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

Abstract

The earliest studies of electron-transfer proteins1 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.