Synergistic Foaming and Surface Properties of a Weakly Interacting

Article pubs.acs.org/JAFC

Synergistic Foaming and Surface Properties of a Weakly Interacting Mixture of Soy Glycinin and Biosurfactant Stevioside Zhi-Li Wan,† Li-Ying Wang,† Jin-Mei Wang,† Yang Yuan,† and Xiao-Quan Yang*,†,‡ †

Research and Development Center of Food Proteins, Department of Food Science and Technology, South China University of Technology, Guangzhou 510640, People’s Republic of China ‡ State Key Laboratory of Pulp and Paper Engineering, South China University of Technology, Guangzhou 510640, People’s Republic of China S Supporting Information *

ABSTRACT: The adsorption of the mixtures of soy glycinin (11S) with a biosurfactant stevioside (STE) at the air−water interface was studied to understand its relation with foaming properties. A combination of several techniques such as dynamic surface tension, dilatational rheology, fluorescence spectroscopy, and isothermal titration calorimetry (ITC) was used. In the presence of intermediate STE concentrations (0.25−0.5%), the weak binding of STE with 11S in bulk occurred by hydrophobic interactions, which could induce conformational changes of 11S, as evidenced by fluorescence and ITC. Accordingly, the strong synergy in reducing surface tension and the plateau in surface elasticity for mixed 11S−STE layers formed from the weakly interacting mixtures were clearly observed. This effect could be explained by the complexation with STE, which might facilitate the partial dissociation and further unfolding of 11S upon adsorption, thus enhancing the protein−protein and protein−STE interfacial interactions. These surface properties were positively reflected in foams produced by the weakly interacting system, which exhibited good foaming capacity and considerable stability probably due to better response to external stresses. However, at high STE concentrations (1−2%), as a consequence of the interface dominated by STE due to the preferential adsorption of STE molecules, the surface elasticity of layers dramatically decreased, and the resultant foams became less stable. KEYWORDS: soy glycinin, stevioside, synergistic effects, foam, surface properties

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INTRODUCTION Many processed food products consist of foams, such as whipped cream, mousses, beers, breads, and cakes. The formation and stabilization of multiphase foamed systems strongly depend on the properties of surface active components in foaming agents.1−6 Proteins and low-molecular weight (LMW) surfactants are two major types of food-grade surface-active substances. LMW surfactants facilitate the foaming process by quickly and effectively lowering surface tension.1,4 Conversely, proteins stabilize foams on longer time scales by forming highly elastic networks on the bubble surface.1,6,7 However, often quite high protein concentrations are required for foam preparation.5,8 Therefore, in practice, mixtures of proteins and LMW surfactants are widely utilized in most commercial formulations.1,3,4 Accordingly, synergistic or antagonistic effects in protein−LMW surfactant mixtures often occurred due to mutual interactions between both molecules. The interactions between proteins and LMW surfactants have been extensively studied by many researchers due to their strong influence on foaming properties.1,3,9 The interaction types can be divided into relatively weak interactions (mainly hydrophobic forces) or strong electrostatic interactions, which generally depend on the nature of proteins and LMW surfactants.9,10 Proteins interact differently with surfactant monomers and micelles, and the interactions can modify the conformation of protein molecules and the aggregation properties of LMW surfactants, respectively.11,12 Also, the protein−LMW surfactant interactions are different in the bulk and at the interface, which result in the complexes with © 2014 American Chemical Society

different surface activities leading to different surface adsorption properties.3,12,13 In addition, increasing the concentration of LMW surfactants in mixtures affects the complexation processes and the complex characteristics, which subsequently change surface layer composition, as the LMW surfactants will gradually displace the proteins from the interface due to competition adsorption. For LMW surfactant concentrations high enough, proteins contribute little to the surface properties.14−17 To date, most of the studies on protein−LMW surfactant mixtures are mainly focused on petroleum-derived synthetic surfactants,3,12 such as dodecyltrimethylammonium bromide (DTAB) and sodium dodecyl sulfate (SDS). However, the replacement of synthetic surfactants with natural alternatives of biological origin (biosurfactants) has attracted increasing interest in the research field of food and pharmaceutics due to their low toxicity and intrinsic biodegradability. Triterpenoid saponins, plant-derived biosurfactants, have exhibited strong surface activity and are commonly used as efficient foam and emulsion stabilizers in the food industry.18 Most recently, Stanimirova et al.19 and Golemanov et al.20,21 reported that the triterpenoid saponins formed adsorption layers at the air−water interface with high surface elasticity, which attracted currently great research interest. In addition, the adsorption kinetics of Received: Revised: Accepted: Published: 6834

April 29, 2014 June 22, 2014 June 23, 2014 June 23, 2014 dx.doi.org/10.1021/jf502027u | J. Agric. Food Chem. 2014, 62, 6834−6843

