Equilibrium Swelling, Interstitial Forces, and Water Structuring in

Article pubs.acs.org/Langmuir

Equilibrium Swelling, Interstitial Forces, and Water Structuring in Phytoglycogen Nanoparticle Films Michael Grossutti, Eric Bergmann, Ben Baylis, and John R. Dutcher* Department of Physics, University of Guelph, Guelph, Ontario, Canada N1G 2W1 S Supporting Information *

ABSTRACT: Phytoglycogen is a highly branched polymer of glucose that forms dendrimeric nanoparticles. This special structure leads to a strong interaction with water that produces exceptional properties such as high water retention, low viscosity, and high stability of aqueous dispersions. We have used ellipsometry at controlled relative humidity (RH) to measure the equilibrium swelling of ultrathin films of phytoglycogen, which directly probes the interstitial forces acting within the films. Comparison of the swelling behavior of films of highly branched phytoglycogen to that of other glucose-based polysaccharides shows that the chain architecture plays an important role in determining both the strong, shortrange repulsion of the chains at low RH and the repulsive hydration forces at high RH. In particular, the length scale λ0 that characterizes the exponentially decaying hydration forces provides a quantitative, RH-independent measure of film swelling that differs significantly for different glucose-based polysaccharides. By combining ellipsometry with infrared spectroscopy, we have determined the relationship between water structuring and inter-chain separation in the highly branched phytoglycogen nanoparticles, with maintenance of a high degree of water structure as the film swells significantly at high RH. These insights into the structure−hydration relationship for phytoglycogen are essential to the development of new products and technologies based on this sustainable nanomaterial.

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For thin films, the forces acting between the molecules can be interpreted in terms of a disjoining pressure P acting across the film thickness,9 which characterizes driving forces that tend to either thin (P < 0) or thicken (P > 0) the film. Repulsive hydration forces within polysaccharide films, which tend to thicken the films, can be probed by varying the RH of the surrounding gas. This applies an osmotic stress3−8,10−13 that can produce disjoining pressures P that approach 109 Pa,3−6 as determined by

INTRODUCTION Hydrophilic biopolymers such as polysaccharides interact strongly with water and can swell considerably as the relative humidity (RH) of the surrounding environment is increased. Water uptake by polysaccharides such as hyaluronic acid is of central importance in biological systems1 and has been exploited in a variety of technological applications such as drug delivery vehicles, biosensors, and tissue engineering scaffolds.2 Developing a fundamental understanding of the relationship between the structure of polysaccharides and their interaction with water is clearly essential to fully exploit their potential applications as sustainable biomaterials. Hydration of polysaccharides is considered to occur in two RH regimes. At low RH, for which the water content is low and the separation between neighboring monomer units is small, the interaction between monomer units is dominated by very short-range, hard-core repulsion.3 At higher RH, the water content is increased, the monomer units are further apart, and repulsive hydration forces dominate.3−8 Hydration forces are thought to arise via a collective, weak perturbation of the many water molecules associated with the macromolecules,4 and it has been shown that they decay exponentially over distances on the order of an angstrom for many biological molecules including polysaccharides, lipids, proteins, and DNA.5−8 This analysis suggests that the structure of the hydration water hydrogen bond network plays an important role in determining hydration forces. © 2017 American Chemical Society

P=

⎛ RT ⎞ ⎛ RH ⎞ ⎛ RT ⎞ ⎛ p ⎞ μ ⎟ = −⎜ ⎟ ln⎜ ⎟ ln⎜⎜ ⎟⎟ = −⎜ Vm ⎝ Vm ⎠ ⎝ 100 ⎠ ⎝ Vm ⎠ ⎝ p0 ⎠

(1)

where R is the gas constant, T is the temperature, μ is the chemical potential, Vm is the molar volume of water, p is the partial pressure of water vapor, and p0 is the equilibrium vapor pressure of water.3,14 Measurement of changes in film thickness in response to changes in disjoining pressure at constant temperature allows the construction of force−distance isotherms, which quantitatively describe the interstitial forces acting within the film.3,10 Phytoglycogen is a highly branched, dendrimeric polysaccharide nanoparticle produced by certain varieties of plants. Received: January 5, 2017 Revised: February 27, 2017 Published: February 28, 2017 2810

