Ultraviolet radiation (UVR) from the sun is essential for the prebiotic syntheses of nucleotides, but it can also induce photolesions such as the cyclobutane pyrimidine dimers (CPDs) to RNA or DNA oligonucleotide in prebiotic Earth. 2,6-Diaminopurine (26DAP) has been proposed to repair CPDs in high yield under prebiotic conditions and be a key component in enhancing the photostability of higher-order prebiotic DNA structures. However, its electronic relaxation pathways have not been studied, which is necessary to know whether 26DAP could have survived the intense UV fluxes of the prebiotic Earth. We investigate the electronic relaxation mechanism of both 26DAP and its 2′-deoxyribonucleoside (26DAP-d) in aqueous solution using steady-state and femtosecond transient absorption measurements that are complemented with electronic-structure calculations. The results demonstrate that both purine derivatives are significantly photostable to UVR. It is shown that upon excitation at 287 nm, the lowest energy 1 ππ* state is initially populated. The population then branches following two relaxation coordinates in the 1 ππ* potential energy surface, which are identified as the C2- and C6-relaxation coordinates. The population following the C6-coordinate internally converts to the ground state nonradiatively through a nearly barrierless conical intersection within 0.7 ps in 26DAP or within 1.1 ps in 26DAP-d. The population that follows the C2-relaxation coordinate decays back to the ground state by a combination of nonradiative internal conversion via a conical intersection and fluorescence emission from the 1 ππ* minimum in 43 ps and 1.8 ns for the N9 and N7 tautomers of 26DAP, respectively, or in 70 ps for 26DAP-d. Fluorescence quantum yields of 0.037 and 0.008 are determined for 26DAP and 26DAP-d, respectively. Collectively, it is demonstrated that most of the excited state population in 26DAP and 26DAP-d decays back to the ground state via both nonradiative and radiative relaxation pathways. This result lends support to the idea that 26DAP could have accumulated in large enough quantities during the prebiotic era to participate in the formation of prebiotic RNA or DNA oligomers and act as a key component in the protection of the prebiotic genetic alphabet.
more »
« less
Excited state dynamics of 2′-deoxyisoguanosine and isoguanosine in aqueous solution
Photostability is thought to be an inherent property of nucleobases required to survive the extreme ultraviolet radiation conditions of the prebiotic era. Previous studies have shown that absorption of ultraviolet radiation by the canonical nucleosides results in ultrafast internal conversion to the ground state, demonstrating that these nucleosides efficiently dissipate the excess electronic energy to the environment. In recent years, studies on the photophysical and photochemical properties of nucleobase derivatives have revealed that chemical substitution influences the electronic relaxation pathways of purine and pyrimidine nucleobases. It has been suggested that amino or carbonyl substitution at the C6 position could increase the photostability of the purine derivatives more than the substitution at the C2 position. This investigation aims to elucidate the excited state dynamics of 2′-deoxyisoguanosine (dIsoGuo) and isoguanosine (IsoGuo) in aqueous solution at pH 7.4 and 1.4, which contain an amino group at the C6 position and a carbonyl group at the C2 position of the purine chromophore. The study of these derivatives is performed using absorption and emission spectroscopies, broadband transient absorption spectroscopy, and density functional and time-dependent density functional levels of theory. It is shown that the primary relaxation mechanism of dIsoGuo and IsoGuo involves nonradiative decay pathways, where the population decays from the S 1 (ππ*) state through internal conversion to the ground state via two relaxation pathways with lifetimes of hundreds of femtoseconds and less than 2 ps, making these purine nucleosides photostable in aqueous solution.
