State- and time-resolved observation of ultrafast intermolecular proton transfer in hydrated biomolecules

Abstract

Proton transfer underpins number of chemical and biochemical processes, yet its sub-100 fs dynamics have rarely been captured in real time. Here, we report direct and time-resolved observation of ionizing radiation-induced proton transfer in a heteroaromatic hydrate: the pyrrole-water complex. Both the electron-impact and strong-field laser experiments create a locally and doubly charged pyrrole unit (C₄H₅N²⁺), which immediately (within 60 fs) donates a proton to the adjacent H₂O, generating deprotonated C₄H₄N⁺ and hydronium H₃O⁺ cations that subsequently undergo Coulomb explosion. The electron-impact experiments directly revealed initial states and provided dynamical insights through fragment ions and electron coincidence momentum imaging. The strong-field femtosecond laser experiments tracked the ultrafast dynamics of proton transfer; complementary ab initio calculations unraveled the dynamical details. The 50-60 fs proton transfer qualifies as one of the fastest acid-base reactions observed to date. This study offers a novel perspective on radiation-induced proton transfer in hydrated biomolecules.

Fig. 1. Schematic of COLTRIMS reaction microscope upon electron-impact and proton transfer pathway of H₃O⁺ + C₄H₄N⁺ and measured TOF correlation spectrum.

a The local double ionization of C₄H₅N-H₂O complex upon electron-impact. The dots between water and pyrrole denote intermolecular H-bond; b Proton transfer from doubly ionized C₄H₅N²⁺ to H₂O molecule; Atomic colors: C (gray), H (white), N (blue). c Schematic diagram of the COLTRIMS setup. Purple, red, blue and turquoise lines respectively represent UV laser, ions, electrons and gas jet. The black arrows represent the directions of electric and magnetic fields. d Measured TOF correlation map between the first and the second cations. The cyan and green arrows represent the direct dissociation H₂O⁺+C₄H₅N⁺ and the proton transfer H₃O⁺+C₄H₄N⁺ channels, respectively. The vertical and horizontal lines are from false coincidence. The count intensity is color-coded on a linear scale. Source data are provided as a Source Data file.

Fig. 2. Projectile energy loss and KER spectra.

a Projectile energy loss spectrum for the proton transfer channel H₃O⁺ + C₄H₄N⁺. The vertical dashed line represents the double-ionization threshold of the hydrated pyrrole complex. b, c Measured and (d, e) calculated KER for the proton transfer channel H₃O⁺ + C₄H₄N⁺. The solid (b) and hollow dots (c), as well as solid (d) and hollow (e) bars, represent the results of electron-impact and laser experiments, AIMD and CASPT2 theoretical calculations, respectively. Error bars in (a–c) represent statistical standard deviation (s.d.), and were calculated by the square root of the true coincidence counts. Source data are provided as a Source Data file.

Fig. 3. Molecular dynamics simulation diagrams.

a The rigid two-dimensional potential energy surface scan in triplet ground state, calculated with the CCSD/aug-cc-pVDZ method. A white curve with arrows describes the minimum-energy path toward proton transfer and subsequent Coulomb explosion. b, c Evolution of interatomic distances analyzed from AIMD simulation in triplet ground state using the B3LYP/cc-pVDZ method. Distances between O and N atoms (r_O−N) (b) and distances between O atom and H atom on pyrrole molecule (r_O−H) (c) as functions of time. d Reaction channel evolution for surface hopping starting from state T₀ with the localized charge on pyrrole molecule. The channel analysis focused on the dissociation of water molecules, and PT followed by dissociation. Other channels, such as dissociation of the hydrogen atom, were not observed. Channel ratio refers to the proportion of the dissociation events of the ground state hydrated pyrrole dication that occur via different channels. e, f Evolution of interatomic distances analyzed from the surface hopping simulation in triplet ground state for r_O−N (e) and r_O−H (f) as functions of time. The black solid curves in (b, c) and (e, f) represent the average data of all the trajectories. Source data are provided as a Source Data file.

Fig. 4. Femtosecond tracking of proton transfer dynamics.

a Calculated time-dependent yield of the PT channel. The yield is fitted with a growth function (pink dashed line), giving a PT time constant of τ = 52.8  ± 0.5 fs. b Schematic of the laser pump-probe experiment. Black, red, and purple arrows represent the 800 nm pump, 800 nm probe, and 400 nm probe, respectively. Black, blue, red and purple shadows represent wave packets on the PECs of C₄H₅N-H₂O, C₄H₅N²⁺-H₂O, C₄H₅N⁺-H₂O⁺, and C₄H₄N⁺-H₃O⁺. Red shadows at 3.1 eV and 3.9 eV delineated by black dotted lines represent the expected KER of the 800 nm pump - 800 nm probe and 800 nm pump - 400 nm probe schemes, respectively. c H₂O⁺ + C₄H₅N⁺ yields versus pump-probe time delay, which are smoothed with a moving average. The PT times τ₁ = 34  ± 5 fs and τ₂ = 31  ± 6 fs are determined by fitting with decay functions (pink/purple dashed lines). The orange line shows the instrument response function (IRF). d Time delay-dependent KER distribution. Dashed box highlights the 3.9 eV transient. e Time-dependent yield curve for the direct dissociation channel at KER  ~ 3.9 eV in the case of 800 nm pump - 400 nm probe. The PT time τ = 55  ± 24 fs is determined by fitting with decay functions. Error bars represent statistical s.d., and were calculated by the square root of the true coincidence counts. The PECs (blue, red, and purple solid curves) in (b) are calculated using constrained DFT with Configurational Interaction approach and the B3LYP/aug-cc-PVTZ method. Source data are provided as a Source Data file.