ENERGY MIGRATION

AND ITS ROLE IN BIOLOGICAL PROCESSES

N. V. Riehl

One of the most interesting problems of modern science is the elucidation of the essence of life processes.

The difficulty of this problem is often explained by the complexity of biological phenomena. Undoubtedly, the exceptional complexity of biological objects is one of the obstacles preventing an exhaustive analysis of their structure and their behavior. It would, however, be entirely wrong to identify this complexity with a disorderliness of the physicochemical processes taking place in a living organism. On the contrary, every biological phenomenon—for example, the strict reproducibility of one cell from another—points to the exceptional orderliness of the processes that underlie life, an orderliness that we encounter only very rarely in inanimate nature. In striving to understand the peculiarities of the phenomenon of life on the basis of physics and chemistry, we must therefore turn first of all to those phenomena of physics that consist in a strictly ordered interaction among the atoms participating in the given process. We must direct our attention to those physical processes that do not lead to a substantial increase in disorder.

Every phenomenon of nature, both inanimate and living, is associated with the transfer or displacement of energy. In the overwhelming majority of cases, the transfer of energy is associated with the scattering, with the “dissipation,” of the latter. Thus, the energy liberated in chemical reactions is usually released in the form of heat, i.e. it is distributed over all degrees of freedom of the surrounding atoms. The same thing usually occurs when a light quantum is absorbed. Its energy is transformed into the energy of thermal motion of atoms; the disorder of the system increases, entropy grows. Phenomena of this kind are of little use for understanding the distinctive features of life processes. They are suitable for describing the majority of phenomena of inanimate nature, for describing the processes occurring in the corpse of an animal, but not for describing the behavior of a living organism. A living organism preserves, despite the multitude and complexity of the processes occurring in it,

reactions and transformations, the structural character inherent in it, and the strict regularity and reproducibility of the processes occurring in it. Thus, in order to understand the characteristic features of vital processes, we must assume that the transfer of energy in reactions occurring in the organism takes place in a considerably more ordered fashion than in dead nature, and that mechanisms operate here which prevent the rapid dissipation of energy. Hence the question arises: are there processes known in physics in which the transfer of energy occurs without any substantial dissipation of that energy?

We can answer this question in the affirmative.

In certain areas of physics, phenomena of energy migration have been discovered, which consist in the fact that, under certain conditions, quanta of energy can move through matter over large distances without the participation of the ordinary mechanism of energy transfer by radiation or by diffusing atoms and molecules; moreover, each quantum moves as a whole, i.e. the energy of a given quantum does not undergo any substantial gradual dissipation along its path. “Migration” of energy, in the sense meant here, occurs spontaneously, i.e. it is determined only by the structure of the given substance and does not require auxiliary external influences, such as the presence of external electric fields, etc. Energy migration is also characterized by the fact that energy passes from the initial point not to just any of the surrounding atoms, but to definite atoms (or groups of atoms), which serve, so to speak, as “receivers” of the energy. The absence (or rather, the limitation) of energy dissipation (despite the length of the path traversed) and the presence of a certain “regularity”—these are precisely the characteristic features of energy migration that make it of interest for interpreting the peculiarities of vital processes.

SOME EXAMPLES OF ENERGY MIGRATION IN DEAD NATURE

Let us now turn to the physical aspect of energy migration. Let us first consider the fundamental approach of modern physics to the problem of the transfer of energy from one atom to another atom separated from it. As is known, in quantum mechanics a strict localization of energy is incompatible with the assumption of a definite value of the energy. If we are dealing, for example, with the absorption of light in a homogeneous crystal, then from the point of view of quantum mechanics it is meaningless to assert that a quantum has been absorbed by precisely this atom of the crystal and not by another. Consequently, when we have before us a crystal consisting of perfectly homogeneous atoms, we have no possibility either of experimentally proving the existence of energy migration or of denying its existence. The situation becomes different in the case when the atoms composing the given object are not homogeneous. Let us imagine that the object contains two kinds of atoms: \(A\) and \(B\). In such a

in this case we can choose the wavelength of the quantum absorbed only by atoms \(A\), and assert that the quantum has been absorbed precisely by only one of the atoms of species \(A\). If it turns out that the energy absorbed at one of the atoms \(A\) produces some action (for example, a chemical transformation or luminescence) at one of the atoms of species \(B\), then we can assert that the energy of the quantum has moved from atom \(A\) to this \(B\). Having information on the arrangement of these unlike atoms in space, we can also draw conclusions about the distances over which the energy of the quantum has moved.

In formations of this kind (in particular, in luminescent substances, in crystals containing foreign atoms, and in certain macromolecules) it has in fact proved possible to demonstrate experimentally the existence of energy migration. It turned out, moreover, that migration can occur over very considerable distances, exceeding by up to a million times the distance between two neighboring atoms. Such a result is somewhat unexpected, since at first sight one might have expected that an energy of several electron-volts should undergo rapid dissipation in the condensed phases under consideration (in which atoms undergo about \(10^{15}\) collisions per second). Indeed, in most cases such dissipation does occur: usually the absorption of a quantum leads to a rapid conversion of its energy into heat. Only under certain conditions is a substance capable of conducting quanta of energy over large distances without substantial dissipation.

The idea of energy transfer over distances exceeding the usual sphere of interaction between atoms was expressed already about twenty years ago in connection with the dependence, established by Perrin, Vavilov, and others, of the yield, polarization, and quenching of fluorescence in solutions on their concentration (and on the nature of the “quenching” foreign molecules). This idea was applied by Vavilov to the quantitative interpretation of experimental results. He introduced the concept of the “sphere of action of impacts of the second kind,” i.e. the sphere of action within which atoms are capable of transferring to one another (without the participation of radiation) quanta of excitation energy[^1]. Vavilov’s experiments showed that sometimes the “sphere of action of impacts of the second kind” substantially exceeds the ordinary, “kinetic” sphere of action of atoms. The unexpectedly large size of the “sphere of action of impacts of the second kind” is evidently explained here by the resonant character of the interaction between the fluorescing and the quenching molecules.

Frenkel[^2] put forward the hypothesis according to which an excited state arising in a crystal as a result of the absorption of a light quantum can move in the crystal, being transferred from one atom to another. An excited state of this kind, “wandering” through the crystal, was called by Frenkel an “exciton.”

The bimolecular law of decay of phosphors, theoretically substantiated by Blokhintsev[^3] and experimentally proved by Antono-

MIGRATION OF ENERGY AND ITS ROLE IN BIOLOGICAL PROCESSES

... by Romanovskii^4, Levshin^5, and others^6, also indicates that the excited state (and, correspondingly, the electron excited in the crystal) is not strictly localized in the crystal lattice.

The presence of some kind of long-range energetic interaction is also indicated by certain features in the absorption spectra of carbon chains with conjugated bonds, i.e. with alternating double and single bonds between carbon atoms ($-\mathrm{C}=\mathrm{C}-\mathrm{C}=\mathrm{C}-\mathrm{C}=\mathrm{C}-$).

The existence of energy migration was experimentally proved by the author in the study of the excitation of luminescent crystals^7. The first convincing results were obtained upon excitation by $\alpha$-rays of zinc sulfide crystals containing traces of copper as an “activator.” Let us consider these results in greater detail.

