Foams Stabilized by Î²-Lactoglobulin Amyloid Fibrils: Effect of pH

Article Cite This: J. Agric. Food Chem. 2017, 65, 10658−10665

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Foams Stabilized by β‑Lactoglobulin Amyloid Fibrils: Effect of pH Dengfeng Peng,†,§ Jinchu Yang,‡ Jing Li,†,§ Cuie Tang,†,§ and Bin Li*,†,§,∥ †

College of Food Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, People’s Republic of China Technology Center, China Tobacco Henan Industrial Company Limited, Zhengzhou, Henan 450000, People’s Republic of China § Key Laboratory of Environment Correlative Dietology, Ministry of Education, Huazhong Agricultural University, Wuhan, Hubei 430070, People’s Republic of China ∥ Functional Food Enginnering & Technology Research Center of Hubei Province, Wuhan, Hubei 430070, People’s Republic of China ‡

S Supporting Information *

ABSTRACT: β-Lactoglobulin fibrils could serve as a surface-active component and form adsorption layers at the air/water interface. In this study, the physical parameters related to the surface adsorption, foaming, and surface properties of βlactoglobulin fibrils as a function of pH (2−8) were investigated. Results showed that an increase of pH from 2 to 5 led to a rise of the viscoelastic modulus of the surface adsorption layer and half-life time (t1/2) of foams, but it decreased foamability. When the pH was close to its isoelectric point (5.2), fibrils had the lowest electrostatic repulsion and entangled at the air/water interface resulting in a tightly packaged adsorption layer around bubbles to prevent coalescence and coarsening. When the pH (7−8) was higher than the pI of fibrils, the negatively charged β-lactoglobulin fibrils possessed good foamability (∼80%) and high foam stability (t1/2 ≈ 8 h) simultaneously even at low concentration (1 mg/mL). It demonstrated that β-lactoglobulin fibrils with negative charges presented a good foaming behavior and could be a potential new foaming agent in the food industry. KEYWORDS: foams, β-lactoglobulin fibrils, pH, charges, surface behaviors, stability

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surface properties of fibrils had been studied extensively, and the data indicated that physical treatments affected the structure and charges of fibrils, resulting in various foaming behaviors.22 Wan et al. studied the surface and foaming properties of 11S fibrils at different pH values and found that the adsorption and interfacial rheological behavior of fibrils were closely related to pH.22 In order to make full use of protein fibrils in wide-range applications, it is important to develop the relationship between the foaming properties of fibrils and pH changes in more detail. Thus, in this work the microstructure, ζ potential, and viscosity of fibril solutions as a function of pH were characterized systematically. The influence of pH on the foaming properties (foam decay, foamability, and half-life time) and surface behaviors (surface tension and surface dilatational modulus) of β-lactoglobulin fibrils were investigated. In addition, changes of the microstructure of foams stabilized by fibrils with a pH range were determined to better understand the stabilization mechanism. It is known that the macroscopic behavior of foams can be affected strongly by the surface properties.15,23,24 Finally, the linkage among the physical properties, foam character, and air/water surface structure of β-lactoglobulin fibrils was illustrated to further understand the effect of pH on the foaming properties of protein fibrils.

INTRODUCTION Foams have been one of the most important components in many food systems due to their abilities to endow special structures, appearance, and taste of products.1,2 Proteins used as surface-active components could form highly elastic surface films to prevent coalescence, drainage, and coarsening of foams.3,4 However, foams stabilized by proteins often need high concentrations in the processing, which increases the cost of production, limiting their applications in the food industry.5,6 In recent years, heat treatment at different pHs and ionic strengths got a structural conversion of native proteins into fibrillar structures,7−9 which improved the foaming and surface properties.10−12 Oboroceanu et al. found that whey protein isolate (WPI) fibrils showed better foaming properties than that of native WPI, and the foamability and foam stability of fibrils seemed to be independent of their length.13 Wan et al. also found that soy glycinin (11S) fibril systems had faster adsorption kinetics and higher surface dilatational modulus than those of native 11S, resulting in better foaming properties.14 β-Lactoglobulin, a main component of whey protein which is commonly applied in aerated food products,15 has the surfaceactive property for forming and stabilizing foams.16 Through heating at pH 2, β-lactoglobulin was converted into fibrils.17−19 The formation kinetics of monomers into fibrils have been studied previously.20,21 Jung et al. contrasted the surface behaviors of native β-lactoglobulin and its heat-induced fibrils. They found that fibrils reduced the surface tension fast and formed a higher elastic network around air bubbles than those of native β-lactoglobulin.10 Basically, protein fibrils were sensitive to changes of physical conditions (pH, ionic strength, etc.). The influence of physical treatments on foaming and © 2017 American Chemical Society