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Figure 1. (a) Best-fit film thickness h for five different phytoglycogen films as a function of RH, (b) swelling ratio h/h0 as a function of RH for the phytoglycogen films, (c) corresponding best-fit values of the refractive index n as calculated using the Garnet equation.10 The dashed blue vertical lines indicate the separation between the two swelling regimes. The uncertainties in the best-fit h and n values are less than the size of the symbols.

degree of water structure maintained as the film swells significantly in the low disjoining pressure regime.

It is composed of α(1,4)-linked glucose units that undergo α(1,6) branching every 10−12 monomers.15−18 The unique structure and hydrophilic character of phytoglycogen nanoparticles result in a range of fundamental and technologically important properties such as monodisperse particle size (hydrated diameter of 34.8 ± 3.2 nm, as measured using small angle neutron scattering19), high water retention, and low viscosity and high stability when dispersed in water.19,20 We have recently studied the structure and dynamics of hydration water in phytoglycogen using neutron scattering and infrared spectroscopic techniques.19,20 These measurements have helped us to understand the effectiveness of the phytoglycogen nanoparticles as a superior natural moisturizing agent in personal care formulations. Clearly the unique hydration properties of phytoglycogen are related to the highly branched, dendrimeric structure of the compact nanoparticles. In the present study, we have achieved unique insights into the structure−hydration relationship of phytoglycogen by using the ultrathin film geometry and ellipsometry to probe shortrange repulsive and hydration forces acting within the films as the RH is changed. We compare the equilibrium swelling behavior of phytoglycogen to that of other polysaccharides composed of glucose monomers that differ only in their degree of branching and hydrogen bonding: dextran measured in the present study and published data for cellulose.10 Dextrans are a class of slightly branched, comblike, glucose-based polysaccharides consisting of α(1,6)-linked D-glucose units with variable branching characteristics (linkage type, length, distribution, and proportion) depending on the microbial source and production conditions.25−27 In this study, we have used dextran (MW = 200 kDa) sourced from Leuconostoc mesenteroides, which has ∼5% α(1,3)-branching linkages.25 The α(1,3)-linked branch side chains are themselves α(1,6)-linked and can be of various lengths.25−27 By contrast, cellulose is a semicrystalline polysaccharide composed of β-1,4-linked D-glucose linear chains that form highly ordered semicrystalline fibers via strong interchain hydrogen bonding.10 We find that the swelling behavior of films of highly branched phytoglycogen nanoparticles is intermediate between that of dextran and cellulose, indicating the importance of chain architecture in determining the short-range repulsive and hydration forces in polysaccharides. By correlating the pressure−distance isotherms with infrared measurements of hydration water structure, we have determined the relationship between water structuring and interchain separation in the highly branched phytoglycogen nanoparticles, with a high

