Formation of Spanning Water Networks on Protein Surfaces via 2D Percolation Transition (original) (raw)
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Percolation Transition of Hydration Water: From Planar Hydrophilic Surfaces to Proteins
Physical Review Letters, 2005
The formation of a spanning hydrogen-bonded network of hydration water is found to occur via a 2D percolation transition in various systems: smooth hydrophilic surfaces, the surface of a single protein molecule, protein powder and diluted peptide solution. The average number of water-water hydrogen bonds nH at the percolation threshold varies from 2.0 to 2.3, depending on temperature, system size and surface properties. Calculation of nH allows an easy estimation of the percolation threshold of hydration water in various systems, including biomolecules. PACS numbers: 61.20Ja, 64.60Ak, 87.15Aa The existence of a spanning network of hydration water in biosystems enables their biological functions . With increasing hydration level, an ensemble of finite (non-spanning) clusters of hydration water transforms via a quasi-2D percolation transition into a state with a spanning water network . The full dynamics of biomolecules is restored, when they are covered by about a "monolayer" of water. The first appearance of such a "monolayer" corresponds to a quasi-2D percolation transition of the hydration water at the surface of a single biomolecule . Simulation studies of various properties of hydrated biosystems below and above the percolation threshold of the hydration water can help to clarify the role of the spanning water network in the onset of biological functions. Such studies require the knowledge of the percolation threshold of water in the system of consideration. This information can be obtained by conventional percolation analysis of water clustering , which is extremely time consuming. In the present paper we propose a simple method to locate the percolation threshold of hydration water even in complex systems, using the average number of water-water hydrogen bonds. This method is derived from extensive computer simulation studies of the percolation transition of hydration water in various systems: water adsorbed at smooth hydrophilic planes and spheres , at surfaces of rigid and flexible single lysozyme molecules and lysozyme powder , hydration water in protein solutions .
Properties of Spanning Water Networks at Protein Surfaces
The Journal of Physical Chemistry B, 2005
The formation of a spanning two-dimensional hydrogen-bonded water network at the surface of proteins via a percolation transition enables their biological function. We show in detail how the spanning (percolating) water network appears at the surfaces of model hydrophilic spheres and at the surface of a single protein (lysozyme) molecule. We have found essential correlations of the linear extension, radius of gyration, and position of the center of mass of the largest water cluster with its size. The specific two-peak structure of the probability distribution of the largest cluster size allowed us to study various properties separately for spanning and nonspanning largest clusters. The radius of gyration of the spanning cluster always exceeds the radii of the spheres or the effective radius of the protein. Any spanning cluster envelops essentially more than half of the surface area. The temporal decay of the spanning networks shows a stretched exponential character. Their average lifetime at the percolation threshold is about the lifetime of a water-water hydrogen bond.
Percolation transition of hydration water at hydrophilic surfaces
Physica A: Statistical Mechanics and its Applications, 2006
An analysis of water clustering is used to study the quasi-2D percolation transition of water adsorbed at planar hydrophilic surfaces. Above the critical temperature of the layering transition (quasi-2D liquid-vapor phase transition of adsorbed molecules) a percolation transition occurs at some threshold surface coverage, which increases with increasing temperature. The location of the percolation line is consistent with the existence of a percolation transition at the critical point. The percolation threshold at a planar surface is weakly sensitive to the size of the system when its lateral dimension increases from 80 to 150 Å . The size distribution of the largest water cluster shows a specific two-peaks structure in a wide range of surface coverage: the lower-and higher-size peaks represent contributions from non-spanning and spanning clusters, respectively. The ratio of the average sizes of spanning and non-spanning largest clusters is about 1.8 for all studied planes. The two-peak structure becomes more pronounced with decreasing size of the planar surface and strongly enhanced at spherical surfaces. r
Thermal breaking of spanning water networks in the hydration shell of proteins
The Journal of Chemical Physics, 2005
The presence of a spanning hydrogen-bonded network of water at the surface of biomolecules is important for their conformational stability, dynamics, and function. We have studied by computer simulations the clustering and percolation of water in the hydration shell of a small elastinlike peptide ͑ELP͒ and the medium-size protein staphylococcal nuclease ͑SNase͒, in aqueous solution. We have found that in both systems a spanning network of hydration water exists at low temperatures and breaks up with increasing temperature via a quasi-two-dimensional percolation transition. The thermal breaking of the spanning water network occurs at biologically relevant temperatures, in the temperature range, which is close to the temperature of the "inverse temperature transition" of ELP and the unfolding temperature of SNase, respectively.