Received: Revised: Accepted: Published: 10658

August 7, 2017 November 13, 2017 November 14, 2017 November 14, 2017 DOI: 10.1021/acs.jafc.7b03669 J. Agric. Food Chem. 2017, 65, 10658−10665

Article

Journal of Agricultural and Food Chemistry

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Surface Tension Measurement. An automatic drop tensiometer (Tracker Teclis/IT Concept, France) was used to monitor the surface tension of β-lactoglobulin fibrils (1 mg/mL) at various pH values of 2−8. All experiments were carried out at 25 °C. β-Lactoglobulin fibril solutions were placed in a rectangular glass cuvette sealed with parafilm. An axisymmetric air drop was formed at the inverted tip of a syringe and monitored with a video camera. The dynamic surface tension of sample solutions was monitored for 3 h at a constant area of the drop (18 mm2). The surface tension (γ) was calculated from shape analysis of a rising drop according to the Gauss/Laplace equation. The surface tension could be converted into surface pressure (π) by using the relation πt = γs − γt, where γs is the surface tension of solvent and γt is the time-dependent surface tension of the corresponding protein fibril solution. Surface Dilatational Rheology. The surface viscoelastic modulus (E), elastic (Ed), and viscous (Ev) components were measured as a function of time (θ) at 10% deformation amplitude (ΔA/A) and 0.1 Hz of angular frequency (ω) according to our previous work.5 The air drop was subjected to repeated measurements of 4 sinusoidal oscillation cycles and 4 static oscillation cycles up to 3 h. The surface dilatational modulus (E) was calculated as given in eq 1

MATERIALS AND METHODS

Materials. β-Lactoglobulin (crude protein content, 95.9%) was kindly supplied by Davisco Foods International, Inc. (Minnesota, USA), and purified according to the method of Jung.10 Thioflavin T (ThT) fluorescence dye was purchased from Sigma-Aldrich Trading Co., Ltd. (Shanghai, China). Other chemicals were of analytical grade and used without further purification. Water purified by a Milli-Q system (γ = 72.8 ± 0.2 mN m−1 at 25 °C, resistivity of 18.2 MΩ cm) was used for sample preparation. Preparation of β-Lactoglobulin Fibrils. β-Lactoglobulin (2%, w/v) stock solution was obtained by dissolving protein powder in DI water under stirring at room temperature (∼25 °C). After adjusting to pH 2.0 using 2.0 M HCl, the protein solution was incubated in a water bath at 90 °C (±0.5 °C) for 5 h under magnetic stirring (∼60 rpm). Then the solution was immediately cooled in an ice bath and dialyzed against pH 2.0 DI water for at least 72 h to remove the unconverted monomers and hydrolyzed peptides. After being dialyzed, the βlactoglobulin fibrils were achieved and stored in the refrigerator (4 °C) until use. Sample Preparation. One mg/mL β-lactoglobulin fibril solutions at different pH values (2, 4, 5, 6, 7, and 8) were prepared upon diluting the above-obtained fibril solution using pH 2.0 DI water and adjusting to the desired value by using 2.0, 0.5, and 0.1 M NaOH. Morphology Observation. The surface morphology of βlactoglobulin fibrils (1 mg/mL) at different pH values was observed using transmission electron microscopy (TEM, JEM-2100F, JEOL, Japan). Images of the fibrils were recorded in randomly selected fields. ζ -Potential Measurements. The ζ potential of samples was determined using ZS Zetasizer Nano (Malvern Instrument Ltd., UK). All measurements were carried out at 25 °C and repeated 3 times. Rheological Measurements. The steady shear measurements of samples were carried out using a DISCOVERY HR-2 hybrid rheometer (DHR2) (TA Instruments, America) with a cone plate geometry (60 mm diameter, cone angle 1.007°, gap 26 μm). The shear rate was increased from 0.1 to 500 s−1, and the viscosity (η) was recorded. All of the measurements were carried out at 25 °C and repeated at least 3 times. Foaming Properties. The foaming properties of samples were characterized by the method of Peng et al.5 and Wan et al.14 with slight modification. a 15 mL amunt of sample was placed in a glass cylinder (internal diameter of 30 mm, height of 150 mm). After whipping with a homogenizer (T25, IKA) at 8000 rpm for 1 min at 25 °C, the foam was immediately poured into the measuring cylinder (50 mL). Then volumes of foam were recorded at 2, 60, 180, 300, 720, 1440, and 2880 min to observe the foam decay. Foamability (FA) was determined by comparing the foam volume at 2 min with the initial liquid volume of samples. Foam stability (FS) was measured by recording the time required for the foam volume to reduce to one-half of its initial volume (half-life time, t1/2).

