Nature of frontier quasi-particle states in nitrogen-base systems

TL;DR

This work addresses the photophysical behavior of DNA by predicting frontier quasi-particle (QP) states in nucleobases, Watson-Crick pairs, and Watson-Crick dimers using the optimally tuned AHBR-mRSH* range-separated hybrid with van der Waals corrections. It provides a coherent framework to predict electron-attached and ionized QP energies, dipole/multipole moments, and transition dipoles, revealing that QP-LUMOs are typically dipole- or multipole-trapped and reside away from hydrogen-bond regions, while QP-HOMOs localize on the higher-energy bases. Through thorough classification of WCds into three classes based on dipole and quadrupole characteristics, the study links electrostatics and vdW interactions to QP localization and optical-transition descriptors $\Delta_{LH}$ and $|M_{LH}|^2$, offering a model for DNA reactivity and photo-activity. The findings advance a practical, vdW-inclusive approach for predicting DNA-related photo-damage pathways and provide a foundation for interpreting experimental electron-attachment processes in DNA subsystems.

Abstract

Understanding photophysical properties of DNA is important: It can help us elucidate and probe the impact of charges and free radicals in the cellular environment. For example, a photoemission at a given nucleobase means that we both charge it and place an electron right next to a neighboring part of the genetic code. Inverse photoemission means that we trap a free electron (at some empty state or resonance), and instead emit a low-energy photon. This may reduce the damage if it happens at an already charged base, but it can cause extra damage if it arises somewhere else. Predicting the nature of sudden optically-driven excitations, termed quasi-particles (QPs), help us detail interactions and possibly control the damage that might follow. Also, these QPs contain information on the larger DNA assembly because they reflect the fingerprints of nucleobase polarity, the hydrogen bonding in Watson-Crick pairs, and the van der Waals (vdW) interactions in the Watson-Crick-pair stacking that makes up the genome. In this study, we utilize the recently developed (optimally tuned) range-separated hybrid vdW density functional, AHBR-mRSH* [JPCM 37, 211501 (2025)] to analyze the electron-attached and ionized QP states of these DNA components, with a particular focus on dipole- and multipole-trapped empty states (bound or resonances). We also evaluate critical properties such as dipole and quadrupole moments, QP HOMO-LUMO energy gaps, and transition-dipole moments. Finally, we classify the Watson-Crick stacked dimers based on their QP nature. This classification provides the foundation for proposing a model of DNA reactivity and photo-physical activity.

Figures (10)

• Figure 1: Four nucleobases (colored atoms) comprise the Watson-Crick pair dimer (WCd) attached to the DNA sugar phosphate backbone (gray atoms), viewed from the minor groove. With a nucleobase $L_1$ ($L_2$) in the lower left (right) corner of the base pair step and with nucleobase $L_3$ ($L_4$) in the upper left (right) corner, we label the step $L_1$p$L_3$. This is here exemplified in the figure with C$_1$, G$_2$, G$_3$, and C$_4$, yielding CpG. In the colored sections, red/brown/blue/white balls represent oxygen/carbon/nitrogen/hydrogen atoms, respectively.
• Figure 2: B86R based KS-HOMO/KS-LUMO orbital densities $|\psi_i(\mathbf{r})|^2$: (a) KS-HOMO of G, (b) KS-HOMO of T, (c) KS-LUMO of G and (d) KS-LUMO of T. Yellow and blue isosurfaces correspond to different signs on the wavefunctions $\psi(\mathbf{r})$ (that are evaluated at $k=0$ and have no complex phase).
• Figure 3: Top panel: Spatial mapping of the binding energy-density arising from the nonlocal-correlation term of the AHBR-mRSH* DFA for the TpC system, i.e., a ($36^\circ$ twisted) stacked WCd comprising an A-T and an C-G WC pair. For non-covalently bonded systems like ours, this variation is completely set by the concentration of vdW interactions between different electron density regions, as tracked by the yellow contour (set at $-8.8\times 10^{-5}$ Ry/$a_0^3$). The panel also shows binding-energy density variation in a cut through the TpC stack, with color coding revealed by the left-most bar. Bottom panel: Atomic structure of the TpC stack shown together with the DFT result (black arrow) for the net dipole that it produces; Atom color coding as in Figure 1. Also shown (to a common scale) are our DFT results for dipoles for the isolated A-T and C-G WC pairs forming components of this TpC stack, blue and red arrows, respectively (and again computed in DFT). Since WCds are held by vdW binding, our dipole results for those two WC-pairs suffice to get a reasonable estimate of the dipoles and quadrupoles of any of the WCds, see text and appendix.
• Figure 4: AHBR-mRSH* based frontier orbital densities and dipole moments for the nucleobases. The first/second/third row shows QP-HOMOs/dipole moment/QP-LUMOs. Atom color coding as in Figure 1.
• Figure 5: First/second/third row showing QP-HOMOs/dipole moment/QP-LUMOs for WC pairs, computed in AHBR-mRSH*. Atom color coding as in Figure 1.