Hydration sphere structure of proteins: A theoretical study
Journal of Molecular Liquids, 2017
Hydration is essential for the proper biological activity of biomolecules. We studied the water network around insulin (as a model protein) in aqueous NaCl solutions using molecular dynamics simulations and statistical analysis of the topological properties (hydrogen bond neighbor number and the interaction energy between hydrogen-bonded water molecules) of the water network. We propose a simple method to define the hydration layers around proteins. Water molecules in the first and second layers form significantly less, but stronger hydrogen bonds with each other than in the bulk phase. Furthermore, water molecules over the hydrophilic and hydrophobic surface of the protein possess slightly different H-bonding properties, supporting the hypothesis of structural and dynamical heterogeneity of the water molecules over protein surface. The protein molecule perturbs the solvent structure at least up to the fourth-fifth hydration layer. Our data suggest the peculiar role of the second hydration shell.
How Protein Surfaces Induce Anomalous Dynamics of Hydration Water
The Journal of Physical Chemistry B, 2007
Water around biomolecules slows down with respect to pure water, and both rotation and translation exhibit anomalous time dependence in the hydration shell. The origin of such behavior remains elusive. We use molecular dynamics simulations of water dynamics around several designed protein models to establish the connection between the appearance of the anomalous dynamics and water-protein interactions. For the first time we quantify the separate effect of protein topological and energetic disorder on the hydration water dynamics. When a static protein structure is simulated, we show that both types of disorder contribute to slow down water diffusion, and that allowing for protein motion, increasing the spatial dimentionality of the interface, reduces the anomalous character of hydration water. The rotation of water is, instead, altered by the energetic disorder only; indeed, when electrostatic interactions between the protein and water are switched off, water reorients even faster than in the bulk. The dynamics of water is also related to the collective structuresà Voir the hydrogen bond (H-bond) networksformed by the solvent enclosing the protein surface. We show that, as expected for a full hydrated protein, when the protein surface offers pinning sites (charged or polar sites), the superficial water-water H-bond network percolates throughout the whole surface, hindering the water diffusion, whereas it does not when the protein surface lacks electrostatic interactions with water and the water diffusion is enhanced.
The Journal of chemical physics, 2014
The percolation temperature of the lateral hydrogen bonding network of the molecules at the free water surface is determined by means of molecular dynamics computer simulation and identification of the truly interfacial molecules analysis for six different water models, including three, four, and five site ones. The results reveal that the lateral percolation temperature coincides with the point where the temperature derivative of the surface tension has a minimum. Hence, the anomalous temperature dependence of the water surface tension is explained by this percolation transition. It is also found that the hydrogen bonding structure of the water surface is largely model-independent at the percolation threshold; the molecules have, on average, 1.90 ± 0.07 hydrogen bonded surface neighbors. The distribution of the molecules according to the number of their hydrogen bonded neighbors at the percolation threshold also agrees very well for all the water models considered. Hydrogen bonding...
