Photochemical selectivity in guanine-cytosine base-pair structures

Abstract

Prebiotic chemistry presumably took place before formation of an oxygen-rich atmosphere and thus under conditions of intense short wavelength UV irradiation. Therefore, the UV photochemical stability of the molecular building blocks of life may have been an important selective factor in determining the eventual chemical makeup of critical biomolecules. To investigate the role of UV irradiation in base-pairing we have studied guanine (G) and cytosine (C) base pairs in the absence of the RNA backbone. We distinguished base-pair structures by IR-UV hole-burning spectroscopy as well as by high-level correlated ab initio calculations. The Watson-Crick structure exhibits broad UV absorption, in stark contrast to other GC structures and other base-pair structures. This broad absorption may be explained by a rapid internal conversion that makes this specific base pair arrangement uniquely photochemically stable.

Fig. 1.

Twenty lowest-energy hydrogen-bonded GC structures. Stabilization energy for each is indicated in kcal/mol relative to that of the lowest-energy configuration, the WC structure (11). Blue circles indicate structures that are not possible with 1-substituted cytosine, and gray circles indicate structures that are not possible with 9-substituted guanine.

Fig. 2.

REMPI spectra recorded at the mass of guanine–cytosine (B and C), 9-ethylguanine-1-methylcytosine (A1), guanine–cytidine (A2), and guanosine–cytidine (A3). All spectra are one-color, two-photon spectra, except B, which is a two-color spectrum with 266 nm for the ionization laser. All spectra were recorded at the parent mass of the respective cluster. The cluster structures in the figure were optimized at the DFT (B3LYP/6–311G^**) level.

Fig. 3.

IR–UV hole-burning spectra of structures A1, B, and C from Fig. 2 (A–C). The vertical bars are frequencies obtained from ab initio calculations (15). The colors indicate the respective modes. When there are two possibilities, asterisks indicate modes that reside on the guanine. “#” indicates two NH₂ antisymmetric stretches that are within 7 cm^-1 from each other. (a), antisymmetric; (s), symmetric.