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.ab initio computation ͉ DNA base pairs ͉ IR-UV spectroscopy ͉ jet cooling ͉ photochemistry T he DNA bases involved in reproduction have short S 1 excited state lifetimes, of the order of 1 ps or less (1-7). It has been argued that this phenomenon serves to protect these bases against photochemical damage, because after excitation they do not cross to the reactive triplet state; instead, they rapidly internally convert to the electronic ground state (8). This mechanism may have been particularly significant under the conditions of the early earth, when purines and pyrimidines presumably were assembled into the first macromolecular structures, producing RNA. At that time, the earth was exposed to shorter wavelength UV radiation than it is today. For an analysis of possible prebiotic chemistry, it is necessary not only to consider the individual bases but also to study them as they interact and to do so without the RNA backbone (9). We achieve such an analysis by studying clusters of guanine (G) and cytosine (C) in the gas phase by using double resonant laser spectroscopy techniques. The experimental studies are accompanied by stateof-the-art quantum chemical and molecular dynamics calculations of the pairing of G and C. These two bases can form many different hydrogen-bonded structures, of which at least 20 are within 12 kcal͞mol of the global minimum. Thus, the familiar Watson-Crick (WC) structure may not be unique, based on energies alone. Here, we report a remarkable difference in excited state properties among the WC structure and other structures. The former exhibits broad UV absorption features; this is in contrast with the sharp UV spectra exhibited by non-WC structures. The broad absorption can be explained by recent theoretical results, predicting a pathway for rapid internal conversion (10). If the difference is solely due to lifetime broadening, these results correspond to a lifetime for the WC structures that is at least 2 orders of magnitude shorter than those of observed non-WC structures. Thus, it appears possible that the WC recognition mechanism involves a structure that was significantly more stab...

Gas-Phase IR Spectroscopy of Nucleobases

“…In the work of Nir et al only a substituted version (9-ethylG-1-methyl-C) was reported (panel (a) Figure 12 and its corresponding two-photon UV spectrum was very broad. Presumably, the WatsonCrick structure has a sub-picosecond excited state lifetime, while other structural arrangements of the same base pair have sharp spectra, consistent with much longer excited state lifetimes (97). To explain the effect, the right column of Figure 12 shows calculated potential curves from Sobolewski and Domcke (96).…”

Ultrafast excited-state dynamics of RNA and DNA C tracts

“…The possibility that base pairing facilitates electronic energy relaxation on an ultrafast time scale by proton or hydrogen atom transfer has been actively discussed recently [23,24,44]. By virtue of the slow energy relaxation seen in the hemiprotonated forms, the CH + ·C base pair joins the growing list of base pairs that support excited states, which are longer-lived than those of monomeric bases-at least for base pairs present in base stacks.…”

“…Markovitsi et al [21] and Buchvarov et al [9] have proposed an alternative assignment of the long-lived states to delocalized Frenkel excitons. Other researchers have emphasized the possibility of hydrogen atom or proton transfer within base pairs as a potential relaxation pathway for excess electronic energy [22][23][24]. Further experimental work on base multimers is urgently needed to better understand the effects of electronic coupling between proximal bases.…”

Nonradiative decay of the lowest excited singlet state of 2-aminopyridine is considerably faster than the radiative decay

“…The ultrashort lifetime of DNA may be associated with base-pairing and base-stacking interaction, genuine electronic property of DNA bases, and the solvation. [1][2][3][4][5][6][7][8][9][10] However, it is difficult to identify the exact mechanism due to the complexity of DNA structures. In this context, the 2-AP dimer was used as a simplified model for DNA base pairs by Schultz et al 1 and Sobolewski and Domcke.…”