Towards tunable exciton delocalization in DNA Holliday junction-templated indodicarbocyanine 5 (Cy5) dye derivative heterodimers

Abstract

We studied the exciton delocalization of indodicarbocyanine 5 dye derivative (Cy5-R) heterodimers templated by a DNA Holliday junction (HJ), which was quantified by the exciton hopping parameter J_m,n. These dyes were modified at the 5 and 5' positions of indole rings with substituent (R) H, Cl, tBu, Peg, and hexyloxy (Hex) groups that exhibit different bulkiness and electron-withdrawing/donating capacities. The substituents tune the physical properties of the dyes, such as hydrophobicity (log P) and solvent-accessible surface area (SASA). We tuned the J_m,n of heterodimers by attaching two Cy5-Rs in adjacent and transverse positions along the DNA-HJ. Adjacent heterodimers exhibited smaller J_m,n compared to transverse heterodimers, and some adjacent heterodimers displayed a mixture of H- and J-like aggregates. Most heterodimers exhibited J_m,n values within the ranges of the corresponding homodimers, but some heterodimers displayed synergistic exciton delocalization that resulted in larger J_m,n compared to their homodimers. We then investigated how chemically distinct Cy5-R conjugated to DNA can interact to create delocalized excitons. We determined that heterodimers involving Cy5-H and Cy5-Cl and a dye with larger substituents (bulky substituents and large SASA) such as Cy5-Peg, Cy5-Hex, and Cy5-tBu resulted in larger J_m,n. The combination provides steric hindrance that optimizes co-facial packing (bulky Cy5-R) with a smaller footprint (small SASA) that maximizes proximity. The results of this study lay a groundwork for rationally optimizing the exciton delocalization in dye aggregates for developing next-generation technologies based on optimized exciton transfer efficiency such as quantum information systems and biomedicine.

Fig. 1. Schematic illustration of electronic transitions of (A) homodimer (m = n) and (B) heterodimers (m ≠ n) relative to their monomers m and n as described by molecular exciton theory. The formation of dye aggregates induces exciton delocalization splitting into higher and lower excited energy states (E⁺ and E⁻) relative to the corresponding monomers. The transition into a higher- (lower-) energy excitonic state is forbidden for J- (H-) aggregates, respectively (dot arrows). In the dye structure, dots (purple and blue) represent modified substituents of Cy5-R in 5 and 5′ positions of indole rings and the arrow represents the TDM orientation.

Fig. 2. Schemes of the Cy5-R structure with attachments in the DNA Holliday junction (DNA-HJ). (A) Scheme of the chemical structure of Cy5-R, within the DNA backbone. The arrow inside the Cy5-R structure represents the transition dipole moment (TDM), and R indicates the 5- and 5′- positions of the indolenine rings where substituents are placed. (B) Schematic structure of R substituents. (C) Cy5-R dye combinations to form heterodimers (Cy5 R_m–R_n) of Cy5 derivatives. (D) Schematic representation of monomers, and adjacent AB and transverse AC heterodimers templated by DNA Holliday junction (DNA-HJ).

Fig. 3. Optical properties of Cy5-R monomers templated by DNA-HJ. (A) Molar extinction coefficient (ε in M⁻¹ cm⁻¹) of Cy5-R determined using the absorption spectra of monomers. (B) Emission intensity of monomers normalized to absorptance at 630 nm excitation wavelength. Measurements were performed in 1xTAE + 15 mM MgCl₂ buffer solution. Shadow in (A) and (B) depicts the variation range of spectra intensity exhibited by the monomers A, B, C, and D templated by DNA-HJ, and values indicate the location of the maximum peak wavelength.

Fig. 4. Optical characterization of the representative (A)–(C) adjacent Cy5 H–Hex AB and (D)–(F) transverse Cy5 H–Hex AC heterodimers templated by a DNA Holliday junction (DNA HJ). The experimental (A) and (D) absorption and (B) and (E) circular dichroism (CD) spectra of heterodimers were converted into molar extinction coefficient units (ε M⁻¹ cm⁻¹). The experimental absorption and CD spectra were modeled (dashed line) using a method based on Kühn–Renger–May approach (KRM model). (C) and (F) Plots of excitation and emission spectra of heterodimer (lines) and absorption spectra of monomers and heterodimer (shadow). The excitation and emission spectra were measured at fixed wavelengths of 740 and 615 nm, respectively. See the spectra of all heterodimers of the present study in Section S3 (ESI†).

Fig. 5. (A) Schematic representation of dyes in dye aggregates (TDM: transition dipole moments of dyes, α_m,n: angle between TDM of dyes, d_m,n: minimum distance between dyes, R_m,n: center-to-center dye distance Θ: slip angle of dyes m and n, and Θ_t: twist angle). (B) Representation of a 3D plot of TDM of dyes (blue arrows) projected to XY, YZ, and XZ planes (black arrows) resulting from KRM modeling. (C) Exciton hopping parameter (J_m,n), (E) R_m,n, and (G) α_m,n of adjacent heterodimers, and (D) J_m,n, (F) R_m,n, and (H) α_m,n of transverse heterodimers resulted from KRM modeling. Data with an asterisk (*) in the heat plot indicate that the heterodimer has subpopulations and the depicted values correspond to the dimer with a larger J_m,n. See details of KRM modeling parameters and results in Section S4 (ESI†).

Fig. 6. Relationship between hydrophobicity (log P) and exciton hopping parameter (J_m,n) of adjacent (A–C) and transverse (D–F) heterodimers. log P of heterodimers is the average value of the two participant dyes in the aggregates. The outliers in the analysis are describes in Section 3.3 of the main text. See analysis for Cy5 Peg–R, Cy5 Hex–R, and the relationship of J_m,n with other properties of Cy5-R in Section S6 (ESI†).

Fig. 7. Transient absorption spectra of (a) Cy5 H–Hex AC transverse and (b) Cy5 H–Hex AB adjacent dimer measured 1 ps after photoexcitation at wavelengths chosen to photoselect any H-like or J-like geometry subpopulations. The excitation wavelengths are indicated and color coded.