FA(%) = V2/15 × 100

(1)

FS(%) = t1/2(half‐life time)

(2)

E = dπ /d ln A

(3)

where π is the surface pressure and A is the surface area of the air drop at times of θ. After 180 min of adsorption, quasi-equilibrium conditions of the interface were obtained, and then the following dilatational rheology measurements at different frequencies (0.01−0.1 Hz) and deformations (10−40%) were performed. All experiments were performed at 25 °C. Statistical Analysis. Values were given as means ± standard deviations (SD). One-way analysis of variance (ANOVA) was performed to establish the significance of differences (p < 0.05) between values.

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RESULTS AND DISCUSSION Characteristics of β-Lactoglobulin Fibrils at Different pH Values. When the stock solution of β-lactoglobulin at pH 2 was heated at 90 °C, the assembly of small peptides formed through hydrolyzing β-lactoglobulin monomers would lead to formation of fibrils.11,25 The aggregation behavior of protein fibrils was similar to proteins under different pHs. Figure 1A shows the visual appearance of β-lactoglobulin fibrils at the pH range from 2 to 8. As the pH gradually increased from 2 to 5, the appearance of β-lactoglobulin fibrils changed from transparent to a light blue color. When the pH was further increased to 8, the solution gradually became transparent again. This behavior was also observed by another researcher.11 Accordingly, the morphology images observed by TEM illustrated that β-lactoglobulin fibrils had a linear structure at pH 2 (Figure 1B), while at pH 4, 5, and 6, fibrillar structures were entwined in the dense network inducing large agglomerates and fibrils became shorter compared to that of pH 2, presenting obvious aggregations. As the pH increased to 7 and 8, fibrils exhibited a linear structure but fibrils were still shorter when compared to that of pH 2 (Figure 1B). This was in agreement with the findings of Gilbert et al.26 Protein aggregation induced by pH always resulted from reducing net charges. Here, Figure 2 presents the ζ potentials of β-lactoglobulin fibrils changing with pH. At pH 2, the ζ potential value was +31.4 ± 3.25 mV. With increasing the pH from 2 to 5, the ζ potential of fibrils gradually decreased from +31.4 ± 3.25 to +6.3 ± 0.6 mV due to being close to the isoelectric point (∼5.2) of β-lactoglobulin fibrils, which was similar to that of other research on β-lactoglobulin fibrils.26,17 When fibrils approached their isoelectric point, electrostatic

where V2 is the foam volume at 2 min and t1/2 is the time for the foam volume to reduce to one-half of its initial volume. Foaming Microstructure Observation by Optical Microscopy. Microscope images of foams after being stored at 25 °C for 120, 600, 1800, 3600, and 10 800 s were obtained on a microscope instrument (Nikon ECLIPSE Ti−S, Japan). Surface Structure Observation of Foams by Fluorescence Microscopy and Super-High-Resolution Microscopy. In order to observe surface structures of foams, β-lactoglobulin fibrils were labeled with 3 mM ThT, which was dispersed into 10 mM phosphate-buffered saline (PBS, pH 7.0). Then foams were prepared according to the procedure mentioned in the method of foaming properties. After whipping, foams under fluorescence field were observed using fluorescence microscopy (Nikon ECLIPSE Ti-S, Japan) and superhigh-resolution microscopy (STORM, Nihonika, Japan). 10659

DOI: 10.1021/acs.jafc.7b03669 J. Agric. Food Chem. 2017, 65, 10658−10665

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Figure 3. Viscosity versus shear rate (0.1−500 s−1) for β-lactoglobulin fibrils (1 mg/mL) at various pH values (2, 4, 5, 6, 7, 8).

