J. Phys. Chem. B 2008, 112, 5189-5198
5189
Microhydration of the Guanine-Cytosine (GC) Base Pair in the Neutral and Anionic Radical States: A Density Functional Study Anil Kumar,† Michael D. Sevilla,*,† and Sa´ ndor Suhai‡ Department of Chemistry, Oakland UniVersity, Rochester, Michigan 48309, and Department of Molecular Biophysics, Deutsches Krebsforschungszentrum, Im Neuenheimer Feld 580, 69120 Heidelberg, Germany ReceiVed: NoVember 16, 2007; In Final Form: February 8, 2008
A density functional study of the effects of microhydration on the guanine-cytosine (GC) base pair and its anion radical is presented. Geometries of the GC base pair in the presence of 6 and 11 water molecules were fully optimized in the neutral (GC-nH2O) and anion radical [(GC-nH2O)•-] (n ) 6 and 11) states using the B3LYP method and the 6-31+G** basis set. Further, vibrational frequency analysis at the same level of theory (B3LYP/6-31+G**) was also performed to ensure the existence of local minima in these hydrated structures. It was found that water molecules surrounding the GC base pair have significant effects on the geometry of the GC base pair and promote nonplanarity in the GC base pair. The calculated structures were found to be in good agreement with those observed experimentally and obtained in molecular dynamics (MD) simulation studies. The water molecules in neutral GC-nH2O complexes lie near the ring plane of the GC base pair where they undergo hydrogen bonding with both GC and each other. However, in the GC anion radical complexes (GC-nH2O, n ) 6, 11), the water molecules are displaced substantially from the GC ring plane. For GC-11H2O•-, a water molecule is hydrogen-bonded with the C6 atom of the cytosine base. We found that the hydration shell initially destabilizes the GC base pair toward electron capture as a transient anion. Energetically unstable diffuse states in the hydration shell are suggested to provide an intermediate state for the excess electron before molecular reorganization of the water molecules and the base pair results in a stable anion formation. The singly occupied molecular orbital (SOMO) in the anion radical complexes clearly shows that an excess electron localizes into a π orbital of cytosine. The zero-point-energy (ZPE-) corrected adiabatic electron affinities (AEAs) of the GC-6H2O and GC-11H2O complexes, at the B3LYP/ 6-31+G** level of theory, were found to be 0.74 and 0.95 eV, respectively. However, the incorporation of bulk water as a solvent using the polarized continuum model (PCM) increases the EAs of these complexes to 1.77 eV.
Introduction In recent years, a variety of experimental1 and theoretical2 efforts have been made to understand the detailed mechanisms of radiation-induced damage to DNA. Ionization is the primary initial radiation damage and results in holes and excess electrons within DNA.3 Whereas holes have been the focus of much study, electrons and their DNA chemistry have become a recent interest because radiation-ejected electrons have been found to play an important role in the production of physical and chemical modifications in DNA.4-6 For example, Sanche and co-workers demonstrated that low-energy electrons (LEEs) can produce both single and double strand breaks in DNA.1g The electron transmission experiments by Naaman and co-workers7 demonstrated the LEE-capturing potential of DNA bases in singleand double-stranded DNA. These studies2b,e,f,8-10 suggested that electron capture in the unoccupied virtual states of the DNA bases (shape resonances) initiates the processes that lead to strand cleavage. By means of electron transmission spectroscopy experiments,11 the gas-phase vertical electron affinities (VEAs) of the DNA/RNA bases adenine (A), guanine (G), thymine (T), * To whom correspondence should be addressed. E-mail: sevilla@ oakland.edu. † Oakland University. ‡ Deutsches Krebsforschungszentrum.
cytosine (C), and uracil (U) were found to be negative. However, the adiabatic electron affinities (AEAs) of T, C, and U are nearly zero, and A and G have negative AEA values.2a,12,13 Bowen and co-workers14a estimated AEAs of 93 ( 7 meV for uracil and 69 ( 7 meV for thymine using negative-ion photoelectron spectroscopy (PES). These anions were characterized as “dipolebound anions”, in which an excess electron binds to the dipolar field of the neutral molecule. Subsequently, electron attachment to A, T, and U was experimentally studied by Schermann and co-workers,15 who estimated the corresponding AEAs (in the dipole-bound state) as 12 ( 5, 54 ( 35, and 68 ( 20 meV, respectively. In contrast, for the “valence-bound state”, they estimated the AEAs to be slightly positive (>0) for U and T and negative (
