Effect of ε-polylysine addition on κ-carrageenan gel properties: Rheology, water mobility, thermal stability and microstructure

Food Hydrocolloids 95 (2019) 212–218

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Effect of ε-polylysine addition on κ-carrageenan gel properties: Rheology, water mobility, thermal stability and microstructure

T

Tingting Lia, Chengrong Wena,∗, Yingying Donga, Dongmei Lia, Miao Liua, Zhongli Wanga, Srinivas Janaswamyb, Beiwei Zhua, Shuang Songa,∗∗ a

National Engineering Research Center of Seafood, National & Local Joint Engineering Laboratory for Marine Bioactive Polysaccharide Development and Application, School of Food Science and Technology, Dalian Polytechnic University, Dalian, 116034, China b Dairy and Food Science Department, South Dakota State University, Brookings, SD, 57007, USA

A R T I C LE I N FO

A B S T R A C T

Keywords: κ-carrageenan ε-Polylysine Gel properties Binary mixtures Synergistic interactions

Kappa-carrageenan is a gel forming anionic sulfated polysaccharide used extensively in food applications. Metal ions, proteins and other polysaccharides influence its gelation. Though polypeptides are known widely for their intrinsic benefits in developing healthy food products, their effect on κ-carrageenan functional properties has not been established yet. Herein, influence of ε-polylysine (0.05, 0.1, 0.15, 0.2 and 0.3%, w/v) on the viscoelastic and thermal properties, water mobility and microstructure of κ-carrageenan gels has been carried out. The storage modulus, gel-sol transition temperature and thermal stability increase with the ε-polylysine addition along with a decrease in the water mobility. The shift in the FT-IR absorption bands of the sulfate groups coupled with the disappeared Amide II clearly accentuate the synergistic interactions between κ-carrageenan and εpolylysine. Such changes reflect on the more regular microstructure with compact cavities filled with the polypeptide. Overall, ε-polylysine exerts favorable interaction mechanisms on the κ-carrageenan gels. The outcome has potential to open up novel research opportunities on the binary mixtures of polysaccharides and polypeptides toward developing new and healthy food products with suitable organoleptic properties for the growing population.

1. Introduction Gels are hydrophilic polymeric networks formed through physical and/or chemical crosslinking. Their intrinsic nature to imbibe large quantities of water or functional fluids bestows widespread utility in food, pharmaceutical and cosmetic formulations as control release agents of bioactive compounds, flavors and drugs (Coviello, Matricardi, Marianecci, & Alhaique, 2007; Li, Ni, Shao, & Mao, 2014). Macromolecules such as synthetic polymers, polysaccharides and proteins have the required ability to form gels (Tako, 2015). In this set, polysaccharides gain special attention due to their biocompatibility, nontoxicity, low-cost coupled with outstanding physicochemical properties (Bhattarai, Gunn, & Zhang, 2010). Among them, carrageenans are interesting to research due to their extensive use as gelling agents, waterholding agents and as materials of microcapsules, wound dressings and

drug delivery systems (Yu Chen, Liao, & Dunstan, 2002; Salgueiro, Danieldasilva, Fateixa, & Trindade, 2013). Carrageenans are anionic sulfated polysaccharides obtained through extraction from cell walls of certain marine red seaweeds. Among the three commercially important carrageenans κ-, ι- and λ-carrageenan, κcarrageenan (KC) is well known for its gel-forming ability (Yu Chen et al., 2002; Hugerth, Nilsson, & Sundelöf, 1999), which is composed of an alternating disaccharide unit of (1–3)- α-D-galactose-4-sulphate and (1–4)-β-3,6-anydro-D-galactose (Liu, Zhan, Wan, Wang, & Wang, 2015; Verma, Pandey, Yadav, & Behari, 2014). In the solution, KC undergoes two conformational transitions: coil state at higher temperature, and double helix followed by aggregation upon cooling. Subsequently, gels with three-dimensional network form especially at lower temperatures (Borgström, Piculell, Viebke, & Talmon, 1996). During this process, presence of other ingredients such as metal ions, proteins,

Abbreviations: KC, κ-carrageenan; PLL, ε-polylysine; DSC, differential scanning calorimeter; LF-NMR, low field nuclear magnetic resonance; NECH, number of echoes; NS, number of scans; TW, duration between successive scans; TE, time of echoes; Cryo-SEM, cryogenic scanning electron microscope; FT-IR, Fourier-transform infrared spectroscopy ∗ Corresponding author. School of Food Science and Technology, Dalian Polytechnic University, No.1 Qinggongyuan, Ganjingzi district, Dalian, 116034, China. ∗∗ Corresponding author. E-mail addresses: [email protected] (C. Wen), [email protected] (S. Song). https://doi.org/10.1016/j.foodhyd.2019.04.027 Received 18 November 2018; Received in revised form 9 April 2019; Accepted 14 April 2019 Available online 15 April 2019 0268-005X/ © 2019 Published by Elsevier Ltd.

