Hole Trapping, Detrapping, and Hopping in DNA ² M. Bixon* and Joshua Jortner* School of Chemistry, Tel AViV UniVersity, Ramat AViV, 69978 Tel AViV, Israel ReceiVed: February 19, 2001; In Final Form: April 17, 2001 In this paper we present a self-consistent kinetic-quantum mechanical analysis of chemical yield data for hole trapping/detrapping in G + (T-A) m GGG duplexes (with free energy gaps Δ t ) and for hole hopping/trapping/ detrapping in G + [(T) m G] n (T) m GGG duplexes of DNA. Bridge specificity of hole trapping/detrapping by GGG traps was specified by superexchange electronic contributions, inferred from electronic coupling matrix elements between nearest-neighbor nucleobases and semiempirical energy gaps, and energetic contributions, which determine the nuclear Franck-Condon factors. Unistep hole-trapping yields are accounted for by a weak bridge length dependence for short (N ) 1, 2) bridges, due to detrapping. Marked bridge specificity is manifested for short (N ) 1, 2) bridges, being distinct for (T) N and for [(A) m+1 (T) m′ ] n (m, m′ g 0 and N ) n(m + m′ + 1)) bridges. For long (N > 2) bridges an exponential bridge size dependence of the trapping yields prevails. Multistep hole transport results in different reaction rates of G + (rate k d ) and of (GGG) + (rate k dt ) with water, i.e., k d /k dt ) 1.6, which, in conjunction with the unistep trapping/detrapping data, results in the free energy gaps for hole trapping of ∆ t ) 0.096 eV in the G + (T) N GGG duplexes and of ∆ t ) 0.062 eV in the G + [(A) m+1 (T) m′ ] n GGG duplexes. 1. Introduction Interest in charge transfer and transport in DNA 1-10 stems from biological implications, e.g., radiation damage, protection and repair, and from the novel area of dynamics, response, and function of nanostructures and biosensors. The majority of the experimental information on charge transport in DNA involves positive charge (hole) migration. For resonance donor-bridge interactions, hole hopping occurs between guanine (G) bases. Experimental chemical yield data of Giese et al., 11-15 Saito et al., 16-19 Barton et al., 20,21 and Schuster et al. 22-25 and time- resolved data of Lewis et al. 26-28 infer that intrastrand GG doublets and GGG triplets act as hole traps from G + in accord with computational results. 19,29,30 Recent semiempirical calculations by Voityuk et al. 29 for the energetics of hole trapping yield stabilization energies of 0.3- 0.13 eV for (GGG) + and for (GG) + relative to G + , with the spread of the energetic values being due to effects of nearest neighbor bases and to directional asymmetry. These calculated energetic data are considerably lower than those calculated by Saito et al., 19,30 and seem to be in semiquantitative agreement with experimental kinetic data of Lewis et al. 27,28 The rates of hole trapping and reversible detrapping in the systems and result in the free energy gaps ∆G t ) 0.053 eV 27,28 between the states GA(GG) + A and G + AGGA, and ∆G t ) 0.077 eV 28 between GA(GGG) + A and G + AGGGA, pointing toward the role of (GG) and (GGG) as shallow hole traps. Meggers et al. 13 provided extensive experimental information for the yields of hole trapping in a series of duplexes G + (T-A) m GGG, which indicates that the relative yields for the reaction with water between the terminal (GGG) and the initial G (separated by the distance R) obey an approximate exponential distance depen- dence of the trapping rate (∝ exp(-R), with  ) 0.9 Å -1 ), in qualitative agreement with unistep superexchange hole transfer for this elementary process. The description of hole transport through G + “resting states” brought together multistep hopping and unistep superexchange, with the individual hopping rates between G bases in GXY...G (with X, Y ) T or A) being superexchange mediated through the bridging (T-A) bases. Experimental evidence for long-range (distance scale 50 Å - 300 Å) hole transport via G bases induced by hole shift or injection, stems from chemical yield data and was reported by Barton et al., 20,21 Giese and Michel-Beyerle, 14 and Schuster et al. 22-25 The moderately large distance scale for hole transport in DNA duplexes is limited by the parallel side reactions of the G + “resting sites” and of the (GGG) + hole traps with water, 11-15,20-25 which involves a major depletion channel for the hole charge carriers in DNA. Analyti- cal kinetic models, based on the superexchange mediated hopping picture in conjunction with the water reaction of the G + radical cations, were applied 31-35 to account for the bridge size dependence of the chemical yields for long-range hole shift in the G + [(T) m G] n (T) m GGG over the G + ...GGG distance scale of 10-40 Å (n ) 0-3, m ) 2) reported by Giese et al. 13,14 The heuristic kinetic analysis of hole trapping in the G + (T-A) n GGG duplexes, 13 and the previous kinetic analysis of hole hopping and trapping in the G + [(T) m G] n (T) m GGG duplexes by Bixon et al. 32,33 and by Berlin, Burin, and Ratner 34,35 and by Siebbeles and Berlin 36,37 considered only exoergic hole ² This work was presented at the PP2000 in Costa do Estoril, Portugal, honoring Professor Ralph Becker’s contributions. * Corresponding authors. G + AGGA { \ } k tr k -tr G A(GG) + A G + AGGGA { \ } k tr k -tr GA(GGG) + A 10322 J. Phys. Chem. A 2001, 105, 10322-10328 10.1021/jp0106552 CCC: $20.00 © 2001 American Chemical Society Published on Web 08/14/2001