The emission spectrum of luminescent zinc sulfide (and of many other “crystal phosphors”) is determined primarily by the nature of the “activator.” The emitting system, consequently, is not the principal substance of the crystal, but the impurity atoms—the activator. We may then pose the question: does the process of excitation (i.e. the absorption of the exciting energy) also take place only in the impurity atoms, or at any place in the crystal lattice, i.e. in the principal substance of the given crystal? An especially convincing answer to this question was obtained in the study of the excitation of crystals by $\alpha$-rays. Our investigations showed that, upon excitation by $\alpha$-rays of, for example, zinc sulfide containing an impurity of $1/100\%$ copper, the kinetic energy of the exciting $\alpha$-particles is almost completely converted into light emitted by the crystal*). On the other hand, we know that an $\alpha$-particle, passing through the crystal lattice, is slowed not only by the few copper atoms scattered through the lattice, but that every zinc or sulfur atom lying along the path of the $\alpha$-particle takes a certain part in its retardation and thus receives some part of its energy. Since, however, the energy of the $\alpha$-particle, as stated above, is almost completely converted into light energy, we may conclude that the energy received from the $\alpha$-particle by any zinc or sulfur atom is transferred in some way to that atom which is capable of emitting light, i.e. to the copper atom. In other words: the process of absorption of the exciting energy takes place not only in the few atoms of the “activator” (i.e. in copper atoms), but every zinc or sulfur atom in the given lattice is capable of receiving the exciting energy and transmitting it without loss to the emitting system, i.e. to the copper atom.

*) The highest “coefficient of efficiency” found by us in certain zinc sulfide preparations especially sensitive to $\alpha$-rays was $80\%$.

We arrive at the same conclusion also on the basis of facts found by us when exciting phosphorescent crystals with ultraviolet rays*). Experiments have shown that here, too, the conversion of the exciting ultraviolet quanta into emitted light quanta occurs almost without losses, i.e., for each ultraviolet quantum absorbed by the crystal one light quantum is emitted (“quantum efficiency” coefficient \(\sim 100\%\)). On the other hand, it was established that the absorption of the ultraviolet rays used by us occurs not only in the atoms of the above-mentioned foreign impurity (for example, copper), but at any point of the crystal lattice, i.e., in any atom of zinc (cadmium) or sulfur. We may therefore conclude that the energy of the “exciting” quanta incident on the crystal is initially received by the main substance of the crystal and only thereafter is transferred to the impurity atoms capable of emitting light.

If one takes into account that, for example, in zinc sulfide with a copper impurity there are not fewer than 10,000 zinc (or sulfur) atoms for each copper atom, then around each copper atom one may imagine a cube of zinc sulfide, each edge of which, along its length, corresponds to more than 20 interatomic distances. Since the energy absorbed at any point of this cube is transferred, with probability equal to unity, to the copper atom, it follows from this that energy quanta are capable of moving in the crystal without dissipation over distances equal to at least 20 interatomic distances.

THEORETICAL CONCEPTION OF THE MECHANISM OF ENERGY MIGRATION IN LUMINESCENT CRYSTALS

We shall not dwell on the numerous other facts and observations proving the existence of energy migration in crystals, organic macromolecules, and other formations**), and shall attempt to outline (using luminescent crystals as an example) a theoretical picture of energy migration. Let us note that this picture is valid only for the above-mentioned luminescent crystals. It by no means embraces all possible kinds of energy migration. For what follows, however, it is especially appropriate, since it connects the displacement of energy with the displacement of electrons; we shall see below, when considering energy migration in proteins, that in these formations, of particular interest to the biologist, energy transfer is also connected with the transfer of electrons. Therefore we—

*) These observations were made mainly on mixed crystals of zinc and cadmium sulfide with an impurity of copper or silver.

**) All these facts are set forth in detail in the author’s book now in press, Energy Migration—a New Type of Energy Transfer in Dead and Living Nature.

we use in discussing energy migration in proteins the same theoretical picture, without, of course, losing sight of the fact that this picture is applicable to proteins by no means in all respects.

The explanation of energy migration in luminescent crystals is based on the scheme of the energy structure of crystals given by quantum mechanics. In principle, it is based on the fact that the outer electrons of atoms located in a crystal cannot be assigned to one or another definite atom of the lattice, but belong, to a certain degree, to the entire crystal as a whole. Let us consider, with the aid of Fig. 1, those energy conditions which make energy migration possible.

In the formation of a crystal, i.e., when the \(n\) atoms constituting it come together, each quantum energy level splits into \(2n\) levels very close to one another. All these levels constitute an almost continuous group of levels—the so-called energy “band.” These bands, belonging to the entire crystal, replace the energy levels of individual atoms. The electrons present in the crystal are distributed among the individual levels constituting the bands, and some of the levels may remain unoccupied. Depending on the character of the distribution of electrons among the levels, the crystal is either a conductor or an insulator. In insulators there exist only such bands as are either completely occupied by electrons or contain none at all*).

In Fig. 1 the band \(B\) (as well as all the bands lying below it) is completely occupied by electrons, whereas the band \(A\) (the “conduction band”) contains none of them at all. The bands lying higher have a greater width than the bands situated lower. The width of a given band is a measure of the exchange interaction of electrons between neighboring atoms. The wider the band, the less the electrons located in it belong to one or another definite atom, i.e., the more they represent a “collective property” of the entire crystal as a whole.

If such an ideal crystal absorbs a quantum and, as a result of this, one of the electrons passes from the occupied band \(B\) into the unoccupied band \(A\), then, for reasons following from quantum mechanics,

*) It is not difficult to understand that, with such a distribution of electrons, the crystal possesses no conductivity. A crystal can be a conductor only when at least some of its electrons can come into motion, i.e., increase their energy under the influence of an electric field. An increase of energy, however, is the transition of the given electron from one level of the band to the next, higher-lying level of the same band. If the higher-lying levels are already occupied by other electrons, then the electron in question cannot move from one level to another, and, consequently, conductivity cannot occur. In contrast to this, in metals there exist bands not completely occupied by electrons, and therefore here there is the possibility of an electron’s transition from one level to other, higher-lying and unoccupied levels of the same band.

connected with the luminescence of the reverse transition of this electron into band \(B\), should not be expected. “Luminous” transitions can occur only between a band and some separate additional level, not belonging

Fig. 1. Energy scheme of a luminescent crystal with a scheme of the process of excitation and luminescence.
1 — excitation upon absorption of a quantum (an electron is raised from the occupied band \(B\) into the unoccupied band \(A\)); 2 — the free place formed in band \(B\) is filled by an electron from level \(C\); 3 — as a result of energetic interaction with the surrounding electrons, the electron that has entered band \(A\) descends to the lower boundary of this band; 4 — luminescence (the electron falls from band \(A\) to level \(C\), which has been freed as a result of process 2).

to any of the bands, located somewhere between the bands. Such local additional levels occur precisely in those crystals which contain foreign impurities, i.e., in the luminescent crystals that are of interest to us in particular,

... crystals containing an “activator” impurity. In the cases considered by us, the additional levels situated near the free band \(A\) contain no electrons, whereas each level lying near the filled band \(B\) is occupied by an electron. On the basis of this energy scheme we obtain the following picture for the mechanism of energy migration.\(^{8}\)

When a quantum is absorbed in the fundamental lattice of the crystal, one of the electrons of the occupied band \(B\) passes into the unoccupied band \(A\), where, giving up the excess of its energy to the surrounding particles, it immediately drops to the lower edge of this band. The vacant place left in band \(B\) is filled by one of the electrons lying near band \(B\) on the additional levels \(C\) (“impurity levels”). Since the outer electrons do not belong wholly to one or another definite atom, and neighboring atoms exchange their electrons, the vacant place in band \(B\) also diffuses from one atom to another. It is therefore not difficult to imagine that this vacant place will collide with one of the local impurity levels \(C\) scattered through the crystal. The emission of light occurs when an electron passes from band \(A\) to the now-vacant level \(C\). In this way the initial state is again restored.

