Steering Electrons on Moving Pathways

Abstract

ConspectusElectron transfer (ET) reactions provide a nexus among chemistry, biochemistry, and physics. These reactions underpin the "power plants" and "power grids" of bioenergetics, and they challenge us to understand how evolution manipulates structure to control ET kinetics. Ball-and-stick models for the machinery of electron transfer, however, fail to capture the rich electronic and nuclear dynamics of ET molecules: these static representations disguise, for example, the range of thermally accessible molecular conformations. The influence of structural fluctuations on electron-transfer kinetics is amplified by the exponential decay of electron tunneling probabilities with distance, as well as the delicate interference among coupling pathways. Fluctuations in the surrounding medium can also switch transport between coherent and incoherent ET mechanisms-and may gate ET so that its kinetics is limited by conformational interconversion times, rather than by the intrinsic ET time scale. Moreover, preparation of a charge-polarized donor state, or of a donor state with linear or angular momentum, can have profound dynamical and kinetic consequences. In this Account, we establish a vocabulary to describe how the conformational ensemble and the prepared donor state influence ET kinetics in macromolecules. This framework is helping to unravel the richness of functional biological ET pathways, which have evolved in within fluctuating macromolecular structures.The conceptual framework for describing nonadiabatic ET seems disarmingly simple: compute the ensemble averaged (mean-squared) donor-acceptor (DA) tunneling interaction, <H DA 2 >, and the Franck-Condon weighted density of states, ρ FC , to describe the rate: (2π/ħ) <H DA 2 > ρ FC . Modern descriptions of the thermally averaged electronic coupling and of the Franck-Condon factor establish a useful predictive framework in biology, chemistry, and nanoscience. Describing the influence of geometric and energetic fluctuations on ET allows us to address a rich array of mechanistic and kinetic puzzles. How strongly is a protein's fold imprinted on the ET kinetics, and might thermal fluctuations "wash out" signatures of structure? What is the influence of thermal fluctuations on ET kinetics beyond averaging of the tunneling barrier structure? Do electronic coupling mechanisms change as donor and acceptor reposition in a protein, and what are the consequences for the ET kinetics? Do fluctuations access minority species that dominate tunneling? Can energy exchanges between the electron and bridge vibrations generate vibronic signatures that label some of the D-to-A pathway traversed by the electron, thus eliminating unmarked pathways that would otherwise contribute to the DA coupling (as in other "which way" or double-slit experiments)? Might medium fluctuations drive tunneling-hopping mechanistic transitions? How does the donor-state preparation -in particular its polarization toward the acceptor and its momentum characteristics (which may introduce complex rather than pur...

Biological charge transfer via flickering resonance

“…For the inhomogeneous system in Fig. S2, the decay of the D-to-A rate for the superexchange mechanism would be proportional to the square of the B-mediated D-A tunneling matrix element V 2 DA ∝ e −βR dA , where β ≈ (2/3.4 Å) ln [(ΔE B /V rms )] in the perturbative limit (1,2,26,27). Substituting V rms = 0.1 eV and ΔE B = 1 eV gives β ≈ 1.4 Å −1 .…”

“…Redox energy fluctuations are of particular significance when transport barrier heights and the energy fluctuations are of similar magnitude. Indeed, the sensitivity of biological electrontransfer (ET) rates to conformational fluctuations and consequent (transient) delocalization is the topic of intense interest (1)(2)(3). Resonant enhancement of biological ET rates is consistent with a growing body of physical and structural data found in DNA ET through stacked nucleobases (4), extended delocalized structures of bacterial photosynthesis (including the special pair, bridging chlorophyll and pheophytin) (5), the polaronic states of oxidized porphyrin arrays up to seven porphyrin diameters in spatial extent (6), micrometer-scale bacterial nanowires (7,8), multiheme oxidoreductases (9,10), amino acid side chains in ribonucleotide reductase (11), engineered protein-based hopping-chains (12), and centimeter-scale charge-transport chains in filamentous bacteria (13).…”

Charge transport network dynamics in molecular aggregates

“…Whereas the static picture provides many insights into the nature of charge transport in soft materials, recent work has emerged indicating the importance of time-dependent fluctuations. Throughout the rest of this article we refer to these fluctuations as "dynamic disorder" (11)(12)(13)(14)(15)(16).In this work we use network analysis to examine the impact of dynamic disorder on charge transport networks of aggregates of two representative organic semiconducting molecules, perylenediimide (PDI, Fig. 1) (17) and bBDTðTDPPÞ 2 (18).…”

Flexibility of the metal-binding region in apo-cupredoxins

“…metalloproteins | nuclear magnetic resonance | protein dynamics L ong-range electron transfer (ET) in proteins is a key chemical event in many essential biological processes such as cellular respiration and photosynthesis (1)(2)(3). According to Marcus' semiclassical theory, the outstanding efficiency of these processes is based on the maximization of the superexchange coupling between donor and acceptor and the minimization of the reorganization energy, given the low driving forces found in most biological systems (4)(5)(6).…”