Evidence for water structuring forces between surfaces

Abstract

Structured water on apposing surfaces can generate significant energies due to reorganization and displacement of water as the surfaces encounter each other. Force measurements on a multitude of biological structures using the osmotic stress technique have elucidated commonalities that point toward an underlying hydration force. In this review, the forces of two contrasting systems are considered in detail: highly charged DNA and nonpolar, uncharged hydroxypropyl cellulose. Conditions for both net repulsion and attraction, along with the measured exclusion of chemically different solutes from these macromolecular surfaces, are explored and demonstrate common features consistent with a hydration force origin. Specifically, the observed interaction forces can be reduced to the effects of perturbing structured surface water.

Figure 1

A comparison of forces measured for several different systems in ordered arrays. Π is the osmotic pressure applied by the excluded polymer in the bulk solution acting on the condensed macromolecular phase. Distances are given as approximate surface-to-surface separations of macromolecules. Schizophyllan [55] and hydroxypropyl cellulose (HPC) [30] are completely uncharged. DNA in NaBr and TMABr, tetramethyl ammonium, (unpublished data) and ι-carrageenan in NaCl (unpublished data) are highly charged linear double helices. DDP (didodecyl phosphate) in TMA⁺ salt is a highly charged planar bilayer (data from [56]). Egg PC is a zwitterionic planar bilayer that has the phosphate and quaternary amine of the head group covalently linked (data from [57]). The TMA⁺-DNA force has also been corrected to planar packing and to the same surface area/phosphate as DDP. The close overlap of the corrected TMA⁺-DNA, egg PC (that has about the same surface area/molecule as DDP) and TMA⁺-DDP forces illustrates the striking similarity of these homologous systems. The salt concentrations for the charged surfaces are high enough that forces are insensitive to ionic strength. The excess pressures due to solute exclusion are also shown for the nonpolar alcohol methylpentane diol (MPD) at 1 molal interacting with DNA and for zwitterionic proline at 1 molal interacting with uncharged HPC. The straight lines show a decay length of ~4 Å. The force amplitudes span a range greater than 100-fold.

Figure 2

The dependence of DNA-DNA forces on NaBr concentration is shown. The diameter of DNA is ~ 20 Å. Forces converge at high pressures for all salt concentrations. For ionic strengths less than ~ 0.8 M, an electrostatic interaction dominates at low pressures. The decay length of the apparent exponential in this regime is consistent with the Debye-Huckel shielding length. At higher ionic strengths, the forces at low pressures converge. The apparent exponential decay length is ~ 4.2 Å. The decay length of the high pressure force obtained after subtracting the low pressure forces is ~ 2 Å and has an amplitude independent of salt concentration.

Figure 3

DNA force curves with different amine counterions are fit to double exponential functions with λ and λ/2 decay lengths. All counterion concentrations are large enough that forces depend only slightly on ionic strength. Spermidine³⁺ and spermine⁴⁺ spontaneously precipitate DNA. The amplitude of the λ decay length exponential changes from repulsive to attractive between putrescine²⁺ and spermidine³⁺. The best fitting decay length λ varies between 4.2 – 5.0 Å. The λ/2 decay length exponential is repulsive for all the charged amines shown. The amplitudes of the λ/2 decay length exponential for DNA interactions in NH₄⁺, putrescine²⁺, spermidine³⁺, and spermine⁴⁺ are closely comparable. A similar result for the λ/2 decay length force was found for DNA with an extended set of homologous arginine peptides ranging from +1 to +6 charges. The triangle symbols with dots and crosses are for DNA in 1.2 M TMA⁺ at 5° and 50° C, respectively. The square symbols with dots and crosses are for DNA in 30 mM putrescine²⁺ at 5° and 50° C. In spite of the ~25% decrease in the dielectric constant of water between 5° and 50° C, forces change negligibly.

Figure 4

Hydroxypropyl cellulose forces are temperature dependent. The diameter of HPC is ~ 12.5 Å. The amplitude of the ~ 4 Å decay exponential is strongly temperature dependent, changing from repulsive to attractive at ~ 40 °C. At higher temperatures, the spacing between polymer chains continues to decrease with no applied osmotic pressure indicating that the attractive force continues to increase. At close spacings, the last 2 Å of separation, a very rapidly changing force is observed, probably due to the steric clash of i-propyl groups extending from the cellulose backbone. The solid lines are double exponential fits to the data. The low pressure force decay length is fixed at 4 Å. The decay length of the high pressure steric interaction is taken as 0.25 Å. The amplitude of this very short-ranged force shows negligible temperature dependence. The inset to the figure shows the linear dependence of the amplitude of the 4 Å decay length force at 12.5 Å, A(T), on temperature. Data taken from [30].

Figure 5

The addition of 2 M NaCl has a much larger impact on neutral and nonpolar HPC-HPC forces than on DNA-DNA interactions. In both cases, the samples were initially in 10 mM TrisCl (pH 7.5), 1 mM EDTA. Salt is acting on HPC through exclusion. The difference in salt concentration between the HPC phase and the bulk solution results in an excess osmotic pressure acting on the condensed phase.

Figure 6

The exclusion of nonpolar alcohols from spermidine³⁺ condensed DNA and of salts and polar solutes from HPC mirrors the forces between macromolecules. Interaxial spacings have been adjusted for macromolecular diameters to give surface separations. The excess osmotic pressure due to exclusion is calculated from the dependence of the interhelical spacing between macromolecules on the salt or solute concentration; Π₀ is the maximal osmotic pressure that could be applied by the salt or solute if completely excluded from the macromolecular phase. For each curve, several different concentrations of salt or solute were used. The overlap indicates that the excess number of water molecules at a fixed spacing is constant, independent of solute concentration. The exponential decay lengths vary between 3.5 and 4.3 Å. Data taken from [31,48,51].