Dipole-Supported Electronic Resonances Mediate Electron-Induced Amide Bond Cleavage

Dissociative electron attachment (DEA) plays a key role in radiation damage of biomolecules under high-energy radiation conditions. The initial step in DEA is often rationalized in terms of resonant electron capture into one of the metastable valence states of a molecule followed by its fragmentation. Our combined theoretical and experimental investigations indicate that the manifold of states responsible for electron capture in the DEA process can be dominated by core-excited (shake-up) dipole-supported resonances. Specifically, we present the results of experimental and computational studies of the gas-phase DEA to three prototypical peptide molecules, formamide, $N$-methylformamide (NMF), and $N$,$N$-dimethyl-formamide (DMF). In contrast to the case of electron capture by positively charged peptides in which amide bond rupture is rare compared to $\mathrm{N}─{\mathrm{C}}_{\alpha }$ bond cleavage, fragmentation of the amide bond was observed in each of these three molecules. The ion yield curves for ions resulting from this amide bond cleavage, such as ${\mathrm{NH}}_2^{-}$ for formamide, ${\mathrm{NHCH}}_3^{-}$ for NMF, and $\mathrm{N}({\mathrm{CH}}_3{)}_2^{-}$ for DMF, showed a double-peak structure in the region between 5 and 8 eV. The peaks are assigned to Feshbach resonances including core-excited dipole-supported resonances populated upon electron attachment based on high-level electronic structure calculations. Moreover, the lower energy peak is attributed to formation of the core-excited resonance that correlates with the triplet state of the neutral molecule. The latter process highlights the role of optically spin-forbidden transitions promoted by electron impact in the DEA process.

Figure 1

Electronic states relevant for DEA processes. (a) Schematic potential energy curves of an initial neutral, dipole-bound state (DBS) and anionic ${\pi }^{*}$ and ${\sigma }^{*}$ states populated upon electron attachment. (b) Electronic configuration of shape and shake-up (core-excited) resonances.

Figure 2

Dissociative electron attachment ion yield curves for formamide (a), NMF (b), and DMF (c). Computed position of ${\pi }^{*}$ resonances (red arrow), thermodynamic thresholds (green), energies of singlet (gray), and triplet (orange) excited states of the neutrals with large enough dipole moment to bind an electron are shown.

Figure 3

EOM-EE-CCSD excitation energies (eV) for five lowest singlet $A^{\prime }$ and $A^{\prime \prime }$ states in formamide. Detachment and attachment densities, and the computed values of dipole moment (a.u.) are also shown [see Sec. S2F of the Supplemental Material for details [27] ].

Figure 4

Schematic electronic configurations of the electron-attached doublet states that correlate with the singlet and triplet excited states of the neutral core.

Figure 5

EOM-SF-CCSD excitation energies (eV) for five lowest triplet $A^{\prime }$ and $A^{\prime \prime }$ states in formamide. Detachment and attachment densities, and the computed values of dipole moment (a.u.) are also shown (see Sec. S2 F of the Supplemental Material for details [27]).