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EXPERIMENTAL SECTION

Polysaccharide Materials and Film Preparation. Monodisperse phytoglycogen nanoparticles (hydrated MW = 14.7 × 106 g/ mol; hydrated diameter of 34.8 ± 3.2 nm)19 extracted and purified from sweet corn were obtained from Mirexus Biotechnologies Inc. Further information regarding the extraction, purification, and characterization of the phytoglycogen particles can be found in ref 19. Dextran (MW = 200 kDa) from L. mesenteroides was obtained from Sigma-Aldrich. The substrates for the samples were Si(100) wafers (1 × 1 cm2) with a native oxide layer which were cleaned by placing them in a UV/ ozone cleaner for 20 min, rinsing with Milli-Q water, and drying under a dry nitrogen flow. Aqueous dispersions (∼2% w/w) of either phytoglycogen nanoparticles or dextran were prepared using Milli-Q water (resistivity of 18.2 MΩ cm). Two to five drops of the phytoglycogen dispersions were spin-coated using a Headway EC101 spincoater onto the wafers at 4000 rpm using the drop-then-spin technique in an 85 ± 5% relative humidity (RH) environment, waiting for 5 min between successive drops. This procedure resulted in dry phytoglycogen film thicknesses h0 that ranged from 40 to 100 nm, and the root-mean-square (RMS) roughness was ∼1 nm over a 10 × 10 μm2 area, as measured using atomic force microscopy (AFM) (Figure S1). Dextran films were made using single drops of the dextran solution in ambient RH, and the spin speed was varied between 3000 and 4000 rpm. This procedure resulted in dry dextran film thicknesses h0 that ranged between 50 and 70 nm, and the RMS roughness was less than 1 nm over a 10 × 10 μm2 area, as measured using AFM. Ellipsometry and FTIR Experimental Methods. Ellipsometry measurements on the phytoglycogen and dextran films were performed using a custom-built, self-nulling single wavelength (λ = 632.8 nm) ellipsometer at a fixed angle of incidence (60.000 ± 0.005°).21,22 Because of the careful design of the ellipsometer, we were able to measure the polarizer P and analyzer A angles with high precision, typically to within ±0.002°.21 The thickness h and refractive index n for each film were calculated using the Fresnel equations for an ideal layer model (a refractive index of 3.858 − i0.152 for silicon with a 2 nm-thick oxide layer, a refractive index of 1.52 for the “dry” polysaccharide film, and a refractive index of 1 for air). Best-fit values of h and n were calculated as the averages of nulling measurements performed in two ellipsometric zones.23 Changes in the refractive index n of the polysaccharide films arising from hydration were calculated using the Garnet equation, following the analysis used in ref 10. The RH in the sample chamber was controlled by adjusting the relative flow of dry and water-saturated nitrogen gas over the films.22 The RH within the sample chamber was monitored using a Sensirion SHT71 humidity sensor. Equilibrium film thicknesses were measured for RH values between ∼4 and ∼90% RH at ∼25 °C. The films were 2811

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Langmuir allowed to equilibrate for at least 20 min at each RH value before data collection. FTIR spectra for dextran films and D2O exchange experiments on phytoglycogen films (Supporting Information) were collected and analyzed as described in detail in ref 20.

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RESULTS AND DISCUSSION In Figure 1, we show the dependence on relative humidity RH of the best-fit phytoglycogen film thickness h, the swelling ratio h/h0 (film thickness normalized with respect to the dry thickness h0 measured with RH < 4%), and the corresponding best-fit refractive index values n for five different films. The dry thickness h0 values ranged from 40 to 100 nm. The overlap between the h/h0(RH) values for the five films with considerably different values of h0 indicates that the swelling is uniform within the films for this range of h0 values. The h/ h0(RH) data show a significant increase in slope at RH ≈ 70%, which is commonly observed for hydrophilic polymer films.3,10 The maximum value of the swelling ratio of h/h0(RH) ≈ 1.35 at RH = 90% is comparable to that measured for other polysaccharides.3,10 The effectiveness of changing the hydration of phytoglycogen films using variable RH gas flow through the sample chamber was characterized by exposing a film that was prepared in H2O and subsequently dried for 30 h in dry nitrogen gas (RH < 4%), to D2O vapor (RH = 85%). This allowed the tracking of the time evolution of the O−H stretching and O−D stretching bands using infrared spectroscopy (Supporting Information). Most of the glucose hydroxyl protons and sorbed water molecules were exchanged very quickly (within 5 min), as seen by a significant decrease in O−H stretching absorbance (Figure S3). Complete exchange occurred after 25 h with no evidence of unexchanged protons in the film, indicating that the entire interior volume of the phytoglycogen particles is accessible to the solvent. As discussed above, measurements of the swelling ratio h/h0 as a function of RH can be expressed as a function of the disjoining pressure P in the film, and quantitative pressure− distance isotherms, corresponding to the logarithm of P versus the swelling ratio h/h0, can be obtained for the phytoglycogen films (red points in Figure 2a). The data obtained for dextran are also shown for comparison (black points in Figure 2a). In both cases, the data are characterized by an abrupt transition from a steep slope for high disjoining pressures (P > 5 × 107 Pa) to a smaller slope for lower disjoining pressures (P < 5 × 107 Pa), corresponding to the two swelling regimes identified in Figure 1. The large difference in slope between the high and low disjoining pressure regimes of the pressure−distance isotherm suggests different physical origins for the forces that drive film swelling. This type of behavior has also been observed for other polysaccharides such as cellulose and hyaluronic acid.3,10,24 In Figure 2a, we show the best fit of the data in the high disjoining pressure regime (P > 5 × 107 Pa) to a power law function of the form P(h/h0) ≈ (h/h0)−m. In this regime, the films are the thinnest (values of h/h0 close to 1) and the swelling behavior is driven by strong repulsive forces between the polysaccharide chains because of molecular orbital overlap.3,10,24 The best-fit value of the exponent m = 17.4 ± 0.7 for phytoglycogen is very large, comparable to the value measured for cellulose (Table 1).10 Correspondingly, phytoglycogen and cellulose have very similar maximum swelling ratios h/h0 ≈ 1.1 in this regime.10 For dextran, we measure a

