Sub-100-fs energy transfer in coenzyme NADH is a coherent process assisted by a charge-transfer state

Abstract

Excitation energy transfer (EET) is a key photoinduced process in biological chromophoric assemblies. Here we investigate the factors which can drive EET into efficient ultrafast sub-ps regimes. We demonstrate how a coherent transport of electronic population could facilitate this in water solvated NADH coenzyme and uncover the role of an intermediate dark charge-transfer state. High temporal resolution ultrafast optical spectroscopy gives a 54±11 fs time constant for the EET process. Nonadiabatic quantum dynamical simulations computed through the time-evolution of multidimensional wavepackets suggest that the population transfer is mediated by photoexcited molecular vibrations due to strong coupling between the electronic states. The polar aqueous solvent environment leads to the active participation of a dark charge transfer state, accelerating the vibronically coherent EET process in favorably stacked conformers and solvent cavities. Our work demonstrates how the interplay of structural and environmental factors leads to diverse pathways for the EET process in flexible heterodimers and provides general insights relevant for coherent EET processes in stacked multichromophoric aggregates like DNA strands.

Fig. 1. Ultrafast energy transfer in NADH.

Transient absorption (TA) maps of a Adenosine (Ade) and b NADH in piperazine-N,N′-bis(2-ethanesulfonic acid) (PIPES) aqueous buffer upon photoexcitation with sub-20-fs pulses at 4.7 eV. The dashed lines indicate the selected time-traces shown in Fig. 1c, d for detection at 3.1 eV (black dashed line) and 2.5 eV (gray dashed line). c, d Time-traces of Ade (green) and NADH (blue) for probing at c 3.1 eV and d 2.5 eV respectively. The faint gray line in Fig. 1c, d defines the zero line (ΔA = 0). Schematics depicting the ultrafast vibronic processes after Ade resonant excitation which lead to e internal conversion (IC) in Ade and f direct/through-CT coherent EET in NADH. Source data are provided as a Source Data file.

Fig. 2. Ultrafast energy transfer dynamics in highest populated clusters.

a–c Conformational representatives of the three largest clusters of Replica-Exchange Molecular Dynamics. The relative orientation of two chromophores in different clusters is shown through arrows colored blue (on Nic) and red (on Ade). Carbon atoms are colored in green, nitrogens in blue, hydrogens in white, oxygen in red and phosphorus in yellow. Details about clustering and the population of clusters are given in Suppl. Note. 2. d–f Quantum Dynamics (using ML-MCTDH) on a representative structure of the three largest clusters. Additional dynamics on other representative structures are shown in Suppl. Fig. 10. Source data are provided as a Source Data file.

Fig. 3. Stacking and solvent effects on energies of charge-transfer (CT) and locally excited (LE) states.

a The natural transition orbitals of the two LE and lowest CT state involved in the EET process. b The electron-hole distance^, in the Nic→Ade CT state in a representative stacked conformer depicted with a dashed line. The two dots specify the position of the center of charges of hole and electron created in the CT state. c Stacking Effect: Vertical transition energies of the CT state vs the electron-hole distance of the CT state in gas-phase. The black and green bands indicate the energies of Nic* and L_a state which show minimal fluctuation compared to CT state. The Gaussian profile shows the spread of the values of the CT state with FWHM of ca. 1 eV. Two structures with markedly different CT energies are highlighted with black dots for studying solvent effects. d, e Solvent Effect: The effect of the solvent fluctuations on the energies of the diabatic states for the two structures highlighted in (c), which represent respectively a case in which the CT is near degenerate with the L_a-state of Ade (d) and a case in which the CT state is significantly higher in energy (e). The two profiles were obtained by running an equilibrated solvent MD around the two frozen NADH solute geometry and computing vertical transition energies at XMS-CASPT2 level. Details in Suppl. Note. 14.

Fig. 4. Wavepacket dynamics on most populated conformer in 100 equilibrated solvent ensembles.

a An ensemble of equilibrated solvent configurations is created around a representative structure of most populated cluster of the REMD. The solute NADH is kept frozen during the solvent equilibrium dynamics. b–d Populations dynamics in the three diabatic electronic states - L_a (left), CT (middle), Nic* (right) – during the first 200 fs after photoexcitation of the L_a state as a function of the relative energy difference between the CT and L_astates (i.e. E_CT-E_La). The plots are generated from individual ML-MCTDH dynamics performed on 100 snapshots from the solvent equilibrium dynamics as indicated in (a), each one with characteristic solvent-modulated electronic energies, electronic and vibronic couplings. Details on the simulation can be found in Suppl. Note. 14. Source data are provided as a Source Data file.