This representation makes it possible to understand many facts that have so far been found in the field of luminescence of inorganic crystals. The migration of energy that interests us here can also be easily understood on the basis of this picture: as a consequence of absorption of a quantum, the electron enters the conduction band \(A\) (for this reason the crystal also becomes electrically conducting under irradiation); in the conduction band the electron can move without hindrance over large distances and, upon reaching the place where the freed impurity level \(C\) is located, pass to this latter level while emitting light. Emission may thus occur at places situated very far from the place where the exciting quantum was absorbed. In this way we can explain not only the fact of energy migration as such, but also the fact that the energy migrates not just anywhere, but precisely to where the impurity atom and the “impurity level” (“distortion level”) associated with it are located.

This type of energy migration we call electronic migration of energy.

ENERGY MIGRATION AND BIOLOGICAL PROCESSES

As has already been said above, in this brief review article we do not intend to dwell on all the observations and facts—some of them very interesting—that point to the action of energy migration.*) We believe that the greatest interest of energy migration

*) The reader will find a detailed exposition of all this material in the monograph, already mentioned above, which is in press.

is applicable to biological, in particular biocatalytic processes. The author therefore devoted special attention to elucidating the role of energy migration in biology. Let us turn to an exposition of the material that has so far been found in this direction.

More than ten years ago, certain observations were made in biology whose interpretation can be given on the basis of the concept of energy migration. One of these observations was made by Timofeeff-Ressovsky, Zimmer, and Delbrück[^9] in the study of mutations of the fly Drosophila induced by radiation.

The experiments of these authors showed that a mutation is caused by a change in the state of a single atom (or, at least, of a few mutually connected atoms) in the chromosome. When the chromosome is irradiated with ionizing rays (for example, X-rays), a single act of ionization (i.e., the formation of one pair of ions) can consequently cause mutation of the entire organism. The investigators mentioned further came to the conclusion that the so-called “target region,” i.e., the region of space in which ionization must occur in order to bring about a mutation, has a volume several orders of magnitude larger than the volume of one atom or of a group of several atoms. This result can be interpreted only on the basis of the assumption that the energy absorbed at the site of primary ionization is somehow transferred to that atom whose change of state leads to mutation. Here, just as in luminescent crystals, we are forced to recognize the necessity of energy migration over large distances. The difference in comparison with observations on the dead objects considered above consists only in the fact that there we dealt with matter of comparatively simple and well-investigated structure, whereas in gene mutation we encounter an object whose physicochemical structure has as yet been studied very little. Attempts to explain the described results otherwise than by means of energy migration, however, lead to contradictions with the experimental data[^10].

Similar conclusions about the role of energy migration are also suggested by certain facts, established long ago, in the field of carbon-dioxide assimilation by plants. We shall return to this question below.

In both of the cases mentioned, we are dealing with complex biological objects whose physicochemical structure has as yet been little studied. The interpretation of the mechanism of energy transfer in these objects therefore at one time caused certain difficulties. The possibility was not excluded that the transfer of energy here occurs by means of the ordinary diffusion of some formed...

during the photoreaction of particles containing excess energy. A more detailed consideration of all the experimental data leads, it is true, to the opinion that the mechanism of energy transfer in these cases corresponds to what we call energy migration. But for a long time it nevertheless remained completely unclear what formations, what physicochemical structures or organic macromolecules in the indicated biological objects were responsible for energy migration, i.e., were the “conductors” of energy. The possibility of energy transfer by means of hydrocarbon chains with conjugated bonds was rejected, since it did not correspond to the chemical data. In physics there were not yet known such processes of radiationless transfer of quantum energy that could be accepted also for protein substance (or other formations essential for the organism). The question of the mechanism of energy transfer in both of the cases mentioned therefore remained open. Some investigators even disputed the very possibility of a phenomenon resembling “energy migration” in the fundamental substances of the living organism.

The situation became clear only after we succeeded in obtaining sufficiently convincing experimental material giving direct and immediate proof of the presence of energy migration in certain formations with a definite, physicochemically clear structure. These results showed the presence of energy transfer over exceptionally large distances, exceeding the distance between neighboring atoms by several orders of magnitude. They further showed that energy migration is inherent in formations very diverse in their physicochemical nature. Finally, they made possible the well-founded assumption that energy migration also exists in proteins11, an assumption which in the very last years has been directly proved by experiment. This last result is especially essential for interpreting biological processes on the basis of the concept of energy migration.

Let us turn to the investigations that led us to this result.

ENERGY MIGRATION

IN THE ENERGETICS OF PROTEINS AND ENZYMES

Proceeding from facts and considerations presented by the author, Szent-Györgyi12 pointed out a number of biochemical phenomena, at first sight inexplicable (especially in the field of enzymes), which can be interpreted with the aid of energy migration. Of particular interest is the following example given by Szent-Györgyi.

As is known, the molecules of certain oxidative enzymes (cytochrome a, cytochrome b, cytochrome c, etc.), participating in respiratory—

processes, are large protein molecules (“enzyme carriers”), with which an “active” heme group containing an iron atom is associated. The latter is capable of passing from the trivalent state to the divalent (and back), i.e., of being reduced and oxidized. It is further known that in a living cell the heme group of one enzyme is capable of transferring energy to the heme groups of other enzymes. Fixed in its place in the cellular substance, the enzyme molecule would therefore have to be situated so that its heme group came into contact with the heme groups of other enzyme molecules. It is possible to arrange two enzyme molecules in this way, but it is impossible to arrange a larger number of molecules in this way. The heme groups of different enzyme molecules are therefore located at a certain, relatively large distance from one another. Nevertheless, an energetic interaction exists between them. According to Szent-Györgyi, this fact, incomprehensible at first sight, can be interpreted if one assumes that individual molecules of different enzymes (or their heme groups) are connected with one another by energy bands passing through the entire structure; i.e., that here there exists the same action of energy at a distance as in luminescent crystals.

The presence of energy migration in oxidative enzymes is of particular interest because, as Riehl noted[^13], from this one may draw the conclusion that in the migration of energy in living tissue the conductor of energy is the protein substance itself as such, and that the mechanism of transfer corresponds to the electronic migration of energy. To convince ourselves of this, let us consider in more detail the processes mentioned above in oxidative enzymes.

It is impossible to imagine that the iron atoms are in immediate proximity to one another, because the heme groups containing them are fixed in the protein framework. The energy passing from one iron atom to another must therefore move over large distances, and the conductor of the energy must be the protein substance itself, since the heme groups between which energetic communication takes place are fixed on the protein, i.e., are connected with one another by protein.

Oxygen, taken up from the air by the iron-containing respiratory pigment, converts the iron from the divalent state (—“heme state”) to the trivalent state (—“heme state”). This change of valence is transmitted further from cytochrome a to cytochrome b, and from cytochrome b to cytochrome c, and is thus delivered gradually to the hydrogen of the substrate (or of some intermediate, iron-free enzyme).

