Jan Swenson

A unified model of protein dynamics

Protein functions require conformational motions. We show here that the dominant conformational motions are slaved by the hydration shell and the bulk solvent. The protein contributes the structure necessary for function. We formulate a model that is based on experiments, insights from the physics of glass-forming liquids, and the concepts of a hierarchically organized energy landscape. To explore the effect of external fluctuations on protein dynamics, we measure the fluctuations in the bulk solvent and the hydration shell with broadband dielectric spectroscopy and compare them with internal fluctuations measured with the Mössbauer effect and neutron scattering. The result is clear. Large-scale protein motions are slaved to the fluctuations in the bulk solvent. They are controlled by the solvent viscosity, and are absent in a solid environment. Internal protein motions are slaved to the beta fluctuations of the hydration shell, are controlled by hydration, and are absent in a dehydrated protein. The model quantitatively predicts the rapid increase of the mean-square displacement above ≈200 K, shows that the external beta fluctuations determine the temperature- and time-dependence of the passage of carbon monoxide through myoglobin, and explains the nonexponential time dependence of the protein relaxation after photodissociation.

Quasielastic neutron scattering of two-dimensional water in a vermiculite clay

A well-characterized Na–vermiculite clay, containing zero, one, or two molecular layers of water between the clay platelets, has been studied by quasielastic neutron scattering (QENS). Experiments were carried out at a temperature of 300 K in two different scattering geometries; the clay platelets being at 45 and 135° angles to the incident beam in order to make the elastic Q-vector perpendicular and parallel, respectively, to the clay platelets for a scattering angle of 90° (Q≈1.33 A−1). The resulting QENS spectra show that almost no hydrogen motion occurs perpendicular to the clay platelets on the experimental time scale (about 2–40 ps). The two-H2O layer vermiculite exhibits a planar rotational motion of water molecules, forming hydration shells around the Na ions, and a basically two-dimensional translational jump-diffusion motion. The translational motion was modeled using the Gaussian jump-length distribution model, resulting in a mean jump length of 1.1 A and an average residence time of 2.3 ps. Us...

A neutron spin-echo study of confined water

We have investigated the dynamics of confined water in a fully hydrated Na-vermiculite clay using the neutron spin-echo (NSE) technique. NSE measures the intermediate self-scattering function, i.e., the dynamics directly in the time domain. In the present experiments we performed measurements, in the time range 3–3000 ps and temperature ranging from 254 to 323 K, on the essentially two-dimensional water with a layer thickness corresponding to only two molecular layers. The data can be described by the Kohlrausch–Williams–Watts (KWW) stretched exponential function, probably indicating a broad distribution of relaxation times. The reason for the very stretched behavior of the intermediate self-scattering function IS(Q,t), particularly in the supercooled regime, is most likely that the water molecules have widely different local environments. Some water molecules are strongly interacting with the clay surfaces or the intercalated Na+ ions, whereas the remaining molecules are interacting only with other water...

Diffraction and IR/Raman data do not prove tetrahedral water

We use the reverse Monte Carlo modeling technique to fit two extreme structure models for water to available x-ray and neutron diffraction data in q space as well as to the electric field distribution as a representation of the OH stretch Raman spectrum of dilue HOD in D(2)O; the internal geometries were fitted to a quantum distribution. Forcing the fit to maximize the number of hydrogen (H) bonds results in a tetrahedral model with 74% double H-bond donors (DD) and 21% single donors (SD). Maximizing instead the number of SD species gives 81% SD and 18% DD, while still reproducing the experimental data and losing only 0.7-1.8 kJ/mole interaction energy. By decomposing the simulated Raman spectrum we can relate the models to the observed ultrafast frequency shifts in recent pump-probe measurements. Within the tetrahedral DD structure model the assumed connection between spectrum position and H-bonding indicates ultrafast dynamics in terms of breaking and reforming H bonds while in the strongly distorted model the observed frequency shifts do not necessarily imply H-bond changes. Both pictures are equally valid based on present diffraction and vibrational experimental data. There is thus no strict proof of tetrahedral water based on these data. We also note that the tetrahedral structure model must, to fit diffraction data, be less structured than most models obtained from molecular dynamics simulations.

Investigating hydration dependence of dynamics of confined water: Monolayer, hydration water and Maxwell-Wagner processes

The dynamics of water confined in silica matrices MCM-41 C10 and C18, with pore diameter of 21 and 36 A, respectively, is examined by broadband dielectric spectroscopy (10(-2)-10(9) Hz) and differential scanning calorimetry for a wide temperature interval (110-340 K). The dynamics from capillary condensed hydration water and surface monolayer of water are separated in the analysis. Contrary to previous reports, the rotational dynamics are shown to be virtually independent on the hydration level and pore size. Moreover, a third process, also reported for other systems, and exhibiting a saddlelike temperature dependence is investigated. We argue that this process is due to a Maxwell-Wagner process and not to strongly bound surface water as previously suggested in the literature. The dynamics of this process is strongly dependent on the amount of hydration water in the pores. The anomalous temperature dependence can then easily be explained by a loss of hydration water at high temperatures in contradiction to previous explanations.

