both orientational and positional information. Although the use of magnetoreception for directional information in migratory animals is well established experimentally, it is not clear by which biophysical mechanism magnetoreception is achieved. However it is known that the magnetic particles form chains linked by microtubule-like strands to a few ion-channels in the membrane of the receptor cell. We hypothesize therefore, that the rotation of magnetic particles cause mechanical deformations of the membrane by selectively pulling the microtubules, thus inducing piezoelectric signals, which in turn, triggers the ion channels that fire nerve cells. Piezoelectricity is sensitive to both the direction and magnitude of the mechanical strains, thus by comparing the electric signals in different channels the brain can calculate the direction and magnitude of the local magnetic fields.