Water makes the proton tremble - ultrafast movements and short-lived structures of hydrated protons

Protons in an aqueous environment play a key role in many chemical and biological processes. In Science, Dahms et al. on the direct recording of ultrafast proton motions by means of vibrational spectroscopy. They show that protons in water are predominantly bound between two water molecules, where they perform fluctuating movements in the femtosecond range. This dynamics is 10 to 50 times faster than the hopping of the proton into a new environment, the elementary step of proton migration in chemistry.

The proton, the positively charged nucleus H+ of the hydrogen atom and the smallest chemical entity, plays a key role in chemistry and biology. Acids release protons into an aqueous environment in which they are highly mobile and dominate the transport of electrical charge. In biological systems, the concentration gradient of protons across cell membranes is the driving force of cell respiration and energy storage. Even after decades of intensive research, however, the molecular geometries of the proton in water and the elementary processes of proton dynamics have remained highly controversial.

Protons in water are usually described by the two boundary structures shown in Fig. 1A. In the so-called self-complex (H9O4+) (left), the proton is part of the central H3O+ molecule, which is surrounded by three water molecules. In the Zundel cation (H5O2+) (right), the proton forms two strong hydrogen bonds with two adjacent water molecules. To describe these systems at the molecular level, the energy potential surface of the proton is used (Figure 1B), which clearly differs for the two geometries. For the self-complex one expects an anharmonic potential with a minimum while the Zundelgeometrie should have a double minimum potential. In water, such potentials are highly dynamic and fluctuate on fast timescales, a behavior caused by thermal movements of the surrounding water molecules and the proton.

Fig.1. Chemical structure of hydrated protons in water. A Schematic representation of the self-cation H9O4+ (left) and of the Zundel cation H5O2+ (right). The arrows mark the coordinate r of the O-H bond and the (O ... H + ... O) proton transfer coordinate z. In the self-cation, the proton is localized by a covalent O-H bond while it is delocalized in the Zundel cation between the two water molecules. B Anharmonic vibrational potential (left) and double-minimum potential of the Zundel cation along the coordinate z (right, red line). The double-minimum potential is distorted by the action of the liquid environment (right, dotted line). The red and blue arrows mark transitions between the quantum states of the proton, red arrows from the ground to the first excited state, and blue arrows from the first to the second excited state. A modulation of the potential surfaces changes the distance of the quantum states and thus the energy of the vibration transitions which is detected by two-dimensional vibration spectroscopy.

Scientists from the Max Born Institute in Berlin and the Ben Gurion University of the Negev in Beer-Sheva, Israel, have now visualized the ultra-fast movements and transient structures of protons in water under ambient conditions. They report experimental and theoretical results in the journal Science (doi: 10.1126 // science.aan5144), which identify the Zundel cation as the predominant species in water. The femtosecond dynamics of the proton motions (1 fs = 10-15 s) were recorded in real time by means of the vibrational transitions between the quantum states of the proton (red and blue arrows in Fig. 1B). The particularly meaningful method of two-dimensional vibration spectroscopy provides the yellow-red and blue contours in Fig. 2A, which characterize the energy range of the two transitions. The blue contour is at higher detection frequencies than the yellow-red one. This result represents the first direct demonstration of the double minimum character of the proton potential (Figure 1B, right) in a native aqueous environment. If the proton were bound in a potential with a minimum (Figure 1B, left), the blue contour would appear at smaller detection frequencies as the yellow-red.

Fig. 2. Femtosecond dynamics of the proton movement (1 fs = 10-15 s). A Two-dimensional vibration spectrum with the transition from the ground to the first excited state (yellow-red contour) and from the first to the second excited state (blue contour). The alignment of the two contours along the axis of the excitation frequency is caused by ultrafast frequency fluctuations and memory loss in the proton position. B Theoretically calculated real-time dynamics of the proton in the Zundel cation. Within less than 100 fs, the proton experiences large deflections along the z-coordinate connecting the two water molecules. Due to the ultrafast modulation of the potential through the surrounding water molecules, the proton temporarily assumes all positions along z.

The alignment of both contours along the vertical frequency axis shows that both oscillations pass through a huge frequency range within less than 100 fs. This is a direct consequence of the ultrafast modulation of the potential surface by the environment. In other words, the proton temporarily takes all of the positions between the two water molecules within less than 100 fs and quickly loses the memory of where it was just before. The modulation of the proton potential is caused by strong electric fields, which exert the water molecules of the environment on the Zundel cation. Their rapid thermal motion leads to strong field fluctuations and modulations of the potential surface in the time range below 100 fs. This picture is supported by reference experiments with selectively prepared Zundel cations in other solvents and by detailed theoretical simulations of proton dynamics (Figure 2B).

Fig 3. Illustration of the dynamics of hydrated protons in a picture of classical physics. The proton smiley sits in the middle of a two seat sofa. When the sofa is raised or lowered by a mechanical force, the shape of the seat changes and the proton moves back and forth on the sofa. These movements occur in the real system on a timescale below 100 fs (10-13 s). After an average time of about 1 ps = 1000 fs = 10-12 s the sofa shatters and the proton moves to a new place. The new sofa consists of a part of the old (blue) and a new part (red).

A proton in a single Zundel cation in water changes into a new local environment through the breaking and reconstruction of hydrogen bonds. These processes are much slower than the proton's dithering motion and run in the time range of a few picoseconds (1 ps = 1000 fs = 10-12 s). The new picture of proton dynamics presented here is of crucial importance for an understanding of proton transport through the famous von Grotthuss mechanism and for proton shifts in biological systems.

Original publication

Large-amplitude transfer motion of hydrated excess protons mapped by ultrafast 2D IR spectroscopy

F. Dahms, B. P. Fingerhut, E. T. J. Nibbering, E. Pines, T. Elsaesser

Science 357 (2017) 491–495