Schematically, this process can be represented as follows*):

\[ \begin{aligned} &\tfrac{1}{2}O_2 \ldots\ldots + 2\mathrm{Fe}^{++} \left(\begin{array}{c} \text{resp.}\\[-2pt] \text{enzyme} \end{array}\right) = 2\mathrm{Fe}^{+++} \left(\begin{array}{c} \text{resp.}\\[-2pt] \text{enzyme} \end{array}\right) + O^{--} \\ &2\mathrm{Fe}^{+++} \left(\begin{array}{c} \text{resp.}\\[-2pt] \text{enzyme} \end{array}\right) + 2\mathrm{Fe}^{++} \left(\begin{array}{c} \text{cytochr.}\\[-2pt] a \end{array}\right) = 2\mathrm{Fe}^{++} \left(\begin{array}{c} \text{resp.}\\[-2pt] \text{enzyme} \end{array}\right) + 2\mathrm{Fe}^{+++} \left(\begin{array}{c} \text{cytochr.}\\[-2pt] a \end{array}\right) \\ &2\mathrm{Fe}^{+++} \left(\begin{array}{c} \text{cytochr.}\\[-2pt] a \end{array}\right) + 2\mathrm{Fe}^{++} \left(\begin{array}{c} \text{cytochr.}\\[-2pt] b \end{array}\right) = 2\mathrm{Fe}^{++} \left(\begin{array}{c} \text{cytochr.}\\[-2pt] a \end{array}\right) + 2\mathrm{Fe}^{+++} \left(\begin{array}{c} \text{cytochr.}\\[-2pt] b \end{array}\right) \\ &2\mathrm{Fe}^{+++} \left(\begin{array}{c} \text{cytochr.}\\[-2pt] b \end{array}\right) + 2\mathrm{Fe}^{++} \left(\begin{array}{c} \text{cytochr.}\\[-2pt] c \end{array}\right) = 2\mathrm{Fe}^{++} \left(\begin{array}{c} \text{cytochr.}\\[-2pt] b \end{array}\right) + 2\mathrm{Fe}^{+++} \left(\begin{array}{c} \text{cytochr.}\\[-2pt] c \end{array}\right) \\ &2\mathrm{Fe}^{+++} \left(\begin{array}{c} \text{cytochr.}\\[-2pt] c \end{array}\right) + H_2 \left(\text{substrate}\right) = 2\mathrm{Fe}^{++} \left(\begin{array}{c} \text{cytochr.}\\[-2pt] c \end{array}\right) + 2H^{+} \end{aligned} \]

\[ O^{--} + 2H^{+} = H_2O \]

From this scheme it is clear that we are dealing here not only with the transfer of energy, but also with the transfer of electric charge, i.e. with migration of energy coupled with the transfer of an electron. If one assumes that only energy is transferred here (and not the electron),

Fig. 2. Diagram of the action of hydrogenating and dehydrogenating enzymes on the basis of electron migration through protein.

then such a conception proves inconsistent with biochemical facts. On the basis of experimental data we have here, without doubt, a successive change in the valence of iron atoms, i.e. the transition of an electron from the iron atom of one cytochrome to the iron atom of another cytochrome. (This transfer of electric charge is compensated by the fact that, at the place left by the electron, one \(H^+\) ion is given up from the adjacent aqueous phase, while at the place to which the electron arrives, one \(H^+\) ion is absorbed from the aqueous phase.)

Fig. 2 gives a schematic picture of the processes occurring here. In the figure the electrons move from right to left. First one

) From the book by L. v. Bertalanffy, Theoretische Biologie*, II.

the electron passes from the respiratory enzyme to the oxygen atom and converts it into an oxygen ion. This electron is followed by an electron from cytochrome a; it occupies the place vacated in the respiratory enzyme and, in so doing, descends to a lower energy level. The same thing is repeated between cytochromes b and a, and so on. In the final result it is as though one and the same electron, falling to ever lower energy levels, moves from one cytochrome to another, in order ultimately to pass to the oxygen atom and convert it into an ion. Thus the large heat of reaction of detonating gas is released not all at once, but gradually, in separate small portions, so that nowhere is there a sudden release of an excessive, harmful amount of heat. These separate small portions of energy can be used for the biochemical reactions necessary to the life of the cell. This kind of subdivision of the available energy constitutes, as is known, an important and characteristic feature of oxidative processes in the living cell.

Thus, the migration of energy in oxidative enzymes must be electronic, and the conductor of the energy must be the protein substance (the polypeptide chain). The processes taking place here are closely related to the processes we have found in luminescent crystals.

In view of the special significance of protein substance for vital processes, questions of energy migration in proteins were subjected to special study, and a number of other arguments were found in favor of the ability of proteins to serve as conductors of quantum energy1.

Recently T. Bücher set himself the task of testing, by an experimentum crucis, the correctness of this hypothesis. He succeeded in finding direct, immediate experimental proof of its validity.

We shall briefly set forth these results of Bücher’s experiments.

As is known, hemoglobin (and also other hemin-containing protein substances) forms compounds with carbon monoxide. Each hemin group binds one molecule of CO. Hemoglobin, for example, contains 4 hemin groups (because it consists of 4 Svedberg nuclei, each of which contains one hemin group); each molecule of hemoglobin therefore binds 4 molecules of CO. Myoglobin (whose molecular weight is 17,000, so that it must consist of only one Svedberg nucleus) accordingly has only one molecule of CO per molecule. Carbon monoxide is split off from hemoglobin, myoglobin, etc. by light.* In all experiments carried out up to now on such

of the kind of splitting, light from that part of the spectrum was used which is absorbed by the hemin group (or by the hemin–CO complex). In contrast to this, Bücher set himself the task of testing whether cleavage would occur also in the case where, upon irradiation, a wavelength is used that is absorbed not by the hemin, but only by the protein.

If the hypothesis of energy migration through the protein substance corresponds to reality, then the splitting of the hemin–CO compound should occur also in the case when the quantum is absorbed not in the hemin group itself, but somewhere in the protein substance (i.e., somewhere in the protein part of the hemoglobin or myoglobin molecule).

The result of the experiment fully confirmed this prediction. The object of Bücher’s experiment was the CO–myoglobin compound. Bücher irradiated this compound with ultraviolet rays corresponding to the absorption region of the protein (for example 2537 Å), and obtained just as strong a cleavage of CO from myoglobin as when irradiating it with light of the wavelength that is absorbed by the hemin itself. Even the quantum yield proved to be exactly the same as upon irradiation in the absorption region of the hemin. Bücher carried out a series of very precise measurements, using different wavelengths both in the protein absorption region and in the hemin absorption region, and in every case obtained a quantum yield practically equal to unity. Thus, for the photochemical reaction of CO cleavage from hemin it proves to be entirely immaterial whether absorption of the quantum takes place in the CO–hemin complex itself or somewhere in the protein molecule. The quantum energy is transported without any losses through the entire large protein molecule to the hemin group*).

These experiments provide direct proof of the ability of protein to conduct quantum energy.

