Session D6: Long-Distance Charge Transfer in Biological Systems

Theory of Electron Transfer and Transport Pathways in Biomolecules

Electron transfer in proteins and nucleic acids occurs over large distances by a combination of short and long range tunneling mechanisms. Electron tunneling is facilitated by virtual oxidized and reduced states of the bridging macromolecule, and theoretical analysis reveals how a macromolecule's fold, energetics, and fluctuations influence the electron-transfer kinetics. Recent studies of protein electron transfer indicate when and why electron tunneling kinetics is sensitive to the structure of the protein's tunneling pathways. Electron transfer across protein-protein interfaces involves thin structured water layers that play a key role in tunneling mediation as well. Tunneling analysis that takes the dynamical fluctuations of the macromolecules into explicit account provides a unified view that links structure and function in protein electron transfer. In the case of DNA electron transport, a critical role is found for structural fluctuations and transport mediated by carrier injection to intervening bases, even at very short distances.   

Long-Range Electron Transfer through Proteins and Solvents

Reactions in which electrons tunnel long distances from donors (D) to acceptors (A) pervade solid-state physics, chemistry and biology. Theory suggests that the barriers to these tunneling processes depend strikingly on the composition and structure of the intervening medium. Poor coupling across nonbonded interfaces produces a strong bias in favor of covalent and hydrogen-bonded pathways between redox sites in proteins. The coupling disparity between bonded and nonbonded interfaces accounts in large part for the finding that protein electron-transfer rates do not exhibit a uniform dependence on distance, but instead depend critically on the composition of the medium between redox sites. Rates at a single D-A separation can differ by three orders of magnitude and D-A distances that differ by as much as 0.5 nm can produce identical rates. Our investigations of electron tunneling through proteins and solvents are aimed at elucidating the factors that determine long-range D-A couplings.   

Correlated electron and proton transport in cytochrome c oxidase: Coulomb proton pump with kinetic gating

I will discuss correlated transport of electrons and protons in cytochrome c oxidase, the terminal enzyme in the respiratory electron transport chain of aerobic organisms. This enzyme catalyzes the reduction of atmospheric oxygen to water in our cells, and utilizes the free energy of oxygen reduction for the creation the membrane proton gradient by pumping protons across the membrane. The proton gradient subsequently drives the synthesis of ATP. The details of the mechanism of this redox-driven proton pump are unknown. Computer simulations and theoretical modeling point to a possible mechanism of this biological molecular machine in which electron transport is coupled to proton translocation.   

Theoretical/Computational Probes of Homogeneous and Interfacial Electron Transfer: Electronic Structure and Energetics

Theoretical and computational techniques are used to elucidate the physical and chemical factors that control the kinetics of homogeneous and interfacial electron-transfer (ET) reactions. These latter include systems for which standard rate constants ($k^{0}(l))$ have been measured electrochemically for ET between substrate Au electrodes and redox couples attached to the electrode surfaces by variable lengths ($l)$ of oligomethylene (OM), oligophenylenevinylene (OPV) and oligophenyleneethynylene (OPE) bridges. These oligomers, spanning a range of $\sim $ 1-4 nm, are components of mixed self-assembled monolayers (SAMs), coupled to the substrate via S atom linkers. The mechanistic analysis of the kinetic behavior, including polaron-based activation and electronic tunneling, is supported by calculations of electronic structure and molecular and medium energetics. Band structure calculations for neat phenylthiolate SAMs on Au and Cu susbstrates were used to probe the properties of the interface, including surface dipole layer and work function, the electronic nature of the `thiolate' linker atoms, and the competition between direct and substrate-mediated coupling.   

A nonadiabatic and nonlinear theory for electron transfer

We propose a general theory both non adiabatic and nonlinear which extends those used for the standard theory of electron transfer (ET) in chemistry but also becomes equivalent to it far from the inversion point. In the vicinity of the inversion point, the model parameters may be finely tuned such that large amplitude electronic oscillations between the donor and an extrasite, associated with large amplitude and collective phonon oscillations at the same frequency, are spontaneously generated (coherent electron–phonon oscillator or CEPO). This extrasite is not a true acceptor but could play the role of a catalyst because by the CEPO it may trigger irreversible and ultrafast ET at low temperature toward a third site which is a real acceptor (while in the absence of catalyst, ET cannot occur). Such a trimer system may be regulated by small perturbations and behaves as a molecular transistor. We illustrate this idea by explicit numerical simulations on trimer models of the type donor-catalyst-acceptor. We discuss the relevance of our approach for understanding the ultrafast electron transfer experimentally observed in biosystems such as the photosynthetic reaction center.