Figure 2. (a) Logarithm of the disjoining pressure P in the same five phytoglycogen films (red points) as in Figure 1 as a function of the swelling ratio h/h0. Data obtained for dextran are also shown (black points). The range of dry film thicknesses h0 was between 40 and 100 nm (phytoglycogen) and 50 and 70 nm (dextran). For each data set, the blue line corresponds to the best fit of the power law function P(h/ h0) ≈ (h/h0)−m to the data at high disjoining pressures (P > 5 × 107 Pa); the best-fit values of m are given in Table 1. (b) Logarithm of P in the same five phytoglycogen films (red points) as in Figure 1 as a function of the change in distance ΔL between neighboring monomers. Data obtained for dextran are also shown (black points). For each data set, the blue line corresponds to the best fit of an exponential function (eq 3) to the data at low disjoining pressures (P < 5 × 107 Pa); the best-fit values of P0 and λ0 are given in Table 1. In (a,b), the dashed blue line at P = 5 × 107 Pa (RH = 70%) corresponds to the transition between the two swelling regimes indicated in Figure 1.

Table 1. Best-Fit Parameters for the High and Low Disjoining Pressure Regimes for Polysaccharide Films, Listed in the Order of Increasing Value of m polysaccharide a

dextran phytoglycogen cellulose10,b a

m

P0 (107 Pa)

λ0 (Å)

14.2 ± 0.8 17.4 ± 0.7 20

8.1 ± 0.5 9.3 ± 0.8 14

1.71 ± 0.10 0.89 ± 0.06 0.32

Dextran MW = 200 kDa. bRegenerated cellulose.

best-fit value of the exponent m = 14.2 ± 0.8, which is less than that for the more highly branched dendrimeric phytoglycogen (Table 1). Apparently, the short-range repulsion, as measured by the parameter m, is correlated with the structure of the polysaccharide chains (Table 1). The dendrimeric architecture of phytoglycogen results in short-range repulsion that is between those of branched dextran and highly ordered, semicrystalline cellulose and is a direct indication of the high density of the polymer chains and a high degree of interchain 2812

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Figure 3. (a) Rnetwork and (b) Rmultimer vs the change in monomer separation ΔL for phytoglycogen20 (red) and dextran (black). See Figure S6 for dextran infrared spectra.