Journal of Agricultural and Food Chemistry

Article

cm) at room temperature (25 °C). The absence of surface active contaminants in the phosphate buffer was checked by surface tension measurements before sample preparation. No aqueous solutions with a surface tension other than that accepted in the literature (72−73 mN/ m at 25 °C) were used. The 11S globulin solution was prepared by dispersing the freeze-dried protein in 10 mM phosphate buffer (pH 7.0) for 2 h under mild magnetic stirring and then was left overnight at 4 °C to allow complete hydration. All measurements were made at constant 11S concentration (0.1 wt %) and varying STE concentration (0−2 wt %) at pH 7.0. The mixed 11S−STE systems were obtained by mixing the appropriate volume of each double concentrated 11S and STE solutions up to the required concentration and stirring for a further 30 min before any measurements. Fluorescence Spectroscopy Measurements. To investigate the effect of STE addition on the intrinsic fluorescence of 11S, fluorescence spectra of solutions containing a fixed 11S concentration (1 mg/mL) and different STE concentrations in 10 mM phosphate buffer (pH 7.0) were recorded using an F7000 fluorescence spectrophotometer (Hitachi Co., Japan) at 25 °C. The excitation wavelength was set at 295 nm, and the emission spectra were collected from 310 to 500 nm. Both the excitation and emission slit widths were set at 5 nm. The reference sample consisting of the phosphate buffer and STE was checked for fluorescence signals. The data on the tryptophan (Trp) fluorescence quenching were analyzed according to the Stern−Volmer equation (eq 1):

mixtures of proteins and a biosurfactant Quillaja Bark Saponin at the air−water and oil−water interfaces have also been described in detail by Wojciechowski and co-workers.22−24 Recently, we reported that natural sweetener stevioside (STE), the most abundant component of steviol glycosides, exhibited a notable surface activity and could also be developed into a new type of biosurfactant.25 The emulsions prepared by the mixtures of soy protein isolate (SPI) and STE showed a remarkable physical stability with small oil droplet size of ∼220 nm.25 STE is a diterpene ent-kaurene glycoside, which consists of a hydrophobic headgroup, called diterpenoid or steviol backbone, with hydrophilic glucosyl and sophorosyl residues. The amphiphilic structure of STE molecules is similar to that of triterpenoid saponins, thus determining their potential capability as biosurfactants. Moreover, STE also exhibits many nontrivial biological activities, such as antitumor progression and antihyperglycemic and immunomodulatory effects.26 In another recent work,27 we further found that the soy protein−STE mixtures displayed interesting competition adsorption behavior by their mutual interactions at the interface, which were positively reflected in the corresponding emulsions with the long-term stability. All these present works to a large extent support the capability of STE as a new biosurfactant and further research on the mixed protein−STE systems due to their potential practical applications as foam/ emulsion formulations. Considering the fact that the behavior of adsorbed layers at the air−water interface obviously differs from that at the oil− water interface due to their different degrees of polarity and hydrophobicity,3,5,12 which can strongly influence the properties of respective foams and emulsions, it is therefore of interest to further study the adsorption of soy protein−STE mixtures at the air−water interface and their relation to the corresponding foaming characteristics. Moreover, to the best of our knowledge, no report about the interactions between protein and STE in the bulk and at the air−water interface has been found to date. Thus, in this work, we focus on the adsorption of soy protein−STE mixtures at the air−water interface by using a combination of dynamic surface tension and dilational rheological studies. The soy glycinin (11S), the major and pure globulin of soybeans, is employed in this study because of its structural and functional properties extensively studied. The bulk 11S−STE interactions are first investigated by fluorescence spectroscopy and isothermal titration calorimetry (ITC) measurements to helpfully understand surface behavior of the mixtures. Subsequently, the foamability and foam stability in mixed 11S−STE systems are determined, and a possible stabilization mechanism is finally proposed to clarify the correlation between surface behavior and the actual foaming properties.

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F0/F = 1 + kqτ0[Q ] = 1 + KSV[Q ] In this equation F0 and F are the fluorescence intensities in the absence and presence of a quencher, respectively, [Q] is the quencher concentration, KSV is the Stern−Volmer quenching constant, kq is the bimolecular quenching rate constant, and τ0 is the lifetime of fluorescence in absence of a quencher. Hence, KSV was determined by linear regression of a plot of F0/F versus [Q] according to eq 1. Pyrene was used as the fluorescence probe to determine the micropolarity of STE with and without 11S solution (1 mg/mL). Each spectrum was measured in the wavelength range 350−500 nm with the excitation wavelength being 335 nm. The excitation and emission slit widths were set at 5 and 2.5 nm, respectively. The intensity ratio of I373 to I385 of the pyrene fluorescence spectrum shows the micropolarity where the probe exists. The final concentration of pyrene in each sample was 6.0 × 10−7 M. Isothermal Titration Calorimetry (ITC). The ITC measurements were performed in a Nano ITC Low Volume instrument (TA Instruments, Newcastle, DE) at 25 °C. In a typical experiment, 250 μL 11S solution (1 mg/mL) was inserted into the sample cell, and the syringe was filled with 50 μL of STE solution (50 mg/mL). All solutions were prepared in phosphate buffer (10 mM, pH 7.0) and were degassed before each titration. After reaching equilibrium, STE solution was titrated into the sample cell as a sequence of 25 injections of 2 μL aliquots. The time delay between successive injections was 350 s. The contents of the sample cell were stirred throughout the experiment at 250 rpm to ensure thorough mixing. Control experiments included the titration of STE into buffer, buffer into protein, and buffer into buffer. The last two controls resulted in small and equal enthalpy changes for each successive injection of buffer and, therefore, were not further considered in the data analysis. Corrected raw data refer to experimental data after subtraction of the STE into buffer control data. The corrected data obtained as a plot of heat flow (μcal s−1) against time (min) were then integrated peak-by-peak and normalized to obtain a plot of observed enthalpy change per mole of STE (ΔH, kcal mol−1) against the STE concentration (mM). The experimental data were further fitted to the one-site independent binding model using the TA Nano Analyzer software, providing the thermodynamic parameters Ka (binding constant), ΔH (enthalpy change), ΔS (entropy change), and n (number of STE molecules bound per mole of 11S). Dynamic Surface Properties Measurements. The dynamic surface properties of 11S, STE, and 11S−STE mixtures at the air−

