Excited States in DNA Strands Investigated by Ultrafast Laser Spectroscopy

Abstract

Ultrafast laser experiments on carefully selected DNA model compounds probe the effects of base stacking, base pairing, and structural disorder on excited electronic states formed by UV absorption in single and double DNA strands. Direct π-orbital overlap between two stacked bases in a dinucleotide or in a longer single strand creates new excited states that decay orders of magnitude more slowly than the generally subpicosecond excited states of monomeric bases. Half or more of all excited states in single strands decay in this manner. Ultrafast mid-IR transient absorption experiments reveal that the long-lived excited states in a number of model compounds are charge transfer states formed by interbase electron transfer, which subsequently decay by charge recombination. The lifetimes of the charge transfer states are surprisingly independent of how the stacked bases are oriented, but disruption of π-stacking, either by elevating temperature or by adding a denaturing co-solvent, completely eliminates this decay channel. Time-resolved emission measurements support the conclusion that these states are populated very rapidly from initial excitons. These experiments also reveal the existence of populations of emissive excited states that decay on the nanosecond time scale. The quantum yield of these states is very small for UVB/UVC excitation, but increases at UVA wavelengths. In double strands, hydrogen bonding between bases perturbs, but does not quench, the long-lived excited states. Kinetic isotope effects on the excited-state dynamics suggest that intrastrand electron transfer may couple to interstrand proton transfer. By revealing how structure and non-covalent interactions affect excited-state dynamics, on-going experimental and theoretical studies of excited states in DNA strands can advance understanding of fundamental photophysics in other nanoscale systems.

UV‐inducedDNADamage: The Role of Electronic Excited States

“…Since the turn of the century, the electronic excited states of nucleic acids per se have been the subject of an increasing number of experimental and theoretical studies. On one hand, the improvement of time-resolved techniques has allowed scientists to study their fate over a large time domain, starting from the femtosecond scale; this is achieved by detecting either nucleic acids' absorption in the UV/visible or IR spectral domains or their fluorescence emission (4)(5)(6)(7)(8)(9)(10)(11). On the other hand, with the development of advanced computational methods, it is now possible to include in the calculation of the excited states factors that are crucial for biological systems, such as water molecules, metal cations or even conformational motions of the phosphodeoxyribose backbone (12)(13)(14)(15)(16)(17)(18).…”

Assessment of the Potential Energy Hypersurfaces in Thymine within Multiconfigurational Theory: CASSCF vs. CASPT2

“…These not only provide the PEHs for mechanistic purposes, but can also yield excited state absorptions [49,50], cationic energies [41], and other related observables with direct experimental counterparts [51,52]. Experimentally, several techniques have been employed to study the photoinduced phenomena of DNA nucleobases, ranging from pump-probe [4,28,[53][54][55], time-resolved infrared [56][57][58][59], photoelectron [17,41,60,61] and recently even Auger spectroscopy [16]. This has allowed postulating different theoretical models to explain the photochemical decay paths of the canonical nucleobases and simulate a range of experimental spectroscopic observables, providing a molecular counterpart.…”

Subnanosecond Emission Dynamics of AT DNA Oligonucleotides

“…[21,22] fs-TAm easurements on the alternating duplex d(AT) 9 ·d(AT) 9 weref irst reportedi n 2005, [23] but were later shown to have been recorded at at emperatureo fa pproximately 40 8Cd ue to heatingb yt he pump laser,a nd not at room temperature as originally stated. [19,21] For this reason,t he fs-TAsignalf rom d(AT) 9 ·d(AT) 9 was re-measured Table 1. Best-fit parametersfor emission decays from (dA) 15 ,d(AT) 9 ·d(AT) 9 ,and the (dA) 10 ·(dT) 10 dumbbell.…”

“…Ground state bleach signals measured by fs-TAe xperiments on DNA strandst ypicallyr ecover biexponentially. [19,29] Af ast component of several picoseconds is assigned to vibrational cooling followingu ltrafast relaxation to the electronic ground state. [19] Additionally,aslow component is observed with al ifetime that can exceed 100 ps.…”

“…[7,18] Consequently,l iterature descriptions of long-lived excited states do not alwaysr efer to the same states. [19] Instead, "long-lived excited states" are often the states with the longest lifetimest hat can be detected by ag iven technique-nanosecondi nt he case of TCSPC studies [8] and subnanosecond for fs-TAe xperiments.A si se vident from their very differentl ifetimes, these states may have little in common.…”