Hydration and Nanoconfined Water: Insights from Computer Simulations
Sub-cellular biochemistry, 2015
The comprehension of the structure and behavior of water at interfaces and under nanoconfinement represents an issue of major concern in several central research areas like hydration, reaction dynamics and biology. From one side, water is known to play a dominant role in the structuring, the dynamics and the functionality of biological molecules, governing main processes like protein folding, protein binding and biological function. In turn, the same principles that rule biological organization at the molecular level are also operative for materials science processes that take place within a water environment, being responsible for the self-assembly of molecular structures to create synthetic supramolecular nanometrically-sized materials. Thus, the understanding of the principles of water hydration, including the development of a theory of hydrophobicity at the nanoscale, is imperative both from a fundamental and an applied standpoint. In this work we present some molecular dynamics studies of the structure and dynamics of water at different interfaces or confinement conditions, ranging from simple model hydrophobic interfaces with different geometrical constraints (in order to single out curvature effects), to selfassembled monolayers, proteins and phospholipid membranes. The tendency of the water molecules to sacrifice the lowest hydrogen bond (HB) coordination as possible at extended interfaces is revealed. This fact makes the first hydration layers to be highly oriented, in some situations even resembling the structure of hexagonal ice. A similar trend to maximize the number of HBs is shown to hold in cavity filling, with small subnanometric hydrophobic cavities remaining empty while larger cavities display an alternation of filled and dry states with a significant inner HB network. We also study interfaces with complex chemical and geometrical nature in order to determine how different conditions affect the local hydration properties. Thus, we show some results for protein hydration and, particularly, some preliminary
Local Structure and Dynamics of Hydration Water in Intrinsically Disordered Proteins
Journal of Physical Chemistry B, 2015
Hydration water around protein surface plays a key role in structure, folding and dynamics of proteins. Intrinsically disordered proteins lack secondary and/or tertiary structure in their native state. Thus characterizing the local structure and dynamics of hydration water around disordered proteins is challenging for both experimentalists and theoreticians. The local structure, orientation and dynamics of hydration water in the vicinity of intrinsically disordered proteins is investigated through molecular dynamics simulations. The analysis of the hydration capacity reveals that the disordered proteins have much larger binding capacity for hydration water than globular proteins. The surface and radial distribution of water molecules around the disordered proteins depict a similar trend. The local structure of the hydration water evaluated in terms of the tetrahedral order parameter, shows a higher order among the water molecules surrounding disordered proteins/regions. Residence time of water molecules clearly exhibit slow dynamics of hydration water around the surface of disordered proteins/regions as compared to globular proteins. The orientation of water molecules is found to be distinctly different for ordered and disordered proteins/regions. This analysis provides a better insight into the structure and dynamics of hydration water around disordered proteins.
Protein Hydration Dynamics and Molecular Mechanism of Coupled Water−Protein Fluctuations
Journal of the American Chemical Society, 2009
Protein surface hydration is fundamental to its structural stability and flexibility, and water-protein fluctuations are essential to biological function. Here, we report a systematic global mapping of water motions in the hydration layer around a model protein of apomyoglobin in both native and molten globule states. With site-directed mutagenesis, we use intrinsic tryptophan as a local optical probe to scan the protein surface one at a time with single-site specificity. With femtosecond resolution, we examined 16 mutants in two states and observed two types of water-network relaxation with distinct energy and time distributions. The first water motion results from the local collective hydrogen-bond network relaxation and occurs in a few picoseconds. The initial hindered motions, observed in bulk water in femtoseconds, are highly suppressed and drastically slow down due to structured water-network collectivity in the layer. The second water-network relaxation unambiguously results from the lateral cooperative rearrangements in the inner hydration shell and occurs in tens to hundreds of picoseconds. Significantly, this longtime dynamics is the coupled interfacial water-protein motions and is the direct measurement of such cooperative fluctuations. These local protein motions, although highly constrained, are necessary to assist the longtime water-network relaxation. A series of correlations of hydrating water dynamics and coupled fluctuations with local protein's chemical and structural properties were observed. These results are significant and reveal various water behaviors in the hydration layer with wide heterogeneity. We defined a solvation speed and an angular speed to quantify the water-network rigidity and local protein flexibility, respectively. We also observed that the dynamic hydration layer extends to more than 10 Å. Finally, from native to molten globule states, the hydration water networks loosen up, and the protein locally becomes more flexible with larger global plasticity and partial unfolding.