MATERIALS AND METHODS

Materials. STE (purity >95%) was purchased from Jining Aoxing Stevia Products Co., Ltd., China. Pyrene was purchased from SigmaAldrich (St. Louis, MO). Defatted soy flour was provided by Shandong Yuwang Industrial and Commercial Co., Ltd., China. The protein content of soy flour was 55.10% (determined by micro-Kjeldahl method, N × 6.25, dry basis). 11S globulin was prepared as described by Yuan et al.28 Protein content of 11S globulin was 96.29%, determined by Dumas method (N × 6.25) in a Rapid N Cube (Elementar France, Villeurbanne, France). All other chemicals used were of analytical grade. Sample Preparation. All samples were prepared in 10 mM phosphate buffer solution (pH 7.0) using ultrapure water (18.2 MΩ· 6835

dx.doi.org/10.1021/jf502027u | J. Agric. Food Chem. 2014, 62, 6834−6843


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water interface were monitored by recording temporal evolution of surface pressure and surface dilatational parameters using an optical contact angle meter (OCA-20, DataPhysics Instruments GmbH, Germany) equipped with oscillating drop accessory (ODG-20), as described elsewhere.30 All the experiments were carried out at 25 °C. The solutions were placed in the syringe and were allowed to equilibrate for 30 min to reach the desired constant temperature before the measurements. The drop of sample solution was formed in a rectangular glass cuvette. The cuvette was sealed with a Parafilm M laboratory film (Pechiney Plastic Packaging Company, U.S.A.) and partially filled with the solution under test to saturate the air surrounding the drop and reduce the water evaporation, which could decrease the drop volume and thus falsify the test. Dynamic Surface Tension. A drop of sample solution (12 μL) was delivered and allowed to stand for 180 min to achieve adsorption at the air−water interface. An image of the drop was continuously recorded by a CCD camera and digitalized. The surface tension (γ) was calculated through the shape analysis of a pendant drop according to the Young−Laplace equation analysis. The surface pressure is π = γ0 − γ, where γ0 is the surface tension of phosphate buffer (10 mM, pH 7.0) and γ is the time-dependent surface tension of the tested solutions. The average standard accuracy of the surface tension for at least three measurements with different drops was roughly 0.5 mN/m. Dilatational Rheological Properties. To obtain surface dilatational parameters, sinusoidal interfacial compression and expansion were performed by decreasing and increasing the drop volume at 10% of deformation amplitude (ΔA/A) and 0.1 Hz of angular frequency (ω). The drop was subjected to repeated measurements of five sinusoidal oscillation cycles followed by a time corresponding to 50 cycles without any oscillation up to 180 min required to complete adsorption. Details of this experiment are given elsewhere.31,32 The surface viscoelastic parameters, i.e., surface dilatational modulus, E, its elastic, Ed, and viscous, Ev, components were derived from the change in surface tension (γ) (dilatational stress) resulting from a small change in surface area (dilatational strain). The surface dilatational modulus (E) is a complex quantity and composed of real and imaginary parts (E = Ed + iEv). The real part of the dilatational modulus or storage component is the dilatational elasticity (Ed). The imaginary part of the dilatational modulus or loss component is the surface dilatational viscosity (Ev). Foam Formation and Stability Measurements. The foaming properties of pure STE and 11S−STE mixtures were characterized through their foam formation and stability measured in a Foam Tester R2000 instrument (SITA Messtechnik, GmbH, Germany) at 25 °C, as described elsewhere.33 In all experiments, the used volume of the foaming solutions was 300 mL. The same 11S and STE concentrations were used as in the surface properties study. Every foam test consisted of two cycles, namely, the foam generation and foam decay. Foams were generated by stirring the solutions at 1000 rpm and stopping every 10 s to measure the foam volume by the sensor unit. After 15 such cycles, the foam generation stopped and the foam was left to decay. During decaying, the foam volume was measured for every 1 min. The height of the foam column (mL) in a generation period is taken as a measure of the foamability. The stability of the foam is estimated by measuring the half-life (t1/2, min) of the foam, the time taken for the height to decay to half of the maximum. Statistical Analysis. Unless specified otherwise, three independent trials were performed, each with a new batch of sample preparation. All measurements were carried out in triplicate, and an analysis of variance (ANOVA) of the data was performed using the SPSS 19.0 statistical analysis system. Duncan Test was used for comparison of mean values among three treatments using a level of significance of 5%.

mixtures, the bulk 11S−STE interactions were thus studied by fluorescence spectroscopy and ITC, as shown in Figures 1 and 2.

Figure 1. (A) Effect of STE on the intrinsic Trp fluorescence of 11S (1 mg/mL). The inset shows the Stern−Volmer plots describing fluorescence quenching of 11S in the presence of STE. (B) Pyrene fluorescence intensity ratios I373/I385 in different STE concentrations with (CMC2) and without (CMC) 11S. CMC: critical micelles concentration.

