Superexchange Mediated Charge Hopping in DNA ² Joshua Jortner,* ,‡ M. Bixon, ‡ Alexander A. Voityuk, § and Notker Ro 1 sch § School of Chemistry, Tel AViV UniVersity, Ramat AViV, 69978 Tel AViV, Israel, and Institut fu ¨ r Physikalische und Theoretische Chemie, Technische UniVersita ¨ t Mu ¨ nchen, 85747 Garching, Germany ReceiVed: NoVember 15, 2001; In Final Form: February 4, 2002 We explore the relationship between the electronic-nuclear level structure, the electronic couplings, and the dynamics of hole hopping transport in DNA. We utilized the electronic coupling matrix elements for hole transfer between nearest-neighbor nucleobases in DNA [Voityuk, A. A.; Jortner, J.; Bixon, M.; Ro ¨sch, N. J. Chem. Phys. 2001, 114, 5614] to evaluate intrastrand and interstrand superexchange electronic couplings, which determine hole hopping rates within the framework of a semiempirical quantum mechanical-kinetic model. Calculations of the exponential distance (R) dependence of the superexchange mediated intrastrand electronic couplings |V super | 2 ∝ exp(-R) between guanines (G) in “short” G + (T-A) n G(n j 3) duplexes result in  ) 0.8-0.9 Å -1 . We interpret the experimental data on time-resolved hole transport in the presence of a site-specifically bound methyl transferase mutant in DNA [Wagenknecht, H.-A.; Rajski, S. R.; Pascally, M.; Stemp, E. D. A.; Barton, J. K. J. Am. Chem. Soc. 2001, 123, 4400] in terms of composite sequential, interstrand and intrastrand superexchange mediated, and direct interstrand hole hopping. This mechanism accounts for the rate determining step, for the weak duplex size dependence of the rate, and for the long- range charge transport induced by interstrand superexchange via short (T-A) bridges, containing a single mediating nucleobase. For hole transfer via longer (T-A) n (n J 3) bridges, the superexchange mechanism is replaced by the parallel mechanism of thermally induced hole hopping (TIH) via long (A) n chains. A kinetic analysis of the experimental data for hole transport through seven GG pairs separated by (T-A) n (n ) 2-5) bridges across the 3′-5′ strand of the DNA duplex [Sartor, V.; Boone, E.; Schuster, G. B. J. Phys. Chem. B, 2001, 105, 11057] reveals that the superexchange-TIH crossover occurs at n ) n x ) 3. The explorations of the range of applicability and the breakdown of the superexchange mechanism in DNA lay the foundations for the scrutiny of the universality and system specificity of this mechanism in large-scale chemical and biophysical systems. I. Prologue Wilse Robinson made seminal contributions to modern chemical physics, encompassing pioneering experimental and theoretical explorations of matrix isolation electronic spectros- copy, 1 radiationless transitions, 2 elementary electronic-vibra- tional excitations in neat and mixed organic molecular solids, 3 and energy transfer in organic molecular crystals. 4,5 In the latter context of triplet energy transfer in isotopically mixed molecular crystals (e.g., naphthalene and benzene), Nieman and Robinson advanced in 1962 the concept of superexchange mediated triplet energy transfer. 4,5 They proposed that the triplet impurity band of an isotopically mixed crystal is characterized by superex- change interactions where γ is the nearest-neighbor impurity-impurity exchange integral and δE represents the energy separation of the impurity excitation from the center of the exciton band, whereas γ/δE , 1, as appropriate for a perturbative treatment, and n represents the number of the host molecules separating the two impurities. The superexchange electronic coupling, eq 1, can be recast as an exponential interimpurity distance (R) dependence where  h) 2ln(δE/γ)/R 0 , J 0 ) γ exp( h R 0 /2), and R 0 is the nearest-neighbor distance. The triplet energy transfer rate k T ) (2π/p)|J| 2 F, where F is the density of final states, is given by The Robinson superexchange mechanism for triplet energy transfer was extended by Kopelman 6 for the exploration of the percolation model and by Klafter and Jortner 7 for the study of Anderson localization of triplet excitations in substitutionally disordered, isotopically mixed molecular crystals. When Robinson advanced the superexchange mechanism for triplet electronic energy transfer, this mechanism was already of much earlier vintage in other fields, i.e., magnetic interactions in solids and electron transfer (ET) in solution. In 1934 Kramers 8 studied adiabatic demagnetization in paramagnetic salts, which indicated that small exchange couplings existed even between ions separated by one or several diamagnetic groups. Paramag- netic ions could exert spin-dependent perturbations in the wave functions of intervening diamagnetic ions, thereby transmitting the exchange effect over large distances, 8 which led to the name “superexchange”. 9 The concept was revived and extended by ² Part of the special issue “G. Wilse Robinson Festschrift”. Dedicated to the memory of G. Wilse Robinson, a tribute to his seminal contributions to science. * To whom correspondence should be addressed. ‡ Tel Aviv University. § Technische Universita ¨t. J ) J 0 exp(- ( h /2)R) (2a) k T ) (2πJ 0 2 F/p) exp(-  h R) (2b) J ) γ(γ/δE) n (1) 7599 J. Phys. Chem. A 2002, 106, 7599-7606 10.1021/jp014232b CCC: $22.00 © 2002 American Chemical Society Published on Web 07/04/2002