MODEL OF THE ACTION OF OXIDIZING AND REDUCING ENZYMES AS A CONSEQUENCE OF ENERGY MIGRATION

The facts and considerations set forth above lead us to a model of the mechanism of action of all enzymes capable of acting oxidatively or reductively, such as: enzymes containing iron and copper, “yellow enzymes,” pyridino-dehydrase and various “redoxases” of unknown structure (Fig. 3). A denotes the hydrogen donor, and B the hydrogen acceptor. Donor A may be the substrate, and acceptor B the active group of the enzyme molecule, or, on—

*) It should be noted here the results of the investigations of Norrish (Acta Physicochim. URSS 3, 171, 1935), who showed (on simpler organic molecules) that in certain cases light is absorbed in one part of an organic molecule, while another part, located at a considerable distance from the first, is cleaved off.

turn, the active group serves as donor A, and the substrate as acceptor B; or, finally (in intermediate enzymes of the cytochrome type), both A and B are active groups (for example, heme groups). As is known, the reaction of hydrogen transfer from A to B proceeds according to the following reaction equations:

\[ \begin{aligned} \mathrm{AH} &= \mathrm{A}^{-}+\mathrm{H}^{+}\\ \mathrm{A}^{-}+\mathrm{B} &= \mathrm{A}+\mathrm{B}^{-}\\ \mathrm{B}^{-}+\mathrm{H}^{+} &= \mathrm{BH} \end{aligned} \]

\[ \text{In all: }\mathrm{AH}+\mathrm{B}=\mathrm{A}+\mathrm{BH} \]

Fig. 3 shows how one should imagine the interaction between donor A and acceptor B with the participation of electron energy migration. The donor A gives up an ion \(\mathrm{H}^{+}\) to the adjacent aqueous phase; the remaining electron passes through the “conduction band” of the protein (the “carrier enzyme”) to acceptor B; the acceptor captures from the adjacent aqueous phase one of the \(\mathrm{H}^{+}\) ions present in it. This process of hydrogen transfer is thereby completed. Ultimately the electrical balance is restored, and the hydrogen atom (although not individually the very same one) has been transferred from A to B.

In the figure: “aqueous phase,” “protein,” \(A\), \(B\), \(e^{-}\), \(\mathrm{H}^{+}\).

Fig. 3. Scheme of energy migration and electron displacement in oxidative enzymes of aerobic cells.

The most interesting and important feature of our model is the circumstance that donor A and acceptor B react with one another at a distance! The protein here serves as a transmitter (conductor) of electrons, whereas the adjacent aqueous phase accepts from the donor an ion \(\mathrm{H}^{+}\) and supplies the acceptor with another ion \(\mathrm{H}^{+}\) in its place. We encounter here a situation entirely new for chemistry—two molecules can react with one another at a distance.

From our model there follows yet another interesting consequence in the field of catalysis. If, owing to the conductivity of the protein for electrons, reactions between atoms remote from one another become possible, then, one may ask, is it not possible to obtain the same result by replacing the protein with some electron-conducting substance, for example a metal. Indeed, as has long been known, colloid-

…solutions (sols) of metals exhibit considerable catalytic activity (“metal-enzymes,” Bredig’s “inorganic enzymes”). Thus we can also understand the mode of action of inorganic enzymes. There is every reason to suppose that here the same mechanism of the catalytic reaction is operative as in the enzymes considered above, with the only difference that in inorganic enzymes the conductor of electrons is not the conduction band of a protein, but the conduction band of a metal. (Here the donor or acceptor of hydrogen is probably the metal itself.)

The model of enzyme action set forth above also explains the role, hitherto unclear, of the protein enzyme-carrier. Owing to the ability of a protein to conduct electrons (and at the same time to combine specifically with various biologically important molecules), the protein enzyme-carrier serves as an intermediary for reactions between atoms and molecules remote from one another.

Our conception is in good agreement with the fact, established in some cases, that for the substrate on which an enzyme acts, the specific group is not the active (prosthetic) group, but the protein enzyme-carrier. This means that the substrate binds not to the active group, but to the protein part of the enzyme molecule. (This fact has been proved, in particular, precisely for certain dehydrogenases.) It follows from this that the hydrogen donor (substrate) and the hydrogen acceptor (active group) are not fastened directly to one another, but are located (on the surface of the protein) at some distance from one another. Nevertheless an exchange of hydrogen occurs between them. This can be understood only on the basis of the model proposed above (see Fig. 3).

An interesting parallel to the facts and ideas set forth above is provided by the results recently obtained by Schwab^15.

He experimentally investigated the dependence of the activation energy in the catalytic decomposition of gaseous formic acid by metal alloys on the composition of the alloy. (The activation energy \(q\) is, as is known, the only reliable measure of the catalytic effectiveness of a catalyst. It is obtained from the van ’t Hoff–Arrhenius formula \(K = K_0 \cdot e^{-q/RT}\), on the basis of the dependence of the reaction constant \(K\) on temperature. The smaller \(q\) is, the greater the catalytic action of the catalyst.) Schwab found that the activation energy increases in parallel with the “electron concentration” according to Hume-Rothery, i.e., the ratio of the number of valence electrons to the number of atoms. Schwab further refers to Hume-Rothery’s quantum-mechanical interpretation of the “electron concentration”^16 and indicates that the catalytic activity of an alloy-catalyst is determined by the degree to which the Brillouin zone is filled with electrons. The activation energy rises (i.e., the catalytic activity decreases) as the Fermi distribution approaches the boundary of the Brillouin zone. Thus, Schwab concludes,

the catalytic activation of formic acid consists in the removal of electrons from it by the alloy catalyst. The transfer of electrons from formic acid to the alloy catalyst requires the less energy (“activation energy”), the less the metal (alloy) is already saturated with electrons. (The protons formed in this process probably pass into the interatomic space of the metal, while the electrons merge with the electron gas of the metal.) Thus, we see that here too the catalytic action consists in the absorption (and transfer) by the catalyst of the substrate’s electrons.

ENERGY MODEL OF THE ACTION OF HYDROLASES ON THE BASIS OF ENERGY MIGRATION

Up to now we have spoken only of the so-called redoxases, i.e. enzymes capable of acting on a substrate either oxidatively or reductively. Alongside these enzymes, there also act in the organism the so-called hydrolases, i.e. enzymes capable of cleaving certain bonds in molecules of substances essential for the organism (for example, carbohydrates and proteins). In the cleavage (“hydrolysis”) of proteins, i.e. polypeptide chains, the enzyme cleaves the bond —OC—NH— between two adjacent amino acids, and, at the expense of one molecule of water, the groups COOH and H₂N are formed. (According to A. I. Oparin, these same enzymes are capable, under certain conditions, of producing the reverse, synthetic action, i.e., for example, of joining amino acid molecules into a polypeptide chain, with not absorption but, on the contrary, release of one molecule of water.) Let us consider whether our ideas, based on electronic energy migration in proteins, are applicable to enzymes of this group.