Effect of STE on Trp Intrinsic Fluorescence. Figure 1A shows the effect of STE on the Trp intrinsic fluorescence emission spectrum of 11S. The pure 11S exhibited an emission spectrum centered at around 335 nm. For STE concentrations below 1 mg/mL, there were no changes on the fluorescence intensity of 11S, indicating no obvious 11S−STE interactions. Addition of increasing STE concentrations from 2.5 mg/mL to 20 mg/mL gave rise to a progressive quenching of Trp fluorescence of 11S. Data fitting to eq 1 allowed determination of the Stern−Volmer quenching constant. As shown in the inset of Figure 1A, the value of kq (8.29 × 109 M−1 s−1) is much lower than the maximal dynamic quenching constant (2.0 × 1010 M−1 s−1), indicating that the fluorescence quenching induced by STE is dynamic quenching.29 This is in agreement with our previous study,25 suggesting that STE cannot act as a direct Trp fluorescence quencher. Thus, this fluorescence attenuation should be the consequence of STE-induced protein

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RESULTS AND DISCUSSION Interactions between 11S and STE in Bulk Solution. The interaction between proteins and LMW surfactants in bulk solution is usually believed to influence the properties of surface layers and thus the formation and stability of foams.12,13 Herein, to helpfully understand the adsorption behavior of the 6836



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This result is in good agreement with the analysis of Trp intrinsic fluorescence (Figure 1A). The critical micelle concentration (CMC) of STE was determined from the threshold concentration, where the pyrene I373/I385 begins to change markedly.35,36 Therefore, the CMC values of STE in the absence and presence of 11S were determined as 4.20 mg/mL (CMC) and 5.75 mg/mL (CMC2), respectively. The higher CMC value of STE in the presence of 11S revealed that there was interaction between 11S and STE, which sequestered STE molecules and reduced the concentration of free monomeric STE, thus increasing the STE concentration for formation of free micelles.11 This result further supported previous analysis of Trp intrinsic fluorescence (Figure 1A). ITC. The interaction between 11S and STE was further quantitatively studied by ITC, as shown in Figure 2. Upon injecting aliquots of STE solution (around 12 times above the CMC of STE) into 11S solution, the corrected heat trace peaks in Figure 2A demonstrated exothermic enthalpy released in the titration process, which should be caused by the binding of STE to 11S. On the basis of the fluorescence measurements (Figure 1), we can thus conclude that, upon the presence of STE micelles, STE could actually bind to the 11S cooperatively, forming the micelle-like clusters at the surface of 11S, thus resulting in the formation of exothermic peaks. Furthermore, with increasing STE addition, a decrease in exothermic peaks was observed (Figure 2A), suggesting the number of available binding sites on the 11S decreased. Once the protein became saturated with STE, the addition of more STE led to a plateau in the exothermic peaks (Figure 2A). The thermodynamic parameters were determined from the titration curve in Figure 2B. The binding ratio (n) was calculated to be 686 (±12), suggesting that 11S became saturated with 686 molecules of monomer STE bound per molecule of 11S. The binding ratio value was higher than those observed for the interactions between β-lactoglobulin and different types of LMW surfactants, such as SDS, alkyl trimethylammonium chlorides, or alkyl maltopyranosides.11,37 This high binding ratio further supported the formation of STE clusters or micelles at the surface of 11S, in agreement with the Trp intrinsic fluorescence analysis (Figure 1A). Moreover, the larger molecular size of 11S (∼360 kDa) could also provide a greater number of binding sites for STE. Interactions with binding constant Ka > 104 M−1 are considered to be of high affinity.38 Thus, the binding constant (Ka = 1.31 × 103 ± 0.23 × 103 M−1) observed in this study indicated that binding of STE with 11S was much weaker, probably suggesting a nonspecific interaction.34 In addition, the binding entropy was positive (ΔS = 40.67 ± 4.06 kJ mol−1 K−1), indicating that the interaction was mostly driven by entropy. Since it is generally accepted that an entropy-driven reaction mainly involves hydrophobic interactions,34,38 the present result suggested that STE binding to 11S should be mainly driven by interacting unspecifically with hydrophobic domains of 11S, which was again in line with the results of Trp intrinsic fluorescence (Figure 1A). Similar findings on the interaction of trehalose lipid biosurfactant with BSA were observed.34 Surface Behavior of 11S−STE Mixtures. Dynamic Surface Tension. The time evolution of surface tension (γ) for 11S−STE mixtures at the air−water interface is shown in Figure 3A. In all cases, the surface tension values gradually decreased with adsorption time, which can be associated with the surface-active substances adsorption at the interface. For pure 11S, it can be observed that the surface was already

Figure 2. ITC determination of the binding of STE to 11S. (A) Heat flows recorded upon injection of STE solution (50 mg/mL) into 11S solution (1 mg/mL) at 25 °C. (B) Molar heat values obtained through integration of the individual heat flow signals as a function of the STE concentration. The solid line is the theoretical fit.

conformational changes. A similar behavior has been observed for the interaction of trehalose lipid biosurfactant with BSA.34 In addition, as the concentration of STE was increasing from 7.5 mg/mL to 20 mg/mL (above the CMC of STE, see Figure 1B), the maximum emission wavelength underwent a moderate blue shift from 335 to 332 nm, revealing the movement of the Trp residues into a more hydrophobic environment, which was probably due to the interaction with hydrophobic portions of STE molecules (monomers and micelles). Pyrene Fluorescence. The fluorescence emission of hydrophobic pyrene probe is sensitive to its microenvironmental polarity. A lower I373/I385 value stands for higher hydrophobicity of the microenvironment. Upon micellization, pyrene partitions into or close to the hydrophobic interior of micelles, and consequently the intensity ratio I373/I385 is changed.35,36 The changes of the I373/I385 values on the logarithm of STE concentrations with and without 11S were recorded and shown in Figure 1B. As can be seen, for STE concentrations below 1 mg/mL, compared to pure STE, 11S−STE mixtures showed lower I373/I385 values, suggesting a higher hydrophobicity of the microenvironment, which was due to the hydrophobic domains in 11S. Moreover, no significant difference (p > 0.05) in the I373/I385 values was observed when compared with that of pure 11S (1.54), indicating that there might be no obvious 11S−STE interactions when STE concentration was below 1 mg/mL. 6837



