DNA Is Not a Molecular Wire: Protein-like Electron-Transfer Predicted for an Extended π-Electron System

Abstract

The earliest studies of electron-transfer proteins 1 raised the question of whether or not π-electron residues might facilitate electron transport. 2 Three recent long-range electron-transfer experiments utilizing DNA bridges revisit this provocative, yet unresolved, question. 3,4,5 The distance dependence of electron transfer in DNA is not a matter of purely academic concern; it controls the mechanism of DNA damage and repair in cells and is being exploited in new molecular probes of DNA sequence. We present a theoretical analysis based upon very large scale self-consistent-field quantum calculation of all valence electrons (as many as ∼3300) in these three systems. This computation is the first performed on such large macromolecules and also the first to extract long-range electronic interactions at this level of theory. DNA electron transfer is found to be mediated by through-space interactions between the π-electron-containing base pairs, but the magnitude of the coupling facilitated by this channel drops rapidly with distance, as a consequence of the ∼3.4 Å noncovalent gap between base pairs. These predictions are in agreement with most of the experimental data. The rapid decay of electron-transfer rates with distance computed here suggests that biologically controlled DNA electron-transfer events, of importance in DNA repair, 6 must function over relatively short range. Moreover, the predicted distance dependence of electron transfer in DNA is strikingly close to that found in proteins.