The protein glass transition as measured by dielectric spectroscopy and differential scanning calorimetry

The glass transition and its related dynamics of myoglobin in water and in a water-glycerol mixture have been investigated by dielectric spectroscopy and differential scanning calorimetry (DSC). For all samples, the DSC measurements display a glass transition that extends over a large temperature range. Both the temperature of the transition and its broadness decrease rapidly with increasing amount of solvent in the system. The dielectric measurements show several dynamical processes, due to both protein and solvent relaxations, and in the case of pure water as solvent the main protein process (which most likely is due to conformational changes of the protein structure) exhibits a dynamic glass transition (i.e. reaches a relaxation time of 100 s) at about the same temperature as the calorimetric glass transition temperature T(g) is found. This glass transition is most likely caused by the dynamic crossover and the associated vanishing of the alpha-relaxation of the main water relaxation, although it does not contribute to the calorimetric T(g). This is in contrast to myoglobin in water-glycerol, where the main solvent relaxation makes the strongest contribution to the calorimetric glass transition. For all samples it is clear that several proteins processes are involved in the calorimetric glass transition and the broadness of the transition depends on how much these different relaxations are separated in time.

Confined Water as Model of Supercooled Water.

Water in confined geometries has obvious relevance in biology, geology, and other areas where the material properties are strongly dependent on the amount and behavior of water in these types of materials. Another reason to restrict the size of water domains by different types of geometrical confinements has been the possibility to study the structural and dynamical behavior of water in the deeply supercooled regime (e.g., 150-230 K at ambient pressure), where bulk water immediately crystallizes to ice. In this paper we give a short review of studies with this particular goal. However, from these studies it is also clear that the interpretations of the experimental data are far from evident. Therefore, we present three main interpretations to explain the experimental data, and we discuss their advantages and disadvantages. Unfortunately, none of the proposed scenarios is able to predict all the observations for supercooled and glassy bulk water, indicating that either the structural and dynamical alterations of confined water are too severe to make predictions for bulk water or the differences in how the studied water has been prepared (applied cooling rate, resulting density of the water, etc.) are too large for direct and quantitative comparisons.

The glass transition and relaxation behavior of bulk water and a possible relation to confined water

Due to the widespread importance of water and the difficulty to study it in the so-called no mans land between 150 and 235 K, deeply supercooled bulk water is currently heavily debated. It speculates about its properties from extrapolations of experimental data on bulk water above 235 K and below 150 K, computer simulations, and experiments on confined water for which the finite size effects may prevent crystallization in the no mans land. However, it is far from obvious how experimental data on bulk water should be extrapolated to the temperature range of the no mans land or how relevant results from computer simulations and studies of confined water are for bulk water. In this paper the structural and dynamical properties of supercooled bulk water are tried to be understood from experimental results on confined water and comparisons with bulk water. We propose that a similar crossover from a high temperature alpha-relaxation to a low temperature beta-relaxation occurs also for bulk water but at a higher temperature than for confined water due to the larger average number of hydrogen bonds between the water molecules in bulk water. In the case of bulk water the crossover is expected to occur around the critical temperature T(s) approximately 228 K when the buildup of an icelike tetrahedral network structure is completed. The proposed interpretation is the simplest one that is able to explain many of the peculiar properties of supercooled water.

Role of solvent for the dynamics and the glass transition of proteins.

For the first time, a systematic investigation of the glass transition and its related dynamics of myoglobin in water-glycerol solvent mixtures of different water contents is presented. By a combination of broadband dielectric spectroscopy and differential scanning calorimetry (DSC), we have studied the relation between the protein and solvent dynamics with the aim to better understand the calorimetric glass transition, T(g), of proteins and the role of solvent for protein dynamics. The results show that both the viscosity related α-relaxation in the solvent as well as several different protein relaxations are involved in the calorimetric glass transition, and that the broadness (ΔT(g)) of the transition depends strongly on the total amount of solvent. The main reason for this seems to be that the protein relaxation processes become more separated in time with decreasing solvent level. The results are compared to that of hydrated myoglobin where the hydration water does not give any direct contribution to the calorimetric T(g). However, the large-scale α-like relaxation in the hydration water is still responsible for the protein dynamics that freeze-in at T(g). Finally, the dielectric data show clearly that the protein relaxation processes exhibit similar temperature dependences as the α-relaxation in the solvent, as suggested for solvent-slaved protein motions.

Water dynamics in n-propylene glycol aqueous solutions

The relaxation dynamics of dipropylene glycol and tripropylene glycol (nPG-n=2,3) water solutions on the nPG-rich side has been studied by broadband dielectric spectroscopy and differential scanning calorimetry in the temperature range of 130-280 K. Two relaxation processes are observed for all the hydration levels; the slower process (I) is related to the alpha relaxation of the solution whereas the faster one (II) is associated with the reorientation of water molecules in the mixture. Dielectric data for process (II) at temperatures between 150 and 200 K indicate the existence of a critical water concentration (x(c)) below which water mobility is highly restricted. Below x(c), nPG-water domains drive the dielectric signal whereas above x(c), water-water domains dominate the dielectric response at low temperatures. The results also show that process (II) at low temperatures is due to local motions of water molecules in the glassy frozen matrix. Additionally, we will show that the glass transition temperatures (T(g)) for aqueous PG, 2PG, and 3PG solutions do not extrapolate to approximately 136 K, regardless of the extrapolation method. Instead, we find that the extrapolated T(g) value for water from these solutions lies in the neighborhood of 165 K.