In considering oxidizing and reducing enzymes (dehydrases, redoxases) we saw that the meeting of an H⁺ ion with an electron at the acceptor leads to the overcoming of the activation energy required to create a bond between the hydrogen atom and the acceptor, as a result of which hydrogenation of the acceptor occurs. In the hydrolytic cleavage of chemical bonds, for example the —CO—NH— bond, the H atom joins the NH group and the OH radical joins the CO group. By analogy, one may adopt for these two processes the same mechanism that we adopted for the formation of a bond between the H atom and the acceptor in redoxases. In other words: we may suppose that the formation of a bond between H and NH is based on the meeting, at NH, of an H⁺ ion from the adjacent aqueous phase with an electron supplied by the protein, and that the formation of a bond between OH and CO is based, analogously, on the supply of an OH⁻ ion from the aqueous phase and the splitting off of an electron which is transferred to the protein. We thus obtain a large

similarity to the process occurring in reductases according to our model. The question remains open whence comes the electron supplied by the protein to the H+ ion, and where goes the electron given up by the OH ion to the protein. Moreover, the question arises as to what part is played in the process by the so-called “active” or “prosthetic” group of the enzyme. As is known, interaction is inherent in (in very many, and perhaps in all, cases) the aggregate of the protein “enzyme-carrier” and the prosthetic group.

The author has attempted to outline a picture of the action of splitting and synthesizing enzymes (hydrolases) on the basis of electronic energy migration. This attempt leads to rather concrete and simple ideas about the role of the prosthetic group, about the mechanism of the synthesizing action of enzymes in the living organism, and about the connection between assimilatory and dissimilatory processes. These ideas agree so well with the main experimental facts that the author has ventured to publish his considerations.* Here we shall confine ourselves to a brief exposition of the main features of our scheme. The reader will find a detailed substantiation of the scheme and an exposition of the consequences following from it in the monograph cited above.

In considering the migration of energy in reductases we saw that, owing to the capacity of the protein enzyme-carrier to transmit energy, energetic (and even electronic) interaction of atomic groups remote from one another, but connected with one and the same enzyme-carrier, becomes possible. In the field of hydrolyzing ferments (hydrolases) there also exist facts indicating that here too there is some action at a distance, and that the substrate is bound not with the prosthetic group itself, but with some other site of the enzyme molecule (i.e., with the enzyme-carrier). We shall not examine these facts here (they are set forth in detail in the monograph), and shall confine ourselves to pointing out that from them one may draw the following résumé. In the enzyme molecule there exist at least two points that play a decisive role in enzyme action: one point, which binds the substrate, and another (somewhat removed from the first) point, the electron-energy state of which exerts a decisive influence on the splitting activity of the enzyme; the removal from this latter point (or association with it) of a hydrogen ion or of a “poisoning” metal determines with what probability the cleavage of the substrate bound to the first point will occur. As is known, many facts indicate that the nature of the enzyme-carrier determines the specificity of the enzyme with respect to the substrate, while the chemical character of the prostheti—

* See the monograph mentioned above.

…of the chemical group determines specificity with respect to the cleavage of a definite chemical bond. Therefore it may be considered probable that the point binding the substrate is located precisely in the protein—enzyme carrier, while the point effecting the cleavage itself and subject to the action of activating or inhibiting agents may be identified with the prosthetic group (or with some part of it).

The question arises as to how the prosthetic group can act on a substrate that is not bound to it directly, but is situated at some (perhaps even considerable) distance from it. Clearly, one should try to answer this question by means of the concept of electronic migration of energy. The strongly expressed dependence of the cleaving activity on the electron-energy state of the group responsible for cleavage (i.e. the prosthetic group) already suggests that here we are dealing with some kind of electron transfer.

In order to answer the question posed, let us return to the conception proposed above. In the example of the cleavage of the peptide bond \((-\mathrm{CO}-\mathrm{NH}-)\), it was stated there that, during cleavage, an H atom becomes joined to the \(\mathrm{NH}\) group, while an \(\mathrm{OH}\) radical becomes joined to the \(\mathrm{CO}\) group; moreover, the H atom arises as a result of the discharge of an \(\mathrm{H}^+\) ion arriving from the aqueous phase, and the \(\mathrm{OH}\) radical arises analogously, by discharge of an \(\mathrm{OH}^-\) ion arriving from the aqueous phase. \(\mathrm{H}^+\) accepts an electron from the protein, while \(\mathrm{OH}^-\) gives an electron to the protein. The protein thus facilitates the transfer of an electron from \(\mathrm{OH}^-\) to \(\mathrm{H}^+\). This function of the protein is equivalent to a lowering of the activation energy required for electron transfer. In other words: if electron transfer occurs through the mediation of the protein, the electron does not encounter those obstacles (energy barriers) that impede its transfer in the absence of the protein. Let us consider the energy aspect of this transfer. As already stated, there are no substantial energy barriers for electron transfer through the protein, because the presence of catalytic action consists precisely in the fact that the activation energy of the process is reduced to the order of \(kT\). But since the overall energy balance of the cleavage reaction is positive (of the order of several kilocalories per mole), the electron must somewhere on its path from \(\mathrm{OH}^-\) to \(\mathrm{H}^+\) descend from one energy level to another, lower one. Somewhere in the enzyme molecule the electron therefore passes through some system (atomic group) that can exist in two different energy states. The circumstances mentioned above give grounds for the supposition that such a system is the prosthetic group.

Thus the following picture of the entire process is obtained: the electron from \(\mathrm{OH}^-\) migrates along one of the energy levels of the protein

to the prosthetic group, there descends to a lower level and then migrates (again through the protein) to H+. (For the sake of clarity, all functions are here ascribed to one and the same electron, and not to the resonance interaction of different electrons.)

According to this conception, the principal energetic “jump” of the electron takes place in the prosthetic group. It becomes clear why it is precisely the prosthetic group that determines the specificity with respect to the bond being split: the difference between the two energy states in the prosthetic group must coincide with the energy liberated upon the cleavage of the given bond.

ENERGY MIGRATION

AND SYNTHETIC PROCESSES IN THE ORGANISM

Up to now we have considered only the cleavage of bonds. According to all available data, the same enzymes can also act synthetically; however, their synthesizing action takes place only under definite chemical, morphological, and energetic conditions. According to Oparin, hydrolases occur in the organism in two different states. Some hydrolases are in a dissolved state, in which they produce only hydrolysis (i.e., not synthesis); in this state they remain after destruction of the cell and can be studied in vitro. Another part of the enzymes is bound, according to Oparin, with mitotic heterogeneous structures (for example, mitochondria); this part is responsible for the synthetic action. The synthesizing action of an enzyme takes place only when the enzyme is coupled with some structures of the cell, i.e., with certain other proteins, enzymes, or other constituent parts of the cell. In addition, much indicates that a further prerequisite for biosynthesis is the supply of the necessary energy. In the cell, energy is developed through the action of respiratory processes, i.e., through the action of reductases. Let us consider whether the model of the action of hydrolases proposed above makes it possible to imagine a coordinated action of reductases with hydrolases, such that the energy obtained as a result of the action of reductases (i.e., respiratory processes) could be used by hydrolases for synthetic processes. This coordination should give us the possibility of understanding the inversion of the action of enzymes in the cell, i.e., the transformation of the cleaving action of hydrolases into a synthesizing one. It is not difficult to see that in this transformation the two different energy states (energy levels) in the prosthetic group, of which we spoke above, must play a role; moreover, during synthesis the electron must not fall from the upper level to the lower one, but, on the contrary, rise from the lower level to the upper one. Such a transition of the electron is, of course, connected with the supply of energy. On the basis of the scheme of enzyme action proposed above, it is easy to understand that when the electron passes from the lower

on the upper level an effect opposite to cleavage will be obtained, i.e. synthesis. There will occur the splitting off of the ion H+ and the ion OH−, which pass into the aqueous phase, while a peptide bond will be formed between the remaining NH and CO groups.