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(2%) coincided with that of pure 2% STE, which indicated that the interface was completely dominated by STE. Surface Dilatational Rheology. The dynamic dilatational properties for pure and mixtures of 11S and STE are shown in Figure 4. The evolution of the dilatational modulus was

Figure 3. (A) Surface tension (γ) as a function of time for mixed solutions of 0.1% 11S with different STE concentrations (0−2%) at the air−water interface. (B) Surface tension versus the concentration of STE for solutions with and without 0.1% 11S. The values represent the surface tension after 180 min of adsorption. Figure 4. (A) Time-dependent dilatational elasticity (Ed) for adsorbed layers formed from mixed solutions of 0.1% 11S with various amounts of STE (0−2%) at the air−water interface. (B) Surface dilatational modulus (E) plotted as a function of surface pressure (π) for the above mixed solutions. Frequency: 0.1 Hz. Amplitude of deformation: 10%.

saturated at the present bulk concentration (0.1%), in agreement with previous studies.15,31,39 For 11S−STE mixtures, at low STE concentration (0.1%), the surface tension decay showed a very similar trend as compared to pure 11S, indicating that the surface layer was mainly dominated by 11S. However, with increasing STE concentrations to intermediate level (0.25 and 0.5%), especially at 0.5% STE, the surface tension decay curves started to differentiate markedly when compared to that of pure 11S, where a significant increase in the decay rate was observed. Upon the further increase of STE concentration (1 and 2%), an obvious slowing down of surface tension decay was found as compared with that of 0.5% STE. Moreover, the dynamic curve of the mixture (2%) started to resemble that for 2% pure STE (Figure 3A). The surface tension after 180 min of adsorption from mixed 11S and STE systems is compared to the corresponding values for pure STE in Figure 3B. The surface tension value for pure 11S was 46.0 mN/m after 180 min, which is in consistent with previously reported results.15,31 With increasing STE concentrations from 0.1% to 0.5%, an obvious decrease in surface tension values was found. Furthermore, it is noteworthy that the surface tension values of mixtures were always lower than those of pure 11S and STE, indicating mixed 11S−STE surface layers were formed. However, with increasing STE concentrations from 1% to 2%, the surface tension values of mixtures started to increase again, suggesting the decreased surface activity. Moreover, the surface tension value of the mixture

followed at the frequency of 0.1 Hz, which was tuned to give a good response for soy globulin, as it allows the collection of enough data points within the present adsorption time.15,31,39 In all cases, it can be noticed that (data not shown) the values for surface dilatational modulus (E) were very similar to those for the dilatational elasticity (Ed), and the dilatational viscosity (Ev) values were low. Thus, from a rheological point of view, these results suggested the surface layers behaved as viscoelastic (primarily elastic) during the adsorption period studied here.15 Figure 4A presents the dynamic elastic modulus (Ed) of surface layers during the adsorption of 11S−STE mixtures. In all cases, the gradual increase in Ed with adsorption time should be associated with the adsorption of surface-active components at the interface. For pure 11S, the Ed increased gradually with time to reach 49.5 mN/m after 180 min, which is similar to those found by others,15,31,39 implying that strong viscoelastic interfacial networks were formed mainly due to a combined effect of protein adsorption and development of strong intermolecular interactions and conformation changes at the interface.1,15,31,40 With increasing amounts of STE in mixtures, even at low STE concentration (0.1%), the Ed clearly decreased as compared to that of pure 11S. This should be mainly due to 6838



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Foaming Properties of 11S−STE Mixtures. On the basis of the characterization of surface layers, we attempted to relate these findings to the properties of macroscopic foams formed from 11S−STE mixtures with the same compositions as used in the surface properties study. Thus, the foamability and foam stability of 11S−STE mixtures were measured, as shown in Figures 5 and 6, respectively.