(Figure 4A and 4B). Foamability (FA) was assessed by comparing the foam volume at 2 min with the initial liquid volume. As shown in Figure 4C, the FA of fibril at pH 2 was 81.8 ± 3.0%, suggesting a good foaming capacity. However, as the pH increased to 5, the FA dropped to 46.4 ± 3.0%. When the pH value further rose to 8, the FA increased to 85.8 ± 6.4%. Besides, the FA of β-lactoglobulin fibrils was much better than that of other proteins, such as soy glycinin,28 soy glycinin fibril,22 sodium caseinate, and ovalbumin.5 The foam decay and half-life time (t1/2) were calculated to evaluate the foam stability (FS), as displayed in Figure 4A and 4D, respectively. With increasing pH from 2 to 5, a substantial decrease in decay rates and increase in t1/2 values (from 57 ± 12 to 1460 ± 139 min) were observed, suggesting an increase of FS. As the pH further increased from 5 to 8, decay rates started to rise and t1/2 began to drop (from 1460 ± 139 to 450 ± 79 min). It implied that fibrils at pH 5 could produce more stable foams compared with other pH values. Compared with β-lactoglobulin (nonfibrils), β-lactoglobulin fibrils (pH 2, 5, and 8) had higher FA and FS (Figure S1). This is consistent with the research results of Oboroceanu, which found foams produced from whey protein fibrils showed a significant improvement in foam stability when compared with nonfibrillar whey proteins.13 It is noteworthy to mention that even at the low concentration (1 mg/mL), βlactoglobulin fibril at pH 5 still exhibited the highest FS (t1/2 ≈ 24 h), which was 2.4- and 12-fold larger than that of the soy glycinin fibril−peptide system (t1/2 ≈ 10 h) and pure soy glycinin fibril system (t1/2 ≈ 2 h), respectively.14 Changes of bubbles size formed by β-lactoglobulin fibril (1 mg/mL) at pHs of 2−8 with the extension of time are presented in Figure 5. For all investigated pHs, bubbles stabilized by fibril systems showed a uniform bubble size distribution with the small spherical bubbles (at 120 s). Moreover, for all pHs, the bubble size gradually increased as a function of time from 120 to 10 800 s. The size of bubbles stabilized by fibrils at pH 5 displayed the slowest rate of increase in all pH values. Compared to other pHs, the shape of bubbles was much closer to the globular shape. This implies that the fibril at pH 5 had the strongest capability to prevent foam coarsening, coalescence, and drainage.22 This was in line with the result of foam decay (Figure 4A and 4B) and the data on the half-life time (t1/2) (Figure 4D). From changes of bubble sizes and shapes as a function of time, it could be concluded that a fibril which is close to its isoelectric point would have a better FS. Surface Structure of Foams. Bubbles prepared by βlactoglobulin fibrils at pHs of 2−8 were observed under

Figure 1. (A) Visual appearance and (B) TEM images of the βlactoglobulin fibrils (1 mg/mL) at different pH values (2, 4, 5, 6, 7, 8).

Figure 2. ζ Potentials of β-lactoglobulin fibrils (1 mg/mL) at various pH values (2, 4, 5, 6, 7, 8).

repulsion became weak and minimized inter- and intrainteractions of fibrils which cause fibrils to aggregate and break into shorter fragments. This is consistent with the result of the TEM images (Figure 1B). On further increasing the pH from 6 to 8, fibrils had a negative charge. This result agrees with the literature values reported by Gao et al.27 Viscosity. Typical viscosity profiles of β-lactoglobulin fibril solutions (1 mg/mL) at pH of 2−8 as a function of shear rate are presented in Figure 3. All of the fibril solutions exhibited a shear thinning behavior upon increasing the shear rate from 0.1 to 500 s−1. At the same shear rate the viscosity increased as the pH increased from 2 to 5. This was because the attracting forces increased and a strong network of fibrils was built, resulting in the increase of viscosity. When the pH was further increased from 5 to 8, the network weakened due to the rise of net charges on the fibril surface and generating the electrostatic repulsion. Foaming Properties. The foam decay, foamability, and half-life time (t1/2) were measured to evaluate the foam properties (Figure 4). Figure 4A shows the variation of foam volume from 2 to 2880 min (2 days). For all pH values, the bubble volumes gradually decreased with increasing time 10660


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Figure 4. (A) Foam decay curves, (B) visual appearance, (C) foamability, and (D) half-life time (t1/2, min) of foams generated from β-lactoglobulin fibrils (1 mg/mL) at pH of 2−8.