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were covered to prevent any water evaporation during the experiment. Prior testing, temperature and shear stress were equilibrated for 5 min to rebuild the gel structure. The strain sweeps in the range of 0.1–100% were performed at 4 and 25 °C to establish the linear viscoelastic region. The frequency sweeps were carried out at 1% strain (within the linear viscoelastic region) at 4 and 25 °C, and temperature sweeps were conducted in the range 4–60 °C at a heating rate of 3 °C/min at 1 Hz and 1% strain (within the linear viscoelastic range).

oligosaccharides and polysaccharides affects the gelation process and corresponding gel properties (Evageliou, Ryan, & Morris, 2019). Interactions between ingredients and KC are interesting. The metal cations (K+, Na+ and Ca2+) tend to electrostatically bound to KC chains (Mangione et al., 2005; Yuan, Du, Zhang, Jin, & Liu, 2016). Cyclodextrins improve the rheological and structural properties by forming hydrogen bonds and inserting in the KC skeletons (Yuan et al., 2016; Chao; Yuan, Sang, Wang, & Cui, 2018). Polysaccharides such as xanthan, konjac glucomannan and locust bean gum interact synergistically with KC and modulate the functional properties (Brenner, Tuvikene, Fang, Matsukawa, & Nishinari, 2015; Chen, Liao, Boger, & Dunstan, 2001). Synergistic interactions among carrageenans and amphoteric proteins are gaining importance in recent times. KC enhances stability and thermal properties of arachin by adsorbing on to the arachin surface (Zhao et al., 2015). Whey protein isolate, soy protein and β-lactoglobulin could form complexes with carrageenans through strong electrostatic interactions (Jones, Decker, & Mcclements, 2010; Li, Hua, Chen, Kong, & Zhang, 2016; Stone & Nickerson, 2012). However, lack of reports on the interactions of polypeptides with KC motivated us to embark on a systematic investigation. Polypeptides play an active role in a wide spectrum of biological functions including blood pressure obesity, lipoprotein metabolism, gut and neurological functions, immunity and mineral metabolism. Their intrinsic health benefits also aid to develop healthy foods. ε-Polylysine (PLL) is a natural polypeptide composed of 25–35 homogeneous L-lysine, linked through peptide bonds between ε-amino and α-carboxyl (Shima & Sakai, 1981; Yoshida & Nagasawa, 2003). It possesses good thermal stability, water solubility, broad-spectrum antimicrobial activity, high safety and could be decomposed into nutrient substance lysine in vivo. It is currently used as preservative, carriers for drug delivery, nanocomposite material and ingredient of high absorbent materials (J & X, 2015; Shen & Ryser, 1981; Shukla, Singh, Pandey, & Mishra, 2012). The FDA approved PLL as a GRAS material for food applications. Herein, effect of PLL on the rheological behavior and thermal stability on KC gels has been reported along with changes in the microstructure and water distribution. The outcome is believed to serve as a basis in furthering studies on deciphering polypeptide-polysaccharide interactions toward developing novel and innovative food and non-food applications.

2.4. LF-NMR measurements Approximately 2g of gel samples in 2 mm diameter glass bottles were used for measuring the water mobility and distribution by low field nuclear magnetic resonance (LF-NMR) (MesoMR23-060V-1, Niumag Electric Corporation, China) equipped with a magnetic field strength of 0.5 T. Samples were placed in the NMR glass tubes and then inserted into a 40 mm radio frequency coil. The proton spin-spin T2 values were acquired using the Carr-Purcell-Meiboom-Gill (CPMG) pulse sequence at 32 °C, number of echoes (NECH) is 18000, number of scans (NS) is 4, duration between successive scans (Tw) is 5000 ms, time of echoes (TE) is 0.3 ms. The pulse width of 90° (P1) and 180° (P2) were 26.00, 54.00 μs, respectively. 2.5. Thermal stability The melting behavior of the gels was carried out using the DSC 250 differential scanning calorimeter from the TA Instruments, USA. Gels were pre-frozen at −32 °C for 24 h, following by vacuum freeze-drying at −60 °C for 72 h to obtain dried gels. Around 5 mg of the dried gels were placed in aluminum pans and equilibrated at 40 °C. Thermal curves were obtained at the healing rate of 5 °C/min in the temperature range 50–300 °C. An empty pan served as the reference. 2.6. FT-IR analysis Spectra from the samples were recorded using the FT-IR spectrophotometer from the PerkinElmer, USA. Freeze-dried gel samples were mixed with KBr and pressed into pellets. The spectra were recorded at room temperature in the wave number range of 400–4000 cm−1, with a resolution of 4 cm−1.

