A team of Russian, Czech and German researchers gained a new perspective on the properties of three materials of biological origin. Besides two reference materials with well-studied properties—serum and albumin and cytochrome C—the researchers looked at the extracellular matrix of the Shewanella oneidensis MR-1 bacterium, which is part of biofuel cells.
The team measured the materials’ dynamic conductivity and dielectric permittivity in a wide range of frequencies and temperatures. In order to interpret their findings, the researchers used theoretical approaches and concepts from condensed matter physics.
"So far, the formalism of condensed matter physics has only found limited use in classical biochemistry and biophysics. As a result, certain interesting effects evade our attention," says Konstantin Motovilov, a senior research scientist at the Laboratory of Terahertz Spectroscopy. "When we do make use of this language, we acquire new ways of modeling observed phenomena and describing biological structures. In our paper, we characterize the behavior of proteins, considered as classical amorphous semiconductors, with the help of the formalism of condensed matter physics."
There are multiple mechanisms of electrical conductivity. For each one there is a corresponding theory that describes the properties of certain materials. For example, the conductivity in metals is adequately explained by the Drude theory. Electrical conductivity is the opposite of electrical resistivity. Within the Drude model, this property doesn’t depend strongly on frequency up to the frequency of the collisions between charge carriers and lattice or impurities.
A large group of conductive materials does not fit this description, but their behavior in an external electromagnetic field is fascinating. Some of these materials include glasses, ionic conductors and amorphous semiconductors.
In order to quantitatively describe the electrical properties of these materials, another theory was proposed about 40 years ago by Andrezej Karol Jonscher, an English physicist. According to this theory, charge carriers can be considered as free at room temperature, provided the alternating current frequency doesn’t exceed several megahertz. Under these conditions, the Drude model is applicable and conductivity is nearly constant. If the frequency is higher, this description is no longer valid and there is an increase in conductivity proportional to a certain power of frequency. The same effect is observed for materials that are gradually cooled, even if the frequency is constant.
Different materials show similar behavior. If you restate the dependencies, the relations for all materials turn out to be identical, revealing the so-called Universal Dielectric Response (UDR). This phenomenon was thoroughly investigated in a study that examined the conduction in glasses and other amorphous materials, offering new insights into their structure and properties.
The authors of the paper showed that Jonscher’s law of conductivity applies to three organic materials. Among them are well-known reference proteins, bovine serum albumin and bovine heart cytochrome C. The structural, physical and chemical properties have been investigated in detail so the researchers used them as reference materials.
In addition, they examined the extracellular matrix and filaments (EMF) of the Shewanella oneidensis MR-1 bacterium, which can produce electricity in biological fuel cells. S. oneidensis has been used in studies with a focus on alternative energy sources, so its electrical properties are of interest to researchers and engineers. In 2010, a team of researchers from the U.S. and Canada showed that the bacterium's extracellular appendages behave a lot like p-type semiconductors. The electrical properties of S. oneidensis MR-1 have not been studied in detail.
The authors measured the conductivity of the materials, as well as the energy losses in a frequency range from 1 hertz to 1.5 terahertz for temperatures from -260 to 40 degrees Celsius. Next, the researchers measured the direct current conductivity of EMF for temperatures from zero to 40 C, as well as the temperature dependence of their heat capacity. For each of the three materials, water content and ion concentration were also determined.
In order to do this, the research pressed the substances into pellets using a 1-centimeter mold. They then applied electrodes to the faces of the pellets to pass an alternating current through them in order to measure the electrical conductivity and dielectric permittivity of the material in the 1-300 million hertz range. For higher frequencies, the approach doesn’t work. So for the 30-1,500 gigahertz, or billion hertz, range, the team obtained the spectra of complex dielectric permittivity using quasi-optical terahertz spectroscopy. No measurements were made in the intermediate frequency range.
At room temperature, EMF conductivity is nearly constant. When the frequency is increased above several million hertz, the conductivity is proportional to a certain power of the frequency. Cytochrome C didn’t exhibit this behavior unless the frequency was low and the temperature high. In the case of albumin, it was not observed at all. This suggests that different conductivity mechanisms are at play in the materials. It is likely that EMF has nearly free charges at room temperature, whereas albumin doesn’t have them and cytochrome C is a mixed bag.
The dependence observed by the researchers can be explained in terms of the individual properties of the materials. Both cytochrome C and albumin are regular proteins. Even though these materials do have some free charges, these are not nearly as many as it would be necessary to justify the Drude model. Comparing the conductivity in EMF to that in metals is more realistic because free charges are more easily generated in the molecules. But a comparison even more valid would be that with a solution of table salt, which has a high concentration of free ions.
Naturally, a complete description is more complex and would require us to take the water content of materials and other factors into account. Because EMF contains significant amounts of loosely bound water, its conductivity grows quadratically at temperatures of around -250 C and frequencies on the order of 100 billion Hertz. Temperatures that low cause the bulk water in the material to freeze, and high frequencies mean that the dielectric properties resulting from water dipole dynamics become non-negligible. The other materials exhibit deviations from Jonscher’s predictions, but they are not as dramatic.
The authors have clearly shown the powerful methodology and instrumentation of condensed matter physics to be effective for fundamental research into the electrodynamics of biological objects. The next step could involve the application of biomaterials research of the wide range of other theories and models that have been effectively used by the physics community for many years.
The research was published in Scientific Reports.