(0.04 s, ∼63 mN/m). This may be due to the high ζ potential and rigid structure of fibril at pH 2, resulting in hindering the fast diffusion to the interface. When the pH increased from 2 to 5, fibrils decreased the surface tension more rapidly (especially the initial surface tension), thus having a faster adsorption rate toward the interface. This suggests that the surface-active properties for fibrils rose with increasing pH from 2 to 5. In addition, with further increasing pH from 5 to 8, the abilities of fibrils to reduce initial surface tension were similar. Interfacial Dilatational Rheology. Figure 8A shows the evolution of E with π for β-lactoglobulin fibrils (pH 2−8). For all pHs, E rapidly increased with increasing π, suggesting that fibrils adsorbed from the bulk onto the interface. The slope of the E−π curve was used to evaluate the interaction of surfaceactive components. When the value was larger than 1 (an ideal gas), it demonstrated existing interaction.28 As can be seen from Figure 8A, the slopes of all pHs were higher than 1 (represented by the dotted line), indicating the presence of molecular interactions among the adsorbed β-lactoglobulin fibrils. The slope of pH 5 was the largest among all pHs, suggesting that the fibril at pH 5 had the strongest interaction. This was attributed to the low ζ potential, which reduced the energy barrier of electrostatic repulsion. The evolution of the viscoelastic modulus (E), elastic modulus (Ed), and viscous modulus (Ev) of β-lactoglobulin fibrils (pH 2−8) with time are presented in Figure 8B-D. For all pHs, E and Ed rapidly increased at the beginning and then

fluorescence microscope (Figure 6). β-Lactoglobulin fibrils were labeled with ThT, which could only specifically bind with fibrillar structures displaying green fluorescence. For all investigated pHs an obvious green fluorescence layer was observed, indicating fibrils at all pHs all were capable to anchor on the air/water interface. In order to further observe the detailed surface structure of bubbles, super-high-resolution microscopy was applied to characterize the surface structure of foams formed by β-lactoglobulin fibrils at different pH values (inset images of Figure 6). Bubbles stabilized by β-lactoglobulin fibrils at pH 4−8 showed uniform fluorescence intensity, indicating they were densely adsorbed on the air/water interface. However, a fluorescence glowing layer with uneven intensity was observed at pH 2. It illustrated that fibrils at pH 2 did not form a densely packed layer against coalescence and prevent air diffusion among bubbles. Thus, foams stabilized by fibril at pH 2 had a lower foam stability than other pH values. This is consistent with the results of Figure 4. Surface Adsorption Behavior. Figure 7 presents the time evolution of the surface tension of β-lactoglobulin fibrils (pH 2−8) at the air/water interface. For all investigated pHs, the surface tension quickly decreased within the first 500 s, suggesting the rapid adsorption of fibrils at the interface. From 500 s to 3 h, the surface tension gradually decreased and became relatively constant. Moreover, β-lactoglobulin fibrils at different pH values exhibited different adsorption kinetics. For fibril at pH 2 system, it had the highest initial surface tension 10661


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Figure 5. Time evolution of air bubbles within foams formed by β-lactoglobulin fibrils (1 mg/mL) with different pHs (2−8). Solid bars in all images correspond to a length of 100 μm.

Figure 6. Microstructure images of the bubbles stabilized by βlactoglobulin fibrils (1 mg/mL) with different pHs (2−8). Fibril was stained green. (Insets) Microstructure images observed by superresolution microscopy.

Figure 7. Time evolution of the surface tension for the adsorption of β-lactoglobulin fibrils (1 mg/mL) with different pH values (2−8) at the air/water interface.

were gradually decreased with time, which was markedly different from other active ingredients.5 To gain more information about the microstructure and mechanical properties of the surface layer, dilatational interfacial rheology (frequency and amplitude sweeps) was performed at various pH values. Modulus (E) as a function of frequency and amplitude sweep curves was recorded in Figure 9. E gradually increased with an increase of frequency, showing a frequency-dependent property (Figure 9A). This behavior

gradually increased after 500 s. Fibril at pH 5 had the highest E value (∼80 mN/m), which was obviously larger than other proteins or protein mixtures, such as β-casein,29 soy globulins,30 and bovine and camel protein mixtures,31 suggesting fibrils had a firm viscoelastic surface film at pH 5. Interestingly, the Ev values of fibrils were about 25 mN/m at the beginning (20 s). This was obviously larger than other proteins, such as casein micelles32 and β-casein.33 In addition, the Ev of fibrils at all pHs 10662


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Figure 8. (A) Surface dilatational modulus (E) as a function of surface pressure (π) for β-lactoglobulin fibrils (1 mg/mL) with different pH values (2−8) at the air/water interface and time evolution of the surface dilatational modulus (B), elastic modulus (C), and viscous modulus (D) for the adsorption of β-lactoglobulin fibrils (1 mg/mL) with different pH values (2−8).

