Experimental test of the vibronically coupled tunneling description of biological electron transfer.

Abstract

Evidence for the constructs central to vibronically coupled electron transfer has been obtained. Our experiments show the existence of a weak (f t 10-v) charge-transfer absorption band in the near infrared for the bound donor-acceptor complex, cytochrome c-Fe(CN 6. Such a charge-transfer band had been predicted from the theory of such transfers. The experimental method, using a form of excitation modulation spectroscopy, measures only the optical absorption that induces charge transfer between the donor and the acceptor (and does etect other absorptions) and allows the study of chargetransfer bands whose absorbances are small compared to the sample absorbance. The energy position and oscillator strength of the band agree with the general predictions of this vibronically coupled tunneling theory. We suggest that, in this system at room temperature, the electron transfer can be described by this tunneling theory. This model system result gives credence to the short electron transfer distances the theory has predicted for biological electron transfers. Electron transfer is an essential process in photosynthetic and aerobic life systems. The molecular mechanism by which solar energy is captured and converted into chemical energy necessitates electron transfer. Photoexcitation of chlorophyll results in a series of electron transfers in which an electron is moved from a high-potential cytochrome to a low-potential molecule on the opposite side of the membrane. Absorption of light results in the creation of an electron-hole pair necessary for useful chemical work. Selectivity must prevent those spontaneous "downhill" transfers that result in electron flow from the low-potential molecule back to the high. Enzyme composition and conformational mobility must be optimized to achieve efficient electron transfers. The molecular mechanism of electron transfer in photosynthesis and in respiration are identical in principle. An understanding of the mechanism of electron transfer in biomolecules is of fundamental importance to an explanation of the functions and meanings of the complex intermolecular relationships of components in an electron transfer chain.There is direct experimental support for the idea that, at low temperatures, tunneling is involved in electron transfer. However, attempts to describe biomolecular electron transfer as an electron tunneling from a bound state of energy on one molecule to an electronic continuum of energies (1, 2) miss the essence of the tunneling problem between two local states, such as two biomolecules. By representing the second site as a metal instead of as a single energy level, one makes a conceptual error which results in an answer permitting huge tunneling distances-30-80 A. To correct this error, a theory based on electron tunneling between two states with the energy conserved by vibronic coupling in the individual molecules (3-5) has been introduced. In this theory, the sites are correctly represented as having a single electronic level. The presence of the Abbreviations: C...

Electron transfers involving biological molecules in solution

“…86 The NMR line broadening data were analyzed to give the following conclusions. The mechanism proposed Fecyt c-Fe(CN)63' ^Fecyt c + Fe(CN)63' (42) with K = 0.4 X 10'3 M'1, k = 208 s'1, and k' = 2.08 X 104 s'1. The measurements were made in 100 mM HEPES buffer, pH 6.9.…”

Ferricytochrome c oxidation of cobaltocytochrome c. Comparison of experiments with electron-transfer theories

“…The first is the theory of outersphere transfer of Marcus (1963Marcus ( ,1964 most commonly employed in the relative form (Marcus and Sutin, 1974). The second one is the theory of multiphonon nonadiabatic electron tunneling (Hopfield, 1974(Hopfield, ,1977Potasek and Hopfield, 1977;Jortner, 1976). The central purpose of our program is to carefully study electron transfer between protein molecules, to consider the relative merits of various models, and to suggest possible direction for refinement of theories.…”

Evaluation of the role of polyisoprenyl functional groups in biological electron transfer. Transition metal models

“…While this viewpoint presents a somewhat comforting rationalization of the problem, it should not be taken as established. Some structural evidence consistent with these suggestions has been presented (Carter et al, 1974a,b;Colman et al, 1978), but other studies suggest that biological reorganizational energies may not be unusually small (Hopfield, 1974;Potasek & Hopfield, 1977;Potasek, 1978). It should be noted, however, that to the extent that these ideas are valid the isoprenyl chain may be capable of promoting electron tunneling in biological particles but not in transition metal ions simply because reorganizational energies in the latter reactions are larger.…”