the fact that the presence of STE could break down the protein intermolecular interactions, thus weakening the film and reducing the viscoelastic properties.1,41 Similar findings were also reported for soy globulins/Tween 20 and hen egg-white lysozyme/C10DMPO mixtures at the air−water interface.14,15 Nevertheless, at intermediate STE concentrations (0.25 and 0.5%), it is very interesting to note that no marked difference in Ed values with increasing STE concentrations was observed. This result revealed that mixed 11S−STE surface layers showed a plateau in the elastic behavior within the STE concentration range. With the further increase in STE concentration (1 and 2%), the Ed values started to decrease again. At high STE concentration of 2%, the Ed value of the mixture was very close to that of 2% pure STE, which led to the conclusion that the interface was predominantly covered by STE. This result is in line with dynamic surface tension analysis (Figure 3). On the other hand, all pure STE samples (0.1−2%) showed very low Ed values (around 5.0−8.0 mN/m) (data not shown), indicating the interface stabilized by pure STE exhibited a low elasticity. Similar behaviors were also observed for many other LMW surfactants.1,3,15,40 The evolution of E with π in the surface layer for the adsorption of 11S−STE mixtures is shown in Figure 4B. The curve of E versus π generally reflects the surface equation of state of the adsorbed material at the interface, and if the E is only due to the amount of surface-active components adsorbed at the interface, all E data should be normalized in a single master curve of E versus π.42 For pure 11S, it can be seen clearly that E increased almost immediately with increasing π value, and this dependence reflects the existence and the increase of interactions between the adsorbed protein residues. Moreover, E was higher at longer adsorption times, in line with the theory of Lucassen−Reynders.43 The slope (2.49) of the E−π plot was higher than 1 (represented by the dotted line in Figure 4B), which implied an important nonideal behavior for higher molecular interactions between the adsorbed proteins compared with those for an ideal behavior.43 With increasing STE concentrations from 0.1% to 1%, all the slopes of E−π plots were higher than 1, revealing an important nonideal behavior with higher molecular interactions between filmforming components. The low STE concentration (0.1%) showed a slope value of 2.51, which was similar to that of pure 11S (2.49), indicating that the interface was mainly dominated by 11S. This is consistent with the dynamic surface tension analysis (Figure 3). In addition, it is worth noting that, the mixtures with STE concentrations of 0.25% and 0.5% also exhibited high slope values of 2.15 and 2.11, respectively, which suggested the presence of high molecular interactions between the adsorbed 11S and STE at the interface. However, with further increasing STE concentrations (1 and 2%), the slope values started to decrease. At high STE concentration (2%), the E−π plot partially overlapped with that of 2% pure STE, and the slope (1.29) was also very close to that of pure STE (1.18). These results indicated that the adsorption layer was formed mainly by STE, which again are in good agreement with previous analysis (Figures 3 and 4A). In addition, in all cases of pure STE (0.1−2%), the slope values of E−π plots were around 1 (characteristic of the behavior of an ideal gas) (data not shown), thus revealing the E is only due to the amounts of STE adsorbed at the interface without apparent STE−STE interfacial interactions, in line with their behaviors at the oil− water interface.27

Figure 5. Maximum foam volume obtained from the solutions of pure STE (0.1−2%) and mixtures of 0.1% 11S with various amounts of STE (0−2%).

Figure 6. (A) Foam volume as a function of time for the solutions of pure STE (0.5−2%) and mixtures of 0.1% 11S with various amounts of STE (0−2%). (B) Half-life (t1/2) of the foams formed by pure STE (0.1−2%) and the above mixed solutions. 6839



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Foamability. Foam formation is influenced by the adsorption of foaming agents at the air−water interface and their ability to reduce surface tension.3,9,44,45 The maximum foam volume for different systems was measured to assess their foamability (Figure 5). As shown in Figure 5, pure 11S exhibited a low foam volume, suggesting a very poor foaming capacity. This might be due to the large size and close-packed globular conformation of 11S,46 which hindered its rapid adsorption at the interface during foaming, thus impairing the foaming capacity. The high initial surface tension value of 11S supported this analysis (Figure S, Supporting Information [SI]). This is in line with previous study,46 which suggested that high 11S concentration (2% or more) was required to make good foams. Compared to that of pure 11S, even at the addition of low STE concentration (0.1%), the maximal foam volume was significantly increased. Moreover, with increasing STE concentration from 0.1% to 0.5%, a gradual increase in the maximal foam volume was observed, suggesting the improved foaming capacity. This improving effect should be due to the greater ability for the mixtures to lower surface tension (Figure 3), hence, facilitating the foaming process. In the presence of high STE concentrations (1 and 2%), no significant difference (p > 0.05) in the maximal foam volume was observed when compared to that of the mixture containing 0.5% STE. This result should be mainly attributed to their similar initial surface tension values (Figure S, SI). On the other hand, at the same concentration (0.1%), the foamability of pure STE was better than that of pure 11S (Figure 5), which should be due to the fast adsorption of STE at the interface and thus the lower initial surface tension (Figure S, SI), which could contribute to foamability. Meanwhile, under STE concentration range from 0.1% to 0.5%, the 11S−STE mixtures exhibited a higher foaming capacity as compared to pure STE. However, at high STE concentrations (1 and 2%), the foamability results for pure STE and the mixed systems were very similar. These results perfectly matched the general trends seen in initial surface tension data (Figure S, SI), suggesting a strong relationship between the foamability and the initial surface tension of foaming agents. Foam Stability. Foams are thermodynamically unstable, and their relative stability is governed by factors such as liquid drainage, coarsening, and coalescence.47 To evaluate the foam stability, the foam volume versus time after foam generation and the half-life time (t1/2) of foams were measured, as presented in A and B of Figure 6, respectively. In all cases, it can be clearly seen that, despite the poor foaming capacity (Figure 5), the foam formed by pure 11S exhibited the lowest foam decay rate (Figure 6A) and the maximum value of t1/2 at 115 min (Figure 6B), indicating pure 11S-stabilized foam was very stable against bubble coarsening and coalescence. With increasing STE concentration from 0.1% to 0.5%, compared to those of pure 11S, the rate of foam decay was slightly increased (Figure 6A), and the formed foams also had slightly lower t1/2 values (Figure 6B). These results suggested that, under the STE concentration range (0.1−0.5%) used, the 11S−STE mixtures could still make relatively stable foams. Moreover, it is worth noting that, despite increasing STE concentrations from 0.25% to 0.5%, no significant difference (p > 0.05) was observed in foam decay rates and t1/2 values. Also, the decay curve of 0.25% practically overlapped with that of 0.5% (Figure 6A). These results indicated that the foams formed by 11S−STE mixtures (0.25 and 0.5%) showed very similar stability. However, at high STE concentrations (1 and 2%), with increasing STE

