Membrane associated thermosynthesis: MTS

Capacitor engines

 During chemiosmosis the membrane functions as a capacitor. Except for the proton pumps and ATPsynthase, the membrane is inert. In contrast, the membrane is active in MTS and PS0. The electrical potential across the membrane changes with the orientation and/or strength of the dipoles embedded within the membrane, which in turn change with the temperature or the light intensity.

MTS and PS0 are similar to capacitor-based devices that have been proposed for power generation in which use is made of cyclic changes in light or temperature [Clin61, Chil62, Gonz76]. Figure A describes a capacitor in which excited states are formed in the dielectric upon light absorption. These excited states have a higher polarizability ('excited electrons are loosely bound'), increasing the capacitor's capacity upon illumination. When switch-1 is closed the battery will charge the capacitor. Just before the end of illumination switch-1 is opened. During the following dark, the excited states decay and the capacity decreases, increasing the voltage. Upon the closing of switch-2, some charge then returns to the battery by the load, upon which work is done. Opening switch-2 then prepares the system for another light-dark cycle (see [Glaz82]).
In Figure A the voltage across the capacitor decreases upon illumination. By using an electret one can imagine a device in which the voltage increases upon illumination. But what is an electret? It is the electrical analogue of a magnet: just as a magnet contains a north and south pole, an electret contains a positive and a negative charge on its surface. Electrets can be certain minerals, wax, certain polymers. Electret behavior of biomolecules and even of nucleic acids has been reported.
When the electrical polarization of the electret strongly depends on the temperature it is called a pyroelectric; when this behaviour is sufficiently 'regular' it is called a ferroelectric.
In Figure B the electric field of the electret is larger than the field of the charges on the capacitor plates. Note that the electret is oriented with the dipole (minus to positive direction) oriented antiparallel to the direction of the field of the charges on the plate (which directs downwards). The result is that the induced dipole increases the voltage across the capacitor. In B switch-1 is therefore opened in the dark, and switch-2 is opened in the light.
The polarization changes in a pyroelectric can be used to gain free energy from cyclic temperature changes as sketched in Figure C.
Figure D finally describes a device which can gain free energy from both temperature and light changes.


capacitor devices

The surface of a spacecraft experiences in particular strong thermal cycling as it rotates in the sunlight. Such situation has been given the name of barbecue mode!
Instead of switches, one can also use diodes for appropriate regulation of the currents.


satellite device

MTS and PS0 function similar to these devices, with the membrane functioning as the capacitor, lipids or light-induced dipoles functioning as the capacitor dielectric, and ATPsynthase functioning as the battery/switches/load partial system.

Dipole layers




An electric potential difference can be obtained in many ways. Some depend on charge separation, which can be effected by friction - static electricity - or by magnetic induction. A voltage difference is however also present across a layer of electric dipoles. This is not only a theoretical idea: upon heating electrical dipoles are generated within some minerals (for instance tourmaline, a pyroelectric). One side of the mineral then becomes positive, the other negative. Because there is always some electrical conduction in air, such dipoles are slowly screened off by charges moving through the air. In water, electrical dipoles are screened off much faster by counterions.
A layer of electrical dipoles can be obtained by placing some particular molecules at the water surface. Soap molecules, for instance, are partly repelled by water, and partly attracted by it. As a result they collect at the water-air interface, and when the molecule is an electric dipole, as most larg molecules are, a layer of oriented electrical dipoles is obtained. The voltage difference across such a layer can be measured. Voltages as high as 1 V have been measured, but for biological important lipids values of a few hundred mV are typical.

monolayer transition The voltage across a monolayer may vary with the temperature. At a certain temperature the variation may be very strong. Such strong variation is considered to be evidence of a phase transition in the monolayer. Upon the transition the disorder in the layer increases, and the dipole potential decreases. Only the average component of the dipole moment, µ, normal to the surface, µ ⊥ , contributes to the dipole potential. During the phase transition this average normal component decreases.


Within cells compartimentation occurs by membranes, also called biomembranes, which consist of two monolayers placed back to back. The membranes may be very good electrical insulators. As a result a voltage difference may be present across the membrane, and the membrane can function as capacitor.



In many biomembranes the constituting monolayers have a different composition, the biomembrane is 'asymmetric'. The dipole potentials of the two monolayers then do not to cancel each other out, and the membrane then has an overall net dipole potential. This membrane dipole potential is screened off by counterions, but such screening off will not be instantaneous. When the net dipole potential changes as a result of a temperature change, the membrane potential must then temporarily change accordingly, to approach zero again later because of conduction.