Figure 9. Surface dilatational modulus (E) as a function of (A) frequency (0.01−0.2 Hz) and (B) amplitude (10−40%) for the air/water interface stabilized by β-lactoglobulin fibrils (1 mg/mL) with different pH values (2−8) at 25 °C.

resulting in the strong electrostatic repulsion among fibrils at the interface. Hence, it had the lowest foam stability. Fibrils at pH 4−6 had higher E due to lower net charges, which result in the formation of a thick protective layer around bubbles by overlapping and entanglement of the fibrils leading to the higher foam stability. Moreover, fibril solutions at pH of 4−6 had high viscosity, which could prevent air diffusion among bubbles. At pH 7 and 8, fibrils had a negative charge and anisotropic shape, which endowed fibrils diffused fast, adsorbed to the air/water interface, and formed tightly packed viscoelastic films. These results explained that fibril simultaneously had good foamability and high foam stability. β-Lactoglobulin fibrils were proved to be sufficient to form and stabilize foams without other surfactant even at low concentration (1 mg/mL). The pH of fibrils had an obvious effect on the foaming properties. From the results of the surface

was attributed to the relaxation mechanism at the air/water interface, which included the behavior of dynamic exchange of molecules between the surface and the bulk phase and structural rearrangements after they adsorbed on the surface.34,35 The surface microstructure was related to the deformation amplitude.14 To investigate the dependence of E on amplitude, amplitude sweeps were performed. As can be seen from Figure 9B, E continuously decreased with increasing amplitude from 10% to 40% for all pHs, indicating that the surface microstructures were affected by the high degree of deformation. In summary, the influence of pH changes (2−8) on the physical characters (morphology, ζ potential, and viscosity), foaming, and surface properties of β-lactoglobulin fibrils were investigated accordingly. At pH 2, the surface of bubbles was not densely packed by fibrils, owing to the higher ζ potential 10663


