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Monte Carlo simulation of the hydration shell of double-helical amylose: a left-handed antiparallel double helix fits best into liquid water structure

Eisenhaber, F., Schulz, W.
Biopolymers 1992 v.32 no.12 pp. 1643-1664
amylose, molecular conformation, water, simulation models, Monte Carlo method
The conformation of double-helical amylose is influenced by its water environment [A. Imberty, H. Chanzy, S. Perez, A. Buleon, and V. Tran (1988) Journal of Molecular Biology, Vol. 201, pp. 365-378; A. Imberty and S. Perez (1988) Biopolymers, Vol. 27, 1205-1221]. For several low-energy conformations of left-handed amylose double helices, we performed Monte Carlo simulations of the (N, V, T)-ensemble of configurations of water molecules surrounding a single duplex. The crucial point of this simulation is the use of cylindrical periodical boundary conditions with a relatively small asymmetric unit comprising a limited number of water molecules. The output data consists of local maxima of water density in the space near the macromolecule and information on one- and two-membered water bridges between polar groups of amylose as well as energetic characteristics of the system under study. A left-handed antiparallel-stranded conformation of the amylose double helix (rise and twist per glucose unit are 0.343 nm and -58.1 degrees) corresponds to the global minimum of intraduplex potential energy [W. Schulz and H. Sklenar (1993) Biopolymers, submitted; W. Schulz, H. Sklenar, W. Hinrichs, and W. Saenger (1993) Biopolymers, to be published]. We found that this conformation is favored also by its hydration shell characteristics in comparison to parallel-stranded structures. Three hydration sites per glucose unit in the vicinity of HO6, O6, and O3 could be identified. Regular water bridges forming a network around the duplex were observed. A moderate change of the helical parameters within the family of left-handed antiparallel structures (to a rise and twist per glucose unit of 0.233 nm and -45 degrees) does not have noteworthy consequences for the characteristics of the hydration shell. The location of the hydration sites with respect to the polar groups of amylose and the observed water bridges are in excellent agreement with the hydration geometry of the heavily hydrated antiparallel-stranded left-handed double helix of p-nitrophenyl alpha-maltohexose described in a high-resolution crystal study [W. Hinrichs, G. Buttner, M. Steifar, Ch. Betzel, V. Zabel, B. Pfannemuller, and W. Saenger (1987) Science, Vol. 238, pp. 205-208; W. Hinrichs and W. Saenger (1990) Journal of the American Chemical Society, Vol. 112, pp. 2789-2796]. In the case of parallel-stranded (nonsymmetric or symmetric) double helices, only one hydration site near the (H) O3 group could be identified. No systematic water bridges with sufficient high probability were observed. The sum of the average potential energies of the amylose-water and water-water interactions is not favourable in comparison with the energy for antiparallel-stranded double helices. The water-water interaction is high, i.e., parallel-stranded amylose breaks the structure of liquid water. This effect would explain the insolubility of natural amylose in cold water and support the occurrence of parallel-stranded double helices in crystallites of starch granules and in amylose microcrystals having only low water content [see Imberty et al. (1988) and Imberty and Perez (1988) above]. Symmetric parallel-stranded double helices have very well-exposed polar groups and their conformation should be favored in crystals by the ability to form extensively interduplex hydrogen bonds directly or via single water molecules. Single water molecules incorporated into the crystal would compensate for the shortage of donors of hydrogen bonds on the surface of the symmetric parallel-stranded double helix. Indeed, in accordance with diffraction data [see Imberty and Perez (1988) above; also A. Imberty, H. Chanzy, S. Perez, A. Buleon, V. Tran (1987) Macromolecules, Vol. 20, pp. 2636-2638] a critical amount of water increases the crystallinity of amylose and only symmetric parallel-stranded double helices would fit into a crystallographic unit cell with c = 1.05 nm. The unfavorable hydration of parallel-stranded double-he