is also a reasonable result because swelling of the films reveals differences in the interstitial environments as determined by the different chain architectures. We find that λ0 provides a quantitative, RH-independent measure of the degree of film swelling in the hydration force regime and indicates the importance of chain architecture in determining hydration forces in polysaccharides. To further examine the relationship between hydration forces and water structure in the phytoglycogen films, we combine the pressure−distance data from the present study with hydration water structure data from previous infrared (IR) absorption spectroscopy measurements.20 The shape of the O−H stretching IR absorption band of water is sensitive to the surrounding hydrogen bond environment and is commonly interpreted in terms of simple models that attribute the IR absorption bands to subpopulations of water molecules in different hydrogen bonding environments.20,29−33 In ref 20, we analyzed the O−H stretching band of interstitial water molecules sorbed by several different polysaccharide films and discussed the spectra in terms of a model that assigned the IR absorption bands to two general water subpopulations: network water and multimer water. Network water is defined as water molecules that are in a network of hydrogen bonds and consist of tetrahedrally coordinated water pentamers and distorted tetrahedral water tetramers.20,29−32 By contrast, multimer water is defined as water molecules that are in a disturbed hydrogen bond network and consist of water clusters containing two or less hydrogen bonds per water molecule.20,29−33 The hydration water structure is characterized by spectral parameters Rnetwork and Rmultimer as determined by comparing the subpopulations of water molecules in different hydrogen bonding environments. Rnetwork is the ratio of the IR absorbance arising from water pentamers in a tetrahedrally coordinated hydrogen bonding environment relative to the absorbance arising from water molecules in a distorted tetrahedral hydrogen bonding environment.20,29−32 Each of these subpopulations is associated with low-density, high-connectivity network water (i.e. water in a hydrogen bonded network), and Rnetwork serves as a measure of the network water hydrogen bond connectivity. Rmultimer is the ratio of the IR absorbance arising from high-density, low-connectivity multimer water clusters compared with that arising from the tetrahedrally coordinated network water pentamers. Thus, Rmultimer provides a measure of the relative subpopulations of multimer water to network water. The spectral parameters Rnetwork and Rmultimer, in combination with the pressure−distance data, allow us to track

interaction in the high-molecular-weight, small phytoglycogen particles. At low disjoining pressures (P < 5 × 107 Pa), the water content of the film increases significantly with increasing RH (Figure S4) corresponding to the regime in which hydration forces dominate.3,10 To quantify the hydration forces in the film, we define a distance parameter ΔL as the change in the average separation between monomer units in response to changes in RH or, equivalently, disjoining pressure P. Following Mathe et al.,3 we use a cubic lattice model in which ΔL can be expressed as a function of the swelling ratio by ΔL = a0((h/h0)1/3 − 1)

(2)

where a0 is the size of the glucose monomer (7.5 Å).3,10,28 It is important to emphasize that ΔL is a measure of the change in the average distance between monomer units. Because the intrachain monomer separation will remain constant throughout the swelling process, the value of ΔL will be less than the change in interchain monomer separation. Nevertheless, ΔL is a useful parameter for comparing the contribution of hydration forces in phytoglycogen to that in other polysaccharides.3,10,24 The hydration pressure within the film can be described empirically by an exponential decay of the form3−6,13 P(ΔL) = P0 e−ΔL / λ0

(3)

where P0 is the intrinsic hydration pressure arising from the hydration forces and λ0 is the characteristic decay length. The value of P0 can differ by orders of magnitude for different materials, whereas decay length values are generally similar and of the order of angstroms.5 In Figure 2b, we plot the logarithm of the disjoining pressure P as a function of ΔL for both phytoglycogen and dextran, in which the straight lines correspond to the best fit of each data set in the low disjoining pressure regime to eq 3. The corresponding best-fit values of P0 and λ0 are given in Table 1. We note the similarity of the bestfit P0 values for all three polysaccharides listed in Table 1, indicating that the internal (repulsive) pressures generated by the hydration forces in the films at small ΔL are comparable. This is reasonable because the polysaccharides are chemically equivalent (all are composed of glucose monomers) and by extrapolating to the highly compressed state of the films in the low RH limit, the differences in their chain architectures should be minimized. By contrast, the best-fit values of λ0 highlight the differences between the polysaccharides: the values differ significantly, with that for phytoglycogen lying between those for the two other polysaccharides, dextran and cellulose.10 This 2813