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surfactant solutions at the water/air interface. Langmuir 2008, 24, 13977−13984. (7) Akkermans, C.; Venema, P.; van der Goot, A. J.; Gruppen, H.; Bakx, E. J.; Boom, R. M.; van der Linden, E. Peptides are building blocks of heat induced fibrillar protein aggregates of ß-lactoglobulin formed at pH2. Biomacromolecules 2008, 9, 1474−1479. (8) Munialo, C. D.; Martin, A. H.; van der Linden, E.; de Jongh, H. H. J. Fibril Formation from Pea Protein and Subsequent Gel Formation. J. Agric. Food Chem. 2014, 62, 2418−2427. (9) Akkermans, C.; Van der Goot, A. J.; Venema, P.; Van der Linden, E.; Boom, R. M. Properties of protein fibrils in whey protein isolate solutions: Microstructure, flow behaviour and gelation. Int. Dairy J. 2008, 18, 1034−1042. (10) Jung, J. M.; Gunes, D. Z.; Mezzenga, R. Interfacial activity and interfacial shear rheology of native beta-lactoglobulin monomers and their heat-induced fibers. Langmuir 2010, 26, 15366−15375. (11) Kroes-Nijboer, A.; Sawalha, H.; Venema, P.; Bot, A.; Flöter, E.; den Adel, R.; Bouwman, W. G.; van der Linden, E. Stability of aqueous food grade fibrillar systems against pH change. Faraday Discuss. 2012, 158, 125−138. (12) Rühs, P. A.; Scheuble, N.; Windhab, E. J.; Fischer, P. Protein adsorption and interfacial rheology interfering in dilatational experiment. Eur. Phys. J.: Spec. Top. 2013, 222, 47−60. (13) Oboroceanu, D.; Wang, L.; Magner, E.; Auty, M. A. E. Fibrillization of whey proteins improves foaming capacity and foam stability at low protein concentrations. J. Food Eng. 2014, 121, 102− 111. (14) Wan, Z.; Yang, X.; Sagis, L. M. Nonlinear Surface Dilatational Rheology and Foaming Behavior of Protein and Protein Fibrillar Aggregates in the Presence of Natural Surfactant. Langmuir 2016, 32, 3679−3690. (15) Dombrowski, J.; Gschwendtner, M.; Kulozik, U. Evaluation of structural characteristics determining surface and foaming properties of β-lactoglobulin aggregates. Colloids Surf., A 2017, 516, 286−295. (16) Dombrowski, J.; Johler, F.; Warncke, M.; Kulozik, U. Correlation between bulk characteristics of aggregated β-lactoglobulin and its surface and foaming properties. Food Hydrocolloids 2016, 61, 318−328. (17) Jones, O. G.; Handschin, S.; Adamcik, J.; Harnau, L.; Bolisetty, S.; Mezzenga, R. Complexation of beta-lactoglobulin fibrils and sulfated polysaccharides. Biomacromolecules 2011, 12, 3056−3065. (18) Ruhs, P. A.; Scheuble, N.; Windhab, E. J.; Mezzenga, R.; Fischer, P. Simultaneous control of pH and ionic strength during interfacial rheology of beta-lactoglobulin fibrils adsorbed at liquid/liquid Interfaces. Langmuir 2012, 28, 12536−12543. (19) Jordens, S.; Ruhs, P. A.; Sieber, C.; Isa, L.; Fischer, P.; Mezzenga, R. Bridging the gap between the nanostructural organization and macroscopic interfacial rheology of amyloid fibrils at liquid interfaces. Langmuir 2014, 30, 10090−10097. (20) Adamcik, J.; Jung, J. M.; Flakowski, J.; De Los Rios, P.; Dietler, G.; Mezzenga, R. Understanding amyloid aggregation by statistical analysis of atomic force microscopy images. Nat. Nanotechnol. 2010, 5, 423−428. (21) Isa, L.; Jung, J. M.; Mezzenga, R. Unravelling adsorption and alignment of amyloid fibrils at interfaces by probe particle tracking. Soft Matter 2011, 7, 8127−8134. (22) Wan, Z.; Yang, X.; Sagis, L. M. Contribution of Long Fibrils and Peptides to Surface and Foaming Behavior of Soy Protein Fibril System. Langmuir 2016, 32, 8092−8101. (23) Davis, J. P.; Doucet, D.; Foegeding, E. A. Foaming and interfacial properties of hydrolyzed beta-lactoglobulin. J. Colloid Interface Sci. 2005, 288, 412−422. (24) Ruíz-Henestrosa, V. P.; Sánchez, C. C.; Escobar, M. d. M. Y.; Jiménez, J. J. P.; Rodríguez, F. M.; Patino, J. M. R. Interfacial and foaming characteristics of soy globulins as a function of pH and ionic strength. Colloids Surf., A 2007, 309, 202−215. (25) Akkermans, C.; Venema, P.; van der Goot, A. J.; Gruppen, H.; Bakx, E. J.; Boom, R. M.; van der Linden, E. Peptides are building

and foaming property measurements, four major results were achieved. First, fibrils at pH 2 had a relatively poor foam stability because they did not form a densely packed layer against coalescence, coarsening, and preventing air diffusion among bubbles. Second, β-lactoglobulin fibrils at pH 5, which are close to the isoelectric point (∼5.2), exhibited excellent foam stability owing to the lower electrostatic repulsion, larger bulk phase viscosity, and formation of a tightly packed surface viscoelastic film. Third, for pH 4−8, fibrils had a higher E than that of pH 2, which endowed them better foam stability. Fourth, fibrils showed frequency- and amplitude-dependent properties. Results showed that β-lactoglobulin fibrils at pH 7 and 8 had high foamability and foam stability simultaneously, which could act as a good foaming agent and be widely applied in the food industry.

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ASSOCIATED CONTENT

* Supporting Information S

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.7b03669. Foam decay curves, visual appearance, foamability, and half-life time (t1/2, min) of foams generated from βlactoglobulin (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Tel.: +86-27-87283462. Fax: +86-27-87282966. ORCID

Bin Li: 0000-0001-7763-4245 Funding

This work was financially supported by the National Key R&D Program of China (Program No. 2017YFD0400200), National Natural Science Foundation of China (Grant No. 31772015), Fundamental Research Funds for the Central Universities (Program No. 2662017JC011), and Wuhan Yellow Crane Special Talents Program. The authors thank Fengrui Wu and Limin He (Huazhong Agricultural University) for their help with the TEM characterization and Zhe Hu (Huazhong Agricultural University) for his help with super-high-resolution microscopy characterization. Notes

The authors declare no competing financial interest.

