Tautomeric selectivity of the excited-state lifetime of guanine/cytosine base pairs: the role of electron-driven proton-transfer processes

Abstract

The UV spectra of three different conformers of the guanine/cytosine base pair were recorded recently with UV-IR double-resonance techniques in a supersonic jet [Abo-Riziq, A., Grace, L., Nir, E., Kabelac, M., Hobza, P. & de Vries, M. S. (2005) Proc. Natl. Acad. Sci. USA 102, 20-23]. The spectra provide evidence for a very efficient excited-state deactivation mechanism that is specific for the Watson-Crick structure and may be essential for the photostability of DNA. Here we report results of ab initio electronic-structure calculations for the excited electronic states of the three lowest-energy conformers of the guanine/cytosine base pair. The calculations reveal that electron-driven interbase proton-transfer processes play an important role in the photochemistry of these systems. The exceptionally short lifetime of the UV-absorbing states of the Watson-Crick conformer is tentatively explained by the existence of a barrierless reaction path that connects the spectroscopic (1)pi pi * excited state with the electronic ground state via two electronic curve crossings. For the non-Watson-Crick structures, the photochemically reactive state is located at higher energies, resulting in a barrier for proton transfer and, thus, a longer lifetime of the UV-absorbing (1)pi pi * state. The computational results support the conjecture that the photochemistry of hydrogen bonds plays a decisive role for the photostability of the molecular encoding of the genetic information in isolated DNA base pairs.

Fig. 1.

Equilibrium structures of the ground state of the three conformers of the GC dimer. The numbers denote bond lengths in angstroms.

Fig. 2.

Equilibrium structures of the ¹π π * CT state after transfer of the proton for the three conformers of the GC dimer. The numbers denote bond lengths in angstroms.

Fig. 3.

Potential-energy functions of the S₀ state, the locally excited ¹π π * states of guanine (blue) and cytosine (green), the lowest ¹nπ * state (violet), and the ¹π π * CT state (red) of the WC conformer (a), the conformer B (b), and the conformer C (c) of the CG dimer. The potential-energy functions have been calculated along the linear-synchronous-transit proton-transfer reaction path from the S₀ minimum (Fig. 1) to the biradical minimum (Fig. 2). (Insets) Potential-energy function of the lowest excited singlet state (the locally excited ¹π π * state of guanine) calculated along the minimum-energy path for stretching of the NH bond of the azine group of guanine (the proton-transfer coordinate). The potential-energy functions shown in the insets provide estimates of the energy barriers for proton transfer.