The MTS cycle

 MTS makes use of the membrane potential change that is caused by the membrane dipole change, in turn the result of a change in temperature. The membrane potential drives ATP synthesis by letting protons 'fall' through ATPsynthase. In regular chemiosmosis the protons are pumped back. How do they return in MTS?
A simple, but valid, solution, is to let them return by conduction. The membrane potential then must change sign, though. A small complication is that biomembranes conduct anions much better than cations; as a result there may be some salt accumulation at one side of the membrane, but this problem may be surmountable (and the associated density changes could be of use during vertical migrations through thermoclines in natural waters).
A second solution is possible, in which the protons are pumped back by the ATPsynthase enzyme itself, working in reverse mode. It then would cost ATP to return these protons. When proton / ATP ratio during ATP synthesis is the same as during proton pumping, then no ATP can be won from the thermal cycle. When the ratio can vary, ATP can be won. So can the H+/ATP ratio vary?
Such variation has been proposed previously [Oosa86]. Van Walraven et al. reported that the H+/ATP stochiometry of Synechoccus varies with the temperature [VanW97]. In membrane vesicles from cells grown at 50°C it is almost 4, from grown at 38°C almost 3. The work of Dilley, who found ATP synthesis at very low potential/pH difference across the membrane under some conditions, can be explained by the occurrence of a high mode under those conditions.

Consider first the relation between membrane potential and H+/ATP ratio. When the ratio is 1, it takes about 480 mV to synthesize ATP; is the ratio 2, it takes 480 / 2 = 240 mV to synthesize ATP, more generally, at ratio n it takes 480 / n mV. Conversely, protons can be pumped using ATP as long as the membrane voltage is lower than 480 mV (assuming H+/ATP ratio, or 'mode', 1), or 240 mV (mode 2), or, more generally, 480 / m mV (mode m).



There is much literature describing H+/ATP ratio variations in a continuous, non-discrete way. References can be found in articles by Hans Westerhoff (which describe the concept of slip):
Hans Westerhoff at the Vrije Universiteit van Amsterdam

and on the website of Anishkin and Lemeshko:
Andrey Anishkin of the University of Maryland and Victor Lemeshko at the University of Medellin


The author finds continuous variations difficult to envisage on an atomic scale. Nevertheless, even continuous variations could permit ATP gain from thermal cycling, at proper variation and when the associated free energy dissipation is small. In order to simplify the analysis from now on only changes in integer values are considered, and no continuous variations.

Cyclic variations of membrane potential during a thermal cycle, and associated changes in membrane potential due to voltage-activated ATP synthesis and proton pumping with different H+/ATP modes during MTS.



The emergence of ATPsynthase

 MTS uses the corresponding change in membrane voltage for synthesizing ATP in the standard chemiosmotic way. How ATPsynthase could do this, and how it could have evolved from pF1?

The ATPsynthase enzyme is complex. The structure of the F1 part has been obtained, but the structure of the Fo is still being investigated. The detailed function of the enzyme is therefore not yet established. The origin of the enzyme can be modelled [Mull95]. Whether the tentative model is correct or not does not concern us too much; any definite structure will have to perform the same functions as described here, and attribute for instance a function to the tightly-bound ATPs.

membrane-associated pF1, pαβ
The evolution of ATPsynthase starts with a pF1 that is bound to a membrane that undergoes a thermotropic phase transition. Since the temperature interval required for a transition decreases with size, the advantage for the pF1 would be a smaller temperature interval for PTS to occur. The name pαβ is used to indicate that it may concern a progenitor of the α and β subunits present in contemporary pF1.

pFopαβ proton pump
The next step is the acquisition of a proton carrier, a pFo: F1 can reversibly yield the energy for the the carrier to traverse the membrane. It obtains this energy by reversibly strongly and loosely binding ATP. The ATP remains bound all the time. The membrane thins upon the thermotropic phase transition, uncovering one of the proton binding sites on the carrier. The figure speaks for itself: during a thermal cycle the engine pumps protons.



pFoF1, ATPsynthase with different H+/ATP ratio
By adding a pF1 unit to the proton pump an enzyme is obtained that can consume and produce ATP. The pF1 unit that can exchange ATP and ADP with the mediun is a progenitor of the β subunit of contemporary F1, the pF1 unit that does not exchange ATP is a progenitor of the α subunit.




ATPsynthase with different H+/ATP ratios during isothermy
pFoF1 still may require thermal cycling. For PS0 the capability to vary the mode during constant temperature, i.e. is mode regulation by the voltage alone.


contemporary ATPsynthase
Contemporary ATPsynthase may not have a variable mode at all, although mode variability may still give an evolutionary advantage. A variable mode can be compared to a gear box; it may not strictly be necessary in a car, but it sure makes driving easier!

Possible applications of MTS

The possible applications of MTS are numerous, and are discussed later. The applications can be divided in cases where the membrane is passively moved, such as where it is carried along by convection currents, and cases where it moves actively, for instance by migrating through thermoclines in natural waters.

Discussion

 MTS makes use of an electrical potential. Use of the electrical potential in the origin of life has of course been proposed previously in general terms - we are able here to give a specific example.
Davies [Davi98, p 14]:

Another idea, popular in the eigteenth century, was to identify the life force with electricity. . . . Belief that electricity could revivify matter was dramatically exploited by Mary Shelley in her famous novel Frankenstein . . .

The next page gives a model for the evolution of bacterial photosynthesis from MTS: Photosystem 0.


Copyright © 1999-2005 Anthonie W.J. Muller
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