concentration, the dramatic increase in decay rates and decrease in t1/2 values were observed, respectively. Moreover, the decay curve and t1/2 value started to be close to those of pure STE. These results completely reproduced the general trends observed in the data from surface properties (Figures 3 and 4); therefore, it can be concluded that interfacial results might be correlated to foam stability. On the other hand, despite the good foaming capacity of pure STE (Figure 5), the foams formed by pure STE in the studied concentration range (0.1− 2%) showed very poor stability, as evidenced by high foam decay rates and low t1/2 values (Figure 6). Similar behavior was observed in foams stabilized by many other LMW surfactants.1,15 General Discussion. Here, the results obtained at different scales, from the molecular to the macroscopic point of view, are discussed to try to provide understanding of the mechanism underlying the foamability and foam stability for 11S−STE mixed systems. On the basis of the results of surface tension (Figure 3), it is thus reasonable to speculate that, at intermediate STE concentrations (0.25 and 0.5%), a strong synergy in reducing the surface tension was observed in 11S− STE mixtures, in agreement with the previous study where similar behavior was seen at the oil−water interface.27 This effect could be explained by the formation of 11S−STE complex at the adsorbed layer, which might possess higher surface activity than that of the individual components (Figure 3B). This speculation is supported by the results of fluorescence spectroscopy and ITC (Figures 1 and 2), which indicated that the 11S−STE complex was formed already in the bulk prior to its adsorption at the interface. The obvious binding of STE with 11S in bulk occurred mainly by nonspecific hydrophobic interactions when STE concentration was above 1 mg/mL (Figures 1 and 2). The binding is rather weak, as evidenced by ITC analysis (Figure 2), but appears to be sufficiently intense to result in the conformational changes of 11S (Figure 1A). Therefore, we can conclude that the complexation with STE might promote the partial dissociation of protein and loosen its rigid structure, which would facilitate further unfolding of 11S upon reaching the interface, thus increasing the surface tension decay rate (Figure 3A). Similar phenomena were reported in the mixtures of β-lactoglobulin/βcasein and Quillaja Bark Saponin.23,24 On the other hand, at low STE concentration (0.1%), complexation of a small amount of STE could not change the protein conformation markedly (Figures 1 and 2). Despite the low initial surface tension (Figure S, SI) due to the fast adsorption of STE, the overall adsorption behavior of 11S−STE mixtures would be similar to that of pure 11S, as evidenced by the surface tension decay of the mixture (0.1%) (Figure 3A). Furthermore, at high STE concentrations (1 and 2%, above the CMC of STE, see Figure 1B), large amounts of STE micelles would exist in the bulk. Meanwhile, with increasing binding of STE, the formation of STE clusters or micelles at the surface of 11S (Figures 1 and 2) might make the complex more hydrophilic, thus leading to the decrease in its surface activity. Considering the initial surface tension of 11S−STE mixture was very close to that of pure STE (Figure S, SI), therefore, we can speculate that the preferential adsorption of small STE molecules over 11S−STE complex at the interface occurred, thus leading to the conclusion that the interface is predominantly covered by STE (Figures 3 and 4). Similar behavior was reported for conventional surfactants, e.g., Tween 20 or SDS, which could also remove proteins completely from the interface.3,17,41 6840



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Figure 7. Schematic illustration of bulk behavior and adsorption at the air−water interface of 11S−STE mixtures with (A) low STE concentration (0.1%); (B) intermediate STE concentration (0.25−0.5%); (C) high STE concentration (1−2%).

The results of dynamic elastic modulus (Ed) and E−π curves exhibited good correlation with each other (Figure 4). For 11S−STE mixtures, it is very interesting to note that, at intermediate STE concentrations (0.25 and 0.5%), a plateau in the elasticity for mixed surface layers was clearly seen (Figure 4A). This behavior could be explained with the partial dissociation and looseness of protein structure, induced by the binding of STE, which could promote further unfolding of 11S at the interface. The unfolding of 11S would facilitate enhancing protein−protein and protein−STE interactions at the surface layer, as evidenced by high slope values of E−π plots (Figure 4B), thus increasing the Ed value.15,41 This increase might offset the lost elastic modulus due to increasing STE concentration at the interface, and thus endowed the mixed surface layer with a plateau in the elasticity. These analyses were in line with surface tension analyses (Figure 3) and supported by fluorescence and ITC results (Figures 1 and 2). On the basis of the above analysis, we can conclude that the synergy in surface tension decay and the plateau in surface elasticity appear to be crucial to the understanding of the dynamic surface properties for 11S−STE mixtures. Moreover, it is noteworthy to mention that no such behavior has been reported for protein/conventional surfactant mixtures. In general, for protein/nonionic surfactant mixtures, a monotonous decrease of the equilibrium surface tension and dilatational elasticity is observed, whereas for ionic surfactants, the surface tension exhibits a sharp decrease below the CMC, which is accompanied by a maximum of dilatational elasticity as the concentration of surfactant increases in the mixture.3,12,14 Considering the real foaming process, the link between surface characteristics and foaming properties is far from straightforward. However, in view of all of these present results, it could be speculated that there is a clear correlation between the surface behavior and the actual foaming properties for 11S− STE mixtures. As discussed previously, the foamability appeared to be affected strongly by the initial surface tension values of foaming agents (Figure 5 and Figure S in the SI). Furthermore, surface elasticity is generally believed to play an important role in foam stability.1,3,40,47 Thus, despite poor foaming capacity of pure 11S (Figure 5), the formed foam remained very stable (Figure 6), which should be due to the formation of surface layers with high surface elasticity (Figure 4A) that protect the bubbles against coalescence.1,3,7,40,47