How is one to picture concretely this entire synthesizing process and the associated transfer of energy from the energy-supplying reductase to the synthesizing hydrolase? Let us recall, for this purpose, the model of the action of reductases proposed by us above (Fig. 2). There we depicted the energy levels along which the electron moves from cytochrome to cytochrome in the form of a staircase. Each step of this staircase corresponds to an Fe atom of the given cytochrome. From each such step the electron descends to the next, lower level, with free energy appearing; thus the energy of the detonating-gas reaction is released not all at once, but in separate portions. In order that the energy liberated at the Fe atom of the cytochrome might be used for the synthetic action of the hydrolase, the cytochrome molecule must be energetically “coupled” (directly or through the mediation of a protein) to the hydrolase molecule. Both the cytochrome molecule and the hydrolase molecule must be in some way fixed in space, i.e. attached to the structural protein of the cell. The transfer of energy from the reductase (cytochrome) to the hydrolase may then be represented, in the simplest case, as follows: an electron migrates from the upper level of the cytochrome through the protein to the upper level of the prosthetic group and from there reaches the substrate, whereupon the OH radical is converted into the OH− ion and passes into the aqueous phase. The electron, on the other hand, liberated upon the conversion of the H atom into the H+ ion, migrates, conversely, to the lower level of the prosthetic group and passes from there further to the lower level of the cytochrome. In the final analysis the following is obtained: 1) the hemin group (the Fe atom) passes from a state of greater energy into a state of lesser energy, and 2) the OH and H radicals are split off (in the form of the ions OH− and H+) from the substrate, which leads to the formation of a peptide bond.

With the aid of this simple scheme of electron transfer we obtain a conception of the connection between the dissimilating action of cytochromes (or of other enzymes participating in the respiratory process) and the assimilating action of hydrolases. On the basis of the scheme it becomes clear why the synthetic action of hydrolases is associated with certain cell structures: it can occur only in the case where the metabolically acting and the catabolically acting enzymes (i.e. the hydrolase and the cytochrome) are so connected with one another (directly or through the mediation of another protein) that an exchange of electrons can take place between their equal (or similar) energy levels. When the structure is destroyed, this energetic connection of the hydrolase with the catabolic system breaks down, and only the cleaving capacity of the hydrolase remains.

Our model also makes it possible to understand the essence of such important phenomena for the regulation of biological processes as activation and inhibition. (This applies both to cleavage and to synthesis.) The site of action of an inhibiting substance must be regarded as the prosthetic group. If, upon coupling of the inhibiting substance with the prosthetic group, the upper energy level in the latter is shifted upward, then the electron from \(OH^{-}\) cannot pass (rise) to this level, and the entire mechanism of electron transfer cannot function.

The same final result is obtained if the inhibiting substance lowers the lower energy level in the prosthetic group. Then the electron that has reached this level can no longer pass to the \(H^{+}\) ion at the substrate. It is clear that inhibition of synthesis can also be explained in an analogous way: electron exchange between the cytochrome and the substrate cannot function, since the electron cannot pass through the prosthetic group (either because the upper energy level of this group is inaccessible to it, or because it cannot leave the lower level).

Let us further mention that, on the basis of the scheme presented above for the interaction of cytochromes and hydrolases, one can also understand the peculiar periodicity—found in natural proteins (for example, in clupein)—in the arrangement of the amino acids composing them. In order not to go too far into biochemical questions, we shall limit ourselves here merely to mentioning this very interesting circumstance.

ENERGY MIGRATION

IN THE PROCESS OF CARBON DIOXIDE ASSIMILATION BY PLANTS

Finally, let us turn to one more area of biology in which energy migration apparently plays a substantial role, namely the assimilation of carbon dioxide by plants.

Emerson and Arnold\(^{17}\), as well as Gaffron and Wohl\(^{18}\), on the basis of certain experimental data, came to the conclusion that chlorophyll molecules are grouped in the living plant into definite groups, complexes (“assimilation units”). According to this conception, several thousand chlorophyll molecules belong to one assimilation unit; they are combined into a single aggregate, so that an energy quantum absorbed at any place in the aggregate is transferred in some way to one definite place, called the “reduction center,” where the energy is used for the reduction of carbon dioxide.

Energy transport of this kind from the place where the quantum is absorbed to the place where carbon dioxide is reduced should be regarded as one of the cases of energy migration. (It can be shown that the transfer of energy here occurs not by diffusion of molecules containing excess—

needed energy*).) The assimilation of carbon dioxide has therefore from the very beginning been counted among the typical examples of energy migration.^19

Several years ago Ruben and Kamen^20 made a series of observations which apparently did not accord with the hypothesis of Gaffron and Wohl, which required the presence of energy migration. In particular, these observations seemed incompatible with the conception of an “assimilation unit.”

Ruben and Kamen’s experiments on the assimilation of carbon dioxide containing radioactive carbon showed that the first step of the assimilation process consists in the non-photochemical reduction of carbon dioxide to a carboxyl (COOH). (This is also consistent with the fact that many organisms not containing chlorophyll are capable of reducing carbon dioxide.)

This first step transfers (independently of the presence of light) the carbon atoms from carbon dioxide into the carboxyl of some chemical compound whose molecular weight is approximately 1000. This compound contains no chlorophyll.

These observations show that the carbon dioxide molecule is not, during reduction, in direct connection with a chlorophyll molecule (or a group of chlorophyll molecules), and that the reduction takes place somewhere else. The notion that the assimilation unit is a complex of chlorophyll molecules with which the carbon dioxide molecule being reduced is connected in some way proves not to correspond to reality. The assimilation unit as a geometric whole, as a “polymerizate” of the chlorophyll molecule, is incompatible with the observations mentioned. If one imagines that energy migrates within such a complex (“polymerizate”), it would remain unclear how the energy reaches the site of reduction (the “reduction center”) located somewhere outside this complex. However, it can be shown that such a contradiction occurs only if one imagines the assimilation unit as a geometric whole. From the facts adduced by Gaffron and Wohl there follows only an energetic interaction between chlorophyll molecules belonging to one assimilation unit, and between these molecules and the CO₂ molecule. Only the energetic, and not the geometrical, connectedness should be regarded as proved. Taking this circumstance into account, and using certain well-founded morphological ideas about the structure of chloroplasts, we can obtain a structural picture which agrees with all the energetic, chemical, and morphological data.**)

*) See the monograph.

**) By accepting only the energetic, and not the geometrical, connectedness of chlorophyll molecules, we obtain the possibility of eliminating yet another difficulty, pointed out by Franck and Gaffron (Advances in Enzymology, Vol. 1, 1941, p. 210 ff.), which consists in the fact that resonance-

From what has been set forth earlier it is evident that the ability to conduct quantum energy is inherent not only in certain special structures, but also in such a widespread structure as the protein substance itself. It may therefore be assumed that, in the assimilation process as well, energy communication between chlorophyll molecules and the reduction center (or the molecule of CO₂ and the products of its transformation) takes place through the medium of the protein substance. For this it is sufficient to imagine that both the chlorophyll molecules and the reduction center are connected with the protein backbone of the chloroplasts.

Fig. 4. Diagram of the morphological relationship between the substances composing chloroplasts. Hydrophilic groups are hatched, hydrophobic groups are black. Chlorophyll molecules are T-shaped; lecithin molecules are fork-shaped; carotenoid molecules are straight; P denotes the protein layer; L denotes the lipid layer. (After Hubert and Frey-Wyssling.)