more »
« less
- Award ID(s):
- 1800052
- NSF-PAR ID:
- 10336278
- Date Published:
- Journal Name:
- Physical Chemistry Chemical Physics
- Volume:
- 24
- Issue:
- 11
- ISSN:
- 1463-9076
- Page Range / eLocation ID:
- 6769 to 6781
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Today’s genetic composition is the result of continual refinement processes on primordial heterocycles present in prebiotic Earth and at least partially regulated by ultraviolet radiation. Femtosecond transient absorption spectroscopy and state-of-the-art ab initio calculations are combined to unravel the electronic relaxation mechanism of pyrimidine―the common chromophore of the nucleobases. Excitation of pyrimidine at 268 nm populates the S1(nπ*) state directly. A fraction of the population intersystem crosses to the triplet manifold within 7.8 ps, partially decaying within 1.5 ns, while another fraction recovers the ground state in >3 ns. The pyrimidine chromophore is not responsible for the photostability of the nucleobases. Instead, C2 and C4 amino and/or carbonyl functionalization is essential for shaping the topography of pyrimidine’s potential energy surfaces, which present accessible conical intersections between the initially populated electronic excited state and the ground state.more » « less
-
null (Ed.)Minor structural modifications to the DNA and RNA nucleobases have a significant effect on their excited state dynamics and electronic relaxation pathways. In this study, the excited state dynamics of 7-deazaguanosine and guanosine 5′-monophosphate are investigated in aqueous solution and in a mixture of methanol and water using femtosecond broadband transient absorption spectroscopy following excitation at 267 nm. The transient spectra are collected using photon densities that ensure no parasitic multiphoton-induced signal from solvated electrons. The data can be fit satisfactorily using a two- or three-component kinetic model. By analyzing the results from steady-state, time-resolved, computational calculations, and the methanol–water mixture, the following general relaxation mechanism is proposed for both molecules, Lb → La → 1πσ*(ICT) → S0, where the 1πσ*(ICT) stands for an intramolecular charge transfer excited singlet state with significant πσ* character. In general, longer lifetimes for internal conversion are obtained for 7-deazaguanosine compared to guanosine 5′-monophosphate. Internal conversion of the 1πσ*(ICT) state to the ground state occurs on a similar time scale of a few picoseconds in both molecules. Collectively, the results demonstrate that substitution of a single nitrogen atom for a methine (C–H) group at position seven of the guanine moiety stabilizes the 1ππ* Lb and La states and alters the topology of their potential energy surfaces in such a way that the relaxation dynamics in 7-deazaguanosine are slowed down compared to those in guanosine 5′-monophosphate but not for the internal conversion of 1πσ*(ICT) state to the ground state.more » « less
-
This work scrutinizes the relaxation mechanism of 2-oxopurine. Contrary to its ancestor, purine, which is a UVC chromophore, 2-oxopurine shows a red-shifted absorption spectrum centered in the UVA region. In 2-oxopurine, relaxation along the ππ* spectroscopic state directs the population from the Franck–Condon (FC) region towards a minimum, which acts as a crossroad for the further decay of the system either to triplet states or, alternatively, to the ground state through a C 6 -puckered S 1 /S 0 funnel. A comparison of the optical properties and excited state potential energy surfaces of purine, 2-oxopurine, 2-aminopurine, 6-oxopurine and adenine, allows establishing how the position and nature of substituent tune the photophysics of purine. For this series, we conclude that both C 2 and C 6 substitution redshift the absorption spectrum of purine, with 2-oxo substitution exhibiting the largest shift. An important exception is the canonical nucleobase adenine, which presents a blue shifted absorption spectrum. The topography of purine's ππ* potential energy surface experiences major changes when functionalized at the C 6 position. In particular, the disappearance of the minimum along the ππ* potential energy surface efficiently funnels the excited state population from the FC region to the ground state and increases the photostability of 6-aminopurine (adenine) and 6-oxopurine (hypoxanthine) nucleobases.more » « less
-
The substitution of an oxygen atom in an exocyclic carbonyl group of the nucleobases by a sulfur atom in a nucleic acid base generates a thiobase. This substitution causes a redshift in the absorption spectrum of the thiobase with respect to the canonical nucleobase, moving the strongly allowed absorption band from the UVC to the UVA region of the electromagnetic spectrum. Due to this redshift and the efficient population of the triplet state, 4-thiothymidine (4tThd) can be selectively excited without exciting canonical DNA, making it a powerful UVA photosensitizer. The synergistic toxicity of 4tThd and UVA radiation allows for the enhanced killing of skin cancer cells. As a result, 4tThd has been proposed for use in conjunction with UVA radiation as potential photodynamic therapy agent, due to its photochemical properties and to a diminished cytotoxicity. Studies of the monomer 4tThd have been performed to explore the prospective use of 4tThd in photochemotherapeutic application with reduced phototoxic side effects. One study of 4tThd in aqueous solution proposed the main kinetic mechanism to consist of intersystem crossing from the S2 state to the triplet manifold. Vertical excitation energies were calculated using the optimized ground state of 4tThd in water and vacuum. These were found to be in good agreement with the values previously reported. After studying the monomer, the next step is to understand what happens when 4tThd interacts with the DNA bases. Therefore, ground state optimizations and vertical excitation energies calculations were performed for a series of 4tThd-containing dinucleotides. These vertical excitation energy calculations predict the order electronic states and likely kinetic mechanisms when 4tThd is incorporated into DNA, which will greatly assist in the interpretation of planned time-resolved experiments.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1039/D1CP05795B