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which hydration forces dominate the swelling behavior of the film. By comparing Figure 3a,b, we can see that swelling in the low disjoining pressure regime is associated with an increase in the number of high-density multimer water clusters and a decrease in network water connectivity. This result can be interpreted as the filling of small pores with dense, disordered water that drives swelling at high water content. The data for dextran show the same general trend of Rmultimer with ΔL, with the values for dextran once again less than the corresponding values for phytoglycogen. We note that the relationship between network water connectivity and interstitial separation characterized for the polysaccharides in the present study is similar to that observed previously for collagen helices.8 In this previous study, an increase in water connectivity (measured using a spectral parameter analogous to Rnetwork) was observed as the interaxial spacing between collagen helices was decreased from 18 to 13 Å, with the associated hydration forces attributed to the rearrangement of interstitial water molecules in response to changes in the collagen interaxial spacing.8 The similarity of the relationship between network water connectivity and interstitial separation for collagen and polysaccharides (Figure 3), despite the much smaller values of the interstitial separations for the polysaccharides, is striking. This comparison demonstrates that the correlation between the structure of interstitial water, hydration forces, and interstitial separation of chains goes beyond a single class of biopolymers such as protein filaments or polysaccharides, providing unique insights into the nature of hydration of hydrophilic polymers.

changes in sorbed water structure with changes in disjoining pressure and interchain spacing. In Figure 3, we plot the spectral parameters Rnetwork and Rmultimer as a function of the change in the monomer separation ΔL for both phytoglycogen and dextran. We note that the values of Rnetwork for the phytoglycogen nanoparticles shown in Figure 3a are very large, greater than those for linear polysaccharides such as hyaluronic acid and chitosan by a factor of 2,20 indicating the overall high degree of ordering and bonding of the interstitial hydration water in phytoglycogen. As ΔL increased to 0.1 Å in the high disjoining pressure regime, a sharp increase in Rnetwork was observed, indicating that small increases in interstitial separation result in a significant increase in the order and connectivity of the interstitial water hydrogen bond network. This is consistent with a filling of the hydrogen bond network via the addition of sorbed water molecules and/ or the structural rearrangement of water molecules and their corresponding H bonds to improve the integrity of the hydrogen bond network. A very large reduction in disjoining pressure of ∼3.5 × 108 Pa (Figure 2) is associated with this very small increase in interstitial separation, which is indicative of the strong, short-range repulsive forces acting in the film in the high disjoining pressure regime. The network water connectivity reaches a plateau value for larger values of ΔL within the high disjoining pressure regime. For further increases in ΔL, corresponding to the low disjoining pressure regime (ΔL > 0.35 Å), Rnetwork remains essentially constant, experiencing only a slight decrease with increasing ΔL, suggesting that the stabilization provided to the water hydrogen bond network by the highly branched phytoglycogen chain architecture decreases only slightly as the interstitial space occupied by the water molecules increases. We note that the disjoining pressure decreases by only ∼3.5 × 107 Pa for 0.35 Å < ΔL < 0.8 Å, which is an order of magnitude smaller than that associated with the increase in ΔL from 0 to 0.1 Å. This is indicative of the weaker hydration forces within the films in the low disjoining pressure regime. For dextran, the dependence of Rnetwork on ΔL is similar to that for phytoglycogen, with several important differences. First, the values of Rnetwork are smaller than those for phytoglycogen, indicating that the water is less structured. In addition, the extent of the decrease in Rnetwork with ΔL in the hydrationforce-driven swelling regime (low disjoining pressures) was much greater than that for phytoglycogen. This difference in behavior suggests that the water hydrogen bond network is stabilized to a greater degree in the phytoglycogen film and suggests that differences in water structure due to differences in chain architecture are responsible for the factor of ∼2 difference in λ0 measured for phytoglycogen (0.89 Å) and dextran (1.71 Å). In Figure 3b, we show the dependence of the spectral parameter Rmultimer on ΔL for both phytoglycogen and dextran. For phytoglycogen, as ΔL increased to ∼0.2 Å, Rmultimer increased sharply, indicating an increase in the fraction of low-connectivity, high-density multimer water relative to highconnectivity, low-density network water. This increase occurred despite the sharp increase in Rnetwork, with approximately the same relative change, within the same range of ΔL values (Figure 3a). This means that despite the increase in the ordering of the water in the high disjoining pressure regime, there is an even larger increase in the amount of disordered water. For further increases in ΔL, Rmultimer increased more slowly in the low disjoining pressure regime (ΔL > 0.35 Å) in