This conception proves especially probable if one takes into account the morphological picture of protoplasts proposed by Hubert²¹ and Frey-Wyssling²². This picture is not an ad hoc hypothesis, but a conception substantiated in detail by many chemical and morphological facts*). The essence of this conception may be explained on the basis of Fig. 4.

…a connection between chlorophyll molecules would have to be expressed in deformation of the spectrum.

) For details of this structural picture of protoplasts see the book by A. Frey-Wyssling, Submikroskopische Morphologie des Protoplasmas*, Berlin, 1938.

The chlorophyll molecule consists, as is known, of a large head portion and a long “tail.” The head portion consists of four pyrrole rings joined into a single porphyrin ring, at the center of which is located a magnesium atom. The phytol “tail” is attached to this head portion.

Fig. 4 depicts the scheme of chloroplast structure according to Hubert and Frey-Wyssling. Everything essential is evident from the drawing itself and the caption. What is important for us is chiefly the fact that the head portion of the chlorophyll molecule, and consequently also the porphyrin ring that absorbs the quanta necessary for the reduction of carbon dioxide, is turned toward the protein and is probably bound to the latter. It is immediately apparent how improbable it would be to suppose that all the various successive photoreactions take place in the narrow region situated directly at the place where the porphyrin ring adjoins the protein. It is even doubtful whether the porphyrin ring is in contact at all with the surrounding solution. It is more likely that none of the chemical reactions participating in the process of assimilation occurs directly at the porphyrin ring, because it is poorly accessible to molecules present in solution. This conclusion is fully consistent with the results of Ruben and Kamen, according to which at least the first stage of the reduction process takes place not at the chlorophyll molecule, but somewhere else.

The question arises: how does the quantum of energy absorbed by the porphyrin ring reach the site of the reaction? After we have seen that the protein itself is capable of conducting quanta of energy, the answer to this question is not difficult. According to the structural picture considered above, the porphyrin ring directly adjoins the protein backbone. The energy absorbed by the porphyrin ring can therefore pass directly to the protein and penetrate through it (by means of migration) to the place where it is expended in sustaining the reactions. Chlorophyll thus plays only the role of a sensitizer, i.e., a receiver of light energy, while all the chemical and photochemical reactions occur at other places, somewhere on the surface of the protein backbone.

We see that this conception gives a simple explanation of the joint energetic action of a large number of chlorophyll molecules, and there is no need to assume that these molecules are bound to one another directly, i.e., in the manner of a polymer. By means of the protein substance, all the chlorophyll molecules located at different places “work” for a single reduction center.

Our picture explains the “assimilation unit” and the migration of energy during assimilation; it coincides with the ability, inferred from the behavior of oxidative enzymes, of quanta of energy to migrate through the protein substance; it corresponds to chemical obser-

...by the data of Ruben and Kamen, and agrees well with the scheme of the molecular-morphological structure of chloroplasts proposed and substantiated by Hubert, Frey-Wyssling, and other authors.

SUMMARY

The facts and concepts presented in this article show that, by using the concept of energy migration, we can approach biological and biochemical problems from a new biophysical point of view. Although some of the concrete ideas set forth are only working hypotheses, they nevertheless allow us to operate in areas that until now have been only little accessible to a biophysical approach. The biological material analyzed from the new point of view is, in essence, still very limited. There is reason to think that many other phenomena connected, for example, with mitogenetic radiation, with the transmission of stimuli in nerves, etc., are also amenable to interpretation on the basis of energy migration. In the introduction it was already emphasized that the transfer of energy without a substantial increase in entropy may prove to be one of the bases for interpreting the characteristic features of the phenomenon of life. One may hope that, by following this path, it will be possible to find new and interesting results.

CITED LITERATURE

1. See, for example, I. M. Frank and S. I. Vavilov, Zeits. f. Phys. 69, 100 (1931).
2. Ya. Frenkel, Phys. Zeits. Sov. Un. 9, 138 (1936).
3. P. I. Baryshnev, DAN 2, 76, 1934.
4. F. F. Antonov-Romanovsky, DAN 2, 2 (1935).
5. V. L. Levshin, DAN 2, 108 (1935); 17 (N. S.), 95 (1937).
6. Riehl and Ortmann, Ann. d. Physik (5) 29, 561 (1937); W. H. Byler, J. Amer. Chem. Soc. 60, 632 (1938).
7. Riehl and H. M. Wolf, Ann. d. Physik (5), 11, 108 (1931); Riehl, Ann. d. Physik (5), 29, 636 (1937); Riehl, Naturwiss. 28, 601 (1940); Riehl, Trans. Faraday Soc. 35, 135 (1939).
8. N. Riehl and M. Schön, Zeits. f. Physik 114, 682 (1939). N. Riehl, “Luminescence,” OGIZ, Gostekhizdat, 1946.
9. N. W. Timofeeff-Ressovsky, K. G. Zimmer, and M. Delbrück, Nachr. Ges. Wiss. Göttingen, Fachgr. VI, N. F. 1, No. 13 (1935); N. W. Timofeeff-Ressovsky and M. Delbrück, Zeits. f. Vererbungsb. 71, 3–2 (1936).
10. N. Riehl, N. W. Timofeeff-Ressovsky, and K. G. Zimmer, Naturwiss. 29, (2) (1941); N. Riehl, R. Rompe, N. W. Timofeeff-Ressovsky, and K. G. Zimmer, Protoplasma 38, 105 (1943).
11. N. Riehl, Transactions of the Chalmers University of Technology (Sweden, Göteborg), 1944, No. 29; N. Riehl and K. G. Zimmer, Naturwiss. 30, 708 (1942).
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1. N. Riehl, Trans. of the Chalmers University of Technology (Sweden, Göteborg), 1944, No. 29; N. Riehl and K. G. Zimmer, Naturwiss. 30, 708 (1942). See also the author’s monograph mentioned above (in press).

2. G. M. Schwab, Trans. Faraday Soc. 42, 689 (1946).

3. See Mott and Jones, The Theory of the Properties of Metals and Alloys, Oxford (1936); Halla, Kristallphysik u. Kristallchemie metallischer Werkstoffe, Leipzig, 1939; Dehlinger, Chemische Physik d. Metalle u. Legierungen, Leipzig, 1939.

4. R. Emerson and W. Arnold, J. Gen. Physiology 16, 191 (1932).

5. H. Gaffron and K. Wohl, Naturwiss. 24, 81 and 103 (1936); K. Wohl, New Phytologist 39, 33 (1940).

6. N. Riehl, Naturwiss. 28, 601 (1940).

7. S. Ruben and M. B. Kamen, Journ. Amer. Chem. Soc. 62, 3451 (1940); S. Ruben, M. B. Kamen and W. Z. Hassid, Journ. Amer. Chem. Soc. 62, 3443 (1940); S. Ruben, M. B. Kamen and L. H. Berry, Journ. Amer. Chem. Soc. 62, 3450 (1940).

8. B. Hubert, Dissert. Leiden, 1935.

9. A. Frey-Wyssling, Submikroskopische Morphologie des Protoplasmas, Berlin, 1938, p. 202.

1. See the well-known investigations of O. Warburg and his school. For example, the general review by O. Warburg, Zeits. f. Elektrochemie, 1929, p. 549. ↩