Multi‐Pathway Excited State Relaxation of Adenine Oligomers in Aqueous Solution: A Joint Theoretical and Experimental Study

Abstract

The singlet excited states of adenine oligomers, model systems widely used for the understanding of the interaction of ultraviolet radiation with DNA, are investigated by fluorescence spectroscopy and time-dependent (TD) DFT calculations. Fluorescence decays, fluorescence anisotropy decays, and time-resolved fluorescence spectra are recorded from the femtosecond to the nanosecond timescales for single strand (dA)20 in aqueous solution. These experimental observations and, in particular, the comparison of the fluorescence behavior upon UVC and UVA excitation allow the identification of various types of electronic transitions with different energy and polarization. Calculations performed for up to five stacked 9-methyladenines, taking into account the solvent, show that different excited states are responsible for the absorption in the UVC and UVA spectral domains. Independently of the number of bases, bright excitons may evolve toward two types of excited dimers having π-π* or charge-transfer character, each one distinguished by its own geometry and spectroscopic signature. According to the picture arising from the joint experimental and theoretical investigation, UVC-induced fluorescence contains contribution from 1) exciton states with a different degree of localization, decaying within a few ps, 2) "neutral" excited dimers decaying on the sub-nanosecond timescale, being the dominant species, and 3) charge-transfer states decaying on the nanosecond timescale. The majority of the photons emitted upon UVA excitation are related to charge-transfer states.

Exciton delocalization, charge transfer, and electronic coupling for singlet excitation energy transfer between stacked nucleobases in DNA: An MS-CASPT2 study

“…Such charge transfer states have been invoked in previous experimental and computational studies on DNA spectroscopy. 17,22,24,26,27,45 In the stacks AT, GC, and GT, there is a low-lying charge transfer state that mixes with the two locally excited diabatic states. In the AC dimer, the charge transfer character is not so prominent (8% for S 2 ).…”

“…Excitonic and charge transfer states have been made responsible for this difference, and the role of these states has been discussed extensively on the basis of experimental 2,3,[15][16][17][19][20][21][22][23][24][25] and theoretical 14,24,[26][27][28] work. Most theoretical ab initio approaches on the excited states of DNA have considered small polymers, for which the excited states are calculated using time-dependent density functional theory 24,[26][27][28] (TD-DFT) or wave function based methods. 14 The excited state studies are often preceded by molecular dynamics calculations to account for the structural fluctuations of the polymer.…”

Charge separation and charge delocalization identified in long-living states of photoexcited DNA

“…Several explanations for these long-living states and the size of their spatial extent have been discussed in the literature (5)(6)(7)(8)(9). Delocalized excitons (9); excitons that decay to charge-separated states or neutral excimer states (10,11); exciplexes located on two neighboring bases (5,8,12,13); or even excited single bases, where steric interactions in the DNA strand impedes the ultrafast decay (14), have been proposed. Further computations suggest a decay of an initially populated delocalized exciton to localized neutral or charged excimer states (15)(16)(17).…”

Computational Modeling of Photoexcitation in DNA Single and Double Strands

“…Using an excitonic model, Improta et al [150] pointed out in particular that there is a fast and effective transfer in stacked adenines between bright excitonic states and dark charge-transfer states, because of their strong coupling. Recent theoretical studies [153,157] on (dA) 4 and (m 9 A) n (n ¼ 1-5) at the PCM/TDDFT level, combined with spectroscopy experiments on (dA) 20 , enriched the proposed scenario: the absorbing states of stacked adenines are bright excitonic states delocalized over up to four bases; they may rapidly localize to bright excited states on base monomers, or evolve into darker 1 π ! π* excimers and/or charge-transfer excimers/exciplexes.…”