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CONCLUSIONS Ellipsometry measurements of the equilibrium swelling of ultrathin films of phytoglycogen nanoparticles under controlled relative humidity conditions have revealed detailed information about repulsive short-range and hydration forces that determine the disjoining pressure acting across the films. At both high and low disjoining pressures, the swelling behavior of phytoglycogen is intermediate between that of the slightly branched, comb-like, glucose-based dextran and that of cellulose,10 a strongly bonded, semicrystalline glucose-based polysaccharide. At high disjoining pressures, for which the water content in the film is low, and the interchain separations are very small, strong short-range repulsive forces dominate the swelling behavior. The large value of the power law exponent m measured for phytoglycogen, which lies between the values for dextran and cellulose, indicates the presence of strong interchain interactions within the highly branched, densely packed, dendrimeric architecture of the nanoparticles. In this regime of high disjoining pressures, the water content in the film is low, and the water structure parameters Rnetwork and Rmultimer have similar dependences on ΔL for both phytoglycogen and dextran. At low disjoining pressures, for which the water content in the film is high and the interchain separation is large, hydration forces dominate the swelling behavior. The best-fit value of the hydration force decay length λ0 measured for phytoglycogen lies between the values measured for the other glucose-based polysaccharides, dextran and cellulose. We find that λ0 provides a quantitative, RH-independent measure of the degree of film swelling in the hydration force regime and indicates the importance of chain architecture in determining hydration forces in polysaccharides. In the low disjoining pressure regime, the water structure parameter Rnetwork for dextran decreases 2814

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Langmuir much more substantially with ΔL than it does for phytoglycogen, suggesting that differences in the sorbed interstitial water hydrogen bond network, arising from differences in the chain architecture, may be responsible for the large (factor of ∼2) difference in the values of λ0. Our analysis provides unique insights into the relationship between the hydration dependence of repulsive short-range and hydration forces, the interchain separation and the high degree of water structuring within phytoglycogen nanoparticles, showing similarities and important differences with the behavior of other polysaccharides and protein filaments. This knowledge will be crucial to fully understand and exploit the unique hydration properties of this promising natural nanomaterial.