Nevertheless, at intermediate STE concentrations (0.25 and 0.5%), surprisingly, although there was a dramatic decrease in surface elasticity (Figure 4A), no marked effect on the foam stability for the mixtures was observed (Figure 6). This suggested that the surface elasticity is not always the major factor influencing the stability of the mixed foams. Indeed, it is often stated and observed that protein−LMW surfactant mixtures could even give more stable foams than proteins alone.1,45 The addition of the LMW surfactants will make the rather rigid protein layer more flexible and mobile, and the formed mixed surface layer might then be much better able to respond to deformations, which would prevent film rupture and thus have a positive effect on the foam stability.1,45 This idea is consistent with the present observation on the stability of foams formed by 11S−STE mixtures (especially at 0.25 and 0.5%) (Figure 6) and is also supported by similar results on previous emulsion systems.27 Accordingly, it might be speculated that the mixed surface layer stabilized by 11S and STE not only provided a relatively constant elasticity (Figure 4A) but also possessed a certain relaxation mechanism due to the existence of STE by the Gibbs−Marangoni effect,1,3,4,6 thus endowing the foams with considerable stability (Figure 6). On the other hand, upon further increase of STE concentration (1 and 2%), the interface was gradually covered by STE (Figures 3 and 4) due to the preferential adsorption of STE molecules. Consequently the interface became weaker (low surface elasticity, see Figure 4A), and thus the resultant foams became less stable (Figure 6). From these series of experiments and analysis, to better understand the correlation between the surface behavior and the actual foaming properties, a schematic illustration of bulk and surface behaviors of 11S−STE mixtures is proposed and shown in Figure 7. In the case of pure 11S, the slow adsorption at the interface impaired its foaming capacity (Figure 5 and Figure S in the SI); however, the formed surface layer with a high dilational elasticity (Figure 4) contributed to the generation of very stable foam (Figure 6). Upon the addition of low STE concentration (0.1%), the foamability of the mixture was obviously increased due to the fast adsorption of STE (Figure 5 and Figure S in the SI). Despite the marked effect on the surface dilational properties by STE, the interface was still mainly dominated by 11S (Figures 3 and 4). At intermediate STE concentrations (0.25 and 0.5%), the weak 6841



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binding of STE with 11S in bulk occurred by nonspecific hydrophobic interactions (Figures 1 and 2). However, the binding was believed to be sufficiently intense to promote the partial dissociation and looseness of protein’s rigid structure (Figure 1A). This would facilitate further unfolding of 11S upon adsorption and thus enhance the protein−protein and protein−STE interfacial interactions. These analyses were supported by the strong synergy in reducing surface tension and the plateau in surface elasticity for mixed layers (Figures 3 and 4), which endowed the corresponding foams with a fine foaming capacity, making the layer be better able to respond to applied stresses without rupturing and providing considerable foam stability against bubble coalescence (Figures 5 and 6). In addition, when high STE concentrations (1 and 2%) were added, large amounts of STE micelles formed in bulk. The preferential adsorption of STE molecules over the 11S−STE complex resulted in the formation of a surface layer covered mainly by STE (Figures 3 and 4), and thus the resultant foams became less stable due to low surface elasticity (Figures 4A and 6). In conclusion, we have studied the adsorption of 11S−STE mixtures at the air−water interface by combining several approaches on different length scales. The obtained results showed clearly that the foaming properties of the mixtures were correlated with their surface behavior, which was found to be strongly influenced by 11S−STE interactions in the bulk. Compared to pure 11S, the surface dilational properties and foaming capacity were markedly affected even at low STE concentration (0.1%). When intermediate STE concentrations (0.25−0.5%) were added, the weak binding of STE with 11S in bulk occurred by nonspecific hydrophobic interactions, which appeared to be sufficiently intense to induce conformational changes of 11S, as evidenced by fluorescence and ITC. As a result, the strong synergy in reducing surface tension and the plateau in surface elasticity for mixed 11S−STE layers formed from the weakly interacting mixtures were clearly observed. This effect could be explained by the complexation with STE, which might facilitate the partial dissociation and further unfolding of 11S upon adsorption, thus enhancing the protein− protein and protein−STE interfacial interactions. These surface properties were positively reflected in foams produced by the weakly interacting system, which exhibited good foaming capacity and considerable stability probably due to better response to external deformations without film rupture. At high STE concentrations (1−2%, above its CMC), the preferential adsorption of STE molecules occurred, and thus the interface was predominantly covered by STE. Consequently, the resultant foams became less stable due to low surface elasticity. Considering the conditions of practical foam formation and evolution, which mainly involve large deformation and high strain rates, the link between the present surface measurements and foaming properties is not straightforward. Further work is required on the study of the detailed microstructure and mechanical properties of adsorbed protein−STE layers under nonlinear conditions and large deformations using appropriate experimental techniques.45,48 However, these results obtained in this work provide valuable information on the relation between the surface behavior and foaming properties of the 11S−STE mixtures. We expect that these findings would open up the potential of mixed protein−STE systems as foam/ emulsion formulations in industrial applications.

Article

ASSOCIATED CONTENT

S Supporting Information *

Figure of initial surface tension values versus the concentration of STE for solutions with and without 0.1% 11S. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*Tel: (086) 20-87114262. Fax: (086) 20-87114263. E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This research was supported by grants from the Chinese National Natural Science Foundation (Serial numbers: 31371744, 31301432, and 31130042), and the Fundamental Research Funds for the Central Universities (SCUT, 2013ZM0052).

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REFERENCES

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Synergistic Foaming and Surface Properties of a Weakly Interacting

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