Hydrated Excess Protons Can Create Their Own Water Wires

Abstract

Grotthuss shuttling of an excess proton charge defect through hydrogen bonded water networks has long been the focus of theoretical and experimental studies. In this work we show that there is a related process in which water molecules move ("shuttle") through a hydrated excess proton charge defect in order to wet the path ahead for subsequent proton charge migration. This process is illustrated through reactive molecular dynamics simulations of proton transport through a hydrophobic nanotube, which penetrates through a hydrophobic region. Surprisingly, before the proton enters the nanotube, it starts "shooting" water molecules into the otherwise dry space via Grotthuss shuttling, effectively creating its own water wire where none existed before. As the proton enters the nanotube (by 2-3 Å), it completes the solvation process, transitioning the nanotube to the fully wet state. By contrast, other monatomic cations (e.g., K(+)) have just the opposite effect, by blocking the wetting process and making the nanotube even drier. As the dry nanotube gradually becomes wet when the proton charge defect enters it, the free energy barrier of proton permeation through the tube via Grotthuss shuttling drops significantly. This finding suggests that an important wetting mechanism may influence proton translocation in biological systems, i.e., one in which protons "create" their own water structures (water "wires") in hydrophobic spaces (e.g., protein pores) before migrating through them. An existing water wire, e.g., one seen in an X-ray crystal structure or MD simulations without an explicit excess proton, is therefore not a requirement for protons to transport through hydrophobic spaces.

Figure 1

Simulations of ion transport through an originally “dry” nanotube as described in the text. (a) Construct of the simulation system. The armchair-type (6,6) CNT structure is assembled between two graphene single layers that separate the bulk water. (b) Overview of the proton induced wetting process along with the motion of the excess proton from bulk–tube interface into about 4 Å of the nanotube. (c) Real-time densities traces of the channel water molecules starting from a partially dry nanotube with the existence of the excess proton. Each bright line can represent the trace of the oxygen atom in a water molecule. (d) Simulation with the K⁺ inside the nanotube, which remains mostly dry.

Figure 2

Free energy profiles of the ion permeation and the water occupancy in different simulation systems. (a) Free energy profiles from the permeations of different cations. The free energy of H⁺ (the hydrated excess proton) has much lower energy barrier than the others, displaying the unique features of the excess H⁺. (b) Free energy profiles of the water occupancy with the H⁺ charge defect (green), K⁺ (red), or classical H₃O⁺ (yellow) fixed at Z = 12.0 Å (2–3 Å inside the mouth of the nanotube), compared to the result without the ions present (blue). The induced wetting process is only seen in the system with H⁺. The average errors are (a) ±0.45 kcal/mol and (b) ±0.30 kcal/mol calculated from 500 ps block averages.

Figure 3

2D free energy surface of the proton induced wetting process. The horizontal axis represents the Z-position of the hydrated excess proton charge defect, while the vertical axis represents the level of CNT water occupancy. The white dotted line (Z = 14.7 Å) indicates the position of the graphene layer and the mouth of the nanotube. A stepwise but coupled mechanism can be observed from the 2D free energy surface, in which three steps, trapping–wetting–permeation, are highlighted by yellow dashed arrows. The average errors are ±0.35 kcal/mol.

Figure 4

1D free energy profiles extracted from the 2D free energy surface in Figure 3. (a) Free energy profiles of the wetting process when the excess proton charge defect is located at different positions along the nanotube axis. (b) Free energy profiles of proton permeation while the nanotube is in different hydration states where NC is defined as the number of confined waters in the nanotube. The average errors are ±0.35 kcal/mol.

Figure 5

2D free energy surfaces for (a) a K⁺ cation and (b) a “classical” H₃O⁺ (non-Grotthuss shuttling) cation showing the free energy for ion permeation relative to nanotube water occupancy and prepared in the same way as for Figure 3. The average errors are ±0.35 kcal/mol.