Time-resolved photoelectron imaging is used to investigate the dynamics of electron attachment and electron interaction with the molecules uracil (U), thymine (T), adenine (A) and imidazole (Im). In this technique, the molecule of interest is clustered with an iodide atom, and a tunable UV photon induces ultrafast electron transfer from iodide to the molecule, forming a transient negative ion with femtosecond time resolution. After a known time delay, a second photon detaches the transient negative ion and the resulting photoelectrons are detected using velocity map imaging. This experimental method allows for insight into how biologically relevant molecules in the gas phase interact with, and accommodate, an excess electron, an important question in radiation biology.
Uracil and thymine interact similarly with excess electrons. We observe two different electron attachment motifs, dependent on the pump pulse excitation energy that induces charge transfer from the iodide atom. The vertical detachment energy (VDE) of the iodide-uracil cluster is 4.11 ± 0.05 eV and 4.05 ± 0.05 eV for the iodide-thymine cluster. Excitation of the clusters with photon energies of approximately 500-700 meV above the I-U and I-T VDEs results in electrons with approximately 500-700 meV of kinetic energy that scatter directly into the valence-bound orbitals of uracil and thymine, forming the valence bound anion. Using lower excitation energies, between 120 meV below the VDE and 110 meV above the I-U and I-T VDEs, the I-T anion ground state is photoexcited to an anion state where the excess electron is bound in a dipole-bound (DB) anion state by the dipole moment of the cluster. Due to a changing photodetachment cross-section of the uracil and thymine DB anion from geometry relaxation at early times, the DB photoelectron signal has a rise-time longer than the cross-correlation of the pump and probe pulses. Subsequently, a small population of the uracil and thymine DB anions transition to the valence-bound (VB) anions, in agreement with theoretical predictions. However, no participation of the uracil or thymine DB anion is observed in the formation of the respective VB anion at excitation energies 500-700 meV above the I-U/T VDEs, contrary to experiments that invoked participation of the dipole-bound anions to explain features in the dissociative electron attachment spectra.
The uracil and thymine DB and VB anions ultimately decay through a variety of mechanisms. In the lower excitation energy region, both the DB and VB anions of uracil and thymine decay bi-exponentially at all of the excitation energies studied. The decay lifetimes range between 2 to 25 ps for the short decay lifetime and 30-2000 ps for the long decay lifetime, depending on excitation energy and anion state. In the higher excitation energy region, the thymine VB anion signal decays completely by 10 ps, unlike uracil that has a bi-exponential long-time lifetime that persists until at least 100 ps. The bi-exponential decays for the DB and VB anions of uracil and thymine are attributed to various mechanisms depending on the molecule and excitation energy including: different rates of autodetachment prior and subsequent to iodine loss, and non-statistical autodetachment versus statistical autodetachment.
Experiments investigating the electron attachment dynamics to adenine show evidence of multiple tautomers of adenine participating in the dynamics. Excitation from the ground state I-A anion cluster to the iodine-adenine DB anion, is induced with excitation energies near the 3.96 ± 0.05 eV VDE of the I-A9 canonical tautomer. The DB anion of adenine is initially formed with a ~250 fs rise-time due to a changing photodetachment cross-section correlated with relaxation of the cluster geometry from the Franck-Condon region, as is observed in uracil and thymine. The DB anion undergoes a complete ultrafast transition to the VB anion at some excitation energies, and a partial transition at other excitation energies. However, electronic structure calculations do not predict a stable valence bound anion of the A9 canonical tautomer of adenine, and the relative intensities of the dipole-bound and valence-bound anions and the dipole-bound anion decay lifetimes display non-monotonic trends. These dynamics are consistent with two tautomers present in the ion beam clustered to iodide, the A9 canonical tautomer and the A3 non-canonical tautomer. The DB to VB transition is due to the A3 tautomer. The A3 tautomer is calculated to support a VB anion with an exothermic transition from the DB to VB state. The A9 canonical tautomer however only supports an excess electron in a DB orbital and the DB anion is formed in a narrower excitation energy range than the A3 tautomer, causing the non-monotonic trends in the dipole-bound and valence-bound anion intensity ratios and dipole-bound anion decay lifetimes.
Imidazole, like the A9 tautomer of adenine, only supports an excess electron in a DB orbital. The VDE of the iodide-imidazole binary cluster is 3.90 ± 0.05 eV. With excitation energies just below 3.90 eV, the ground state I-Im cluster is excited to the I Im-(DB) anionic excited state with an ultrafast rise-time due to geometry changes in the [I Im]- cluster. The DB state decays multi-exponentially with decay dynamics that change rapidly with small changes in the excitation energy. These dynamics suggest that the degree of vibrational excitation in the dipole-bound cluster considerably effects the decay dynamics of the transient [I Im]- ion.
Overall, the systems studied provide a wide picture of the various ways that biologically relevant molecules can interact with, and accommodate, excess charge in dipole- and valence-bound anion states, and the various ways that iodide(iodine) can influence the observed dynamics, through the rise time of the dipole-bound state and the decay of both dipole- and valence-bound anions. A detailed understanding of the electron kinetic energy dependent mechanisms of electron attachment in nucleobases, and any subsequent dipole-bound anion to valence-bound anion transition, is crucial for understanding the various mechanisms of low-energy electron damage to DNA.