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(7) Rand, R. P.; Parsegian, V. A. Hydration forces between phospholipid bilayers. Biochim. Biophys. Acta, Rev. Biomembr. 1989, 988, 351−376. (8) Leikin, S.; Parsegian, V. A.; Yang, W.-H.; Walrafen, G. E. Raman spectral evidence for hydration forces between collagen triple helices. Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 11312−11317. (9) Derjaguin, B. V. Theory of Stability of Colloids and Thin Films; Springer: New York, 1989. (10) Rehfeldt, F.; Tanaka, M. Hydration Forces in Ultrathin Films of Cellulose. Langmuir 2003, 19, 1467−1473. (11) Rehfeldt, F.; Tanaka, M.; Pagnoni, L.; Jordan, R. Static and Dynamic Swelling of Grafted Poly(2-alkyl-2-oxazoline)s. Langmuir 2002, 18, 4908−4914. (12) Wong, J. E.; Rehfeldt, F.; Hänni, P.; Tanaka, M.; Klitzing, R. V. Swelling behavior of polyelectrolyte multilayers in saturated water vapor. Macromolecules 2004, 37, 7285−7289. (13) Tanaka, M. Physics of interactions at biological and biomaterial interfaces. Curr. Opin. Colloid Interface Sci. 2013, 18, 432−439. (14) Israelachvili, J. N. Intermolecular and Surface Forces; Academic Press: London, 1992. (15) Meléndez, R.; Meléndez-Hevia, E.; Cascante, M. How Did Glycogen Structure Evolve to Satisfy the Requirement for Rapid Mobilization of Glucose? A Problem of Physical Constraints in Structure Building. J. Mol. Evol. 1997, 45, 446−455. (16) Powell, P. O.; Sullivan, M. A.; Sweedman, M. C.; Stapleton, D. I.; Hasjim, J.; Gilbert, R. G. Extraction, isolation and characterisation of phytoglycogen from su-1 maize leaves and grain. Carbohydr. Polym. 2014, 101, 423−431. (17) Putaux, J.-L.; Buléon, A.; Borsali, R.; Chanzy, H. Ultrastructural aspects of phytoglycogen from cryo-transmission electron microscopy and quasi-elastic light scattering data. Int. J. Biol. Macromol. 1999, 26, 145−150. (18) Ball, S.; Guan, H.-P.; James, M.; Myers, A.; Keeling, P.; Mouille, G.; Buléon, A.; Colonna, P.; Preiss, J. From Glycogen to Amylopectin: A Model for the Biogenesis of the Plant Starch Granule. Cell 1996, 86, 349−352. (19) Nickels, J. D.; Atkinson, J.; Papp-Szabo, E.; Stanley, C.; Diallo, S. O.; Perticaroli, S.; Baylis, B.; Mahon, P.; Ehlers, G.; Katsaras, J.; Dutcher, J. R. Structure and Hydration of Highly-Branched, Monodisperse Phytoglycogen Nanoparticles. Biomacromolecules 2016, 17, 735−743. (20) Grossutti, M.; Dutcher, J. R. Correlation between Chain Architecture and Hydration Water Structure in Polysaccharides. Biomacromolecules 2016, 17, 1198−1204. (21) Dalnoki-Veress, K.; Forrest, J. A.; Murray, C.; Gigault, C.; Dutcher, J. R. Molecular Weight Dependence of Reductions in the Glass Transition Temperature of Thin, Freely Standing Polymer Films. Phys. Rev. E: Stat., Nonlinear, Soft Matter Phys. 2001, 63, 031801. (22) Murray, C. A.; Dutcher, J. R. Effect of Changes in Relative Humidity and Temperature on Ultrathin Chitosan Films. Biomacromolecules 2006, 7, 3460−3465. (23) Azzam, R. M. A.; Bashara, N. M. Ellipsometry and Polarized Light; North-Holland: Amsterdam, 1977. (24) Tanaka, M. Cell Surface Models on Polymer SupportsFrom Artificial Membranes to Native Cells. In Advances in Planar Lipid Bilayers and Liposomes; Ottova-Leitmannova, A., Ed.; Elsevier: Amsterdam, 2005; Vol. 2, pp 95−120. (25) Vettori, M. H. P. B.; Franchetti, S. M. M.; Contiero, J. Structural characterization of a new dextran with a low degree of branching produced by Leuconostocmesenteroides FT045B dextransucrase. Carbohydr. Polym. 2012, 88, 1440−1444. (26) Ioan, C. E.; Aberle, T.; Burchard, W. Structure Properties of Dextran. 2. Dilute Solution. Macromolecules 2000, 33, 5730−5739. (27) Ioan, C. E.; Aberle, T.; Burchard, W. Light Scattering and Viscosity Behavior of Dextran in Semidilute Solution. Macromolecules 2001, 34, 326−336. (28) Pappenheimer, J. R.; Renkin, E. M.; Borrero, L. M. Filtration, diffusion and molecular sieving through peripheral capillary mem-

ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.langmuir.7b00025. Additional technical details and six supporting data figures (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. ORCID

John R. Dutcher: 0000-0003-2594-5388 Notes

The authors declare the following competing financial interest(s): One of the authors (J.R.D.) is a founder of Mirexus Biotechnologies.

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ACKNOWLEDGMENTS

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REFERENCES

Mirexus Biotechnologies Inc. generously supplied the monodisperse phytoglycogen nanoparticles. This work was funded by grants from the Ontario Ministry of Agriculture (OMAF) and the Natural Sciences and Engineering Research Council (NSERC) of Canada. J.R.D. is the recipient of a Senior Canada Research Chair in Soft Matter and Biological Physics.

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