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REFERENCES

(1) van Kempen, S. E. H. J.; Schols, H. A.; van der Linden, E.; Sagis, L. M. C. Non-linear surface dilatational rheology as a tool for understanding microstructures of air/water interfaces stabilized by oligofructose fatty acid esters. Soft Matter 2013, 9, 9579−9592. (2) Dickinson, E. Food emulsions and foams: Stabilization by particles. Curr. Opin. Colloid Interface Sci. 2010, 15, 40−49. (3) Martin, A. H.; Grolle, K.; Bos, M. A.; Stuart, M.; Vanvliet, T. Network forming properties of various proteins adsorbed at the air/ water interface in relation to foam stability. J. Colloid Interface Sci. 2002, 254, 175−183. (4) Petkov, J. T.; Gurkov, T. D.; Campbell, B. E.; Borwankar, R. P. Dilatational and Shear Elasticity of Gel-like Protein Layers on Air/ Water Interface. Langmuir 2000, 16, 3703−3711. (5) Peng, D.; Jin, W.; Li, J.; Xiong, W.; Pei, Y.; Wang, Y.; Li, Y.; Li, B. Adsorption and Distribution of Edible Gliadin Nanoparticles at the Air/Water Interface. J. Agric. Food Chem. 2017, 65, 2454−2460. (6) Kotsmar, C.; Grigoriev, D.; Xu, F.; Aksenenko, E.; Fainerman, V.; Leser, M.; Miller, R. Equilibrium of adsorption of mixed milk protein/ 10664


Article

Journal of Agricultural and Food Chemistry blocks of heat-induced fibrillar protein aggregates of β-lactoglobulin formed at pH 2. Biomacromolecules 2008, 9, 1474−1479. (26) Gilbert, J.; Campanella, O.; Jones, O. G. Electrostatic stabilization of beta-lactoglobulin fibrils at increased pH with cationic polymers. Biomacromolecules 2014, 15, 3119−3127. (27) Gao, Z.; Zhao, J.; Huang, Y.; Yao, X.; Zhang, K.; Fang, Y.; Nishinari, K.; Phillips, G. O.; Jiang, F.; Yang, H. Edible Pickering emulsion stabilized by protein fibrils. Part 1: Effects of pH and fibrils concentration. LWT - Food Sci. Technol. 2017, 76, 1−8. (28) Wan, Z. L.; Wang, L. Y.; Wang, J. M.; Yuan, Y.; Yang, X. Q. Synergistic foaming and surface properties of a weakly interacting mixture of soy glycinin and biosurfactant stevioside. J. Agric. Food Chem. 2014, 62, 6834−6843. (29) Noskov, B. A. Protein conformational transitions at the liquid− gas interface as studied by dilational surface rheology. Adv. Colloid Interface Sci. 2014, 206, 222−238. (30) Pizones Ruíz-Henestrosa, V.; Carrera Sánchez, C.; Rodríguez Patino, J. M. Formulation engineering can improve the interfacial and foaming properties of soy globulins. J. Agric. Food Chem. 2007, 55, 6339−6348. (31) Lajnaf, R.; Picart-Palmade, L.; Attia, H.; Marchesseau, S.; Ayadi, M. Foaming and adsorption behavior of bovine and camel proteins mixed layers at the air/water interface. Colloids Surf., B 2017, 151, 287−294. (32) Dombrowski, J.; Dechau, J.; Kulozik, U. Multiscale approach to characterize bulk, surface and foaming behavior of casein micelles as a function of alkalinisation. Food Hydrocolloids 2016, 57, 92−102. (33) Blijdenstein, T. B. J.; de Groot, P. W. N.; Stoyanov, S. D. On the link between foam coarsening and surface rheology: why hydrophobins are so different. Soft Matter 2010, 6, 1799−1808. (34) Jin, W.; Zhu, J.; Jiang, Y.; Shao, P.; Li, B.; Huang, Q. GelatinBased Nanocomplex-Stabilized Pickering Emulsions: Regulating Droplet Size and Wettability through Assembly with Glucomannan. J. Agric. Food Chem. 2017, 65, 1401−1409. (35) Freer, E. M.; Yim, K. S.; Fuller, G. G.; Radke, C. J. Shear and dilatational relaxation mechanisms of globular and flexible proteins at the hexadecane/water interface. Langmuir 2004, 20, 10159−10167.

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Foams Stabilized by Î²-Lactoglobulin Amyloid Fibrils: Effect of pH

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