2. Materials and methods 2.7. Microstructure 2.1. Materials The microstructure of gels was analyzed using a cryogenic scanning electron microscope (SU8010, Hitachi, Japan) equipped with PP3010T Cryo-SEM preparation system. The SEM cold trap, SEM cryo stage, prepare stage and cryo preparation chamber cold stage temperatures were −175, −140, −140 and −175 °C, respectively. Gel samples in appropriate amount were placed into the rivets and immersed in slush nitrogen to freeze rapidly. These samples were then put into cryo chamber (PP3010T, Quorum, England), fractured with a razor blade and sublimed at −60 °C for 15 min. Then samples were coated with gold by sputter for 30 s and experiments were conducted at the accelerating voltage of 10 KV.

KC was purchased from Aladdin, USA. The sulfate content was estimated to be 21.6% using the turbidimetric method. Food-grade PLL (98% pure) was purchased from Chemlin, Nanjing, China. Samples were used without further purification along with the double distilled water. 2.2. Gel preparation Initially, KC was dispersed in double distilled water and stirred at 90 °C for 30 min to prepare 1% (w/v) solution. Subsequently, 0.05, 0.1, 0.15, 0.2 and 0.3% (w/v) PLL were added, heated at 90 °C and stirred for 5 min. The dispersions were kept stand still for 5 min and degassed to remove the air bubbles, if any. Later, they were stored at 4 °C for 18 ± 2 h to obtain the gels. They were referred as KC, KCP1, KCP2, KCP3, KCP4, KCP5, for brevity, in the rest of the discussion.

3. Results and discussion 3.1. Viscoelastic properties The changes in the storage modulus (G′) and loss modulus (G″) of KC as a function of frequency are depicted in Fig. 1. The addition of PLL remarkably increases the G′ values of KC. The G′ remains higher than G″ over the entire frequency range suggesting the dominant elasticity proportion and character of the gels (Anvari et al., 2016; Clark, RossMurphy, & Colloids, 1991). The subtle G′ changes with the frequency in the KCP, compared to KC, indicate the formation of stable and solid-like

2.3. Rheological measurements The viscoelastic properties were measured in a Discovery HR-1 rheometer from the TA Instruments, USA equipped with a cone geometry of 2° angle and 40 mm diameter. Samples were placed in 60 °C water bath for 10 min and were transferred to the rheometer plate and 213

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Fig. 1. Effect of PLL on the elastic moduli (G′, filled symbols) and loss moduli (G″, open symbols) of KC gels as a function of frequency at (a) 4 °C and (b) 25 °C.

Fig. 2. Effect of PLL on the tan δ of KC gels as a function of frequency at (a) 4 °C and (b) 25 °C.

Fig. 3. Effect of PLL on the complex viscosity of KC gels as a function of frequency at (a) 4 °C and (b) 25 °C.

enhanced frequency stability and reduced tan δ values of KCP gels clearly indicate the synergistic interactions between the KC chains and PLL toward improving network formation and gel strength. This phenomenon further reflects in the complex viscosity (Fig. 3). A typical shear thinning behavior has been noticed and the complex viscosity decreases with the frequency increase. It is worth noting that the presence of PLL induces higher complex viscosity for KCP gels. Overall, the PLL addition results in increased viscosity implying the curtailed movement of KC chains and portrays stabile gels. The G′, G″ and tan δ variations of KC and KCP in the temperature range 5–60 °C are shown in Fig. 4a and Fig. 4b. The G′ values are higher than the G″ up to around 35 °C with tan δ below 1 reflecting the gelling

gel. Similar phenomenon has been observed in the binary mixture of KC and gelatin (Derkach, Ilyin, Maklakova, Kulichikhin, & Malkin, 2015). The experimental temperature indeed influences the gelation and higher G’ values are observed at 4 °C (Fig. 1a) compared to 25 °C (Fig. 1b). Thus, low temperature appears to be conducive for the gel formation (Yu Chen et al., 2002). This is further supported by the changes in tan δ, which usually reflects the cohesive gel strength. As shown in Fig. 2, tan δ is less than 1 suggesting the gel-like state of the samples. In the case of KCP, a decreasing trend for tan δ depending on PLL levels has been noticed. Especially for KCP4 and KCP5, values are less than 0.1 at 4 °C, indicating the formation of “strong” gels and are in agreement with the reported observations (And & Nishinari, 2001). The 214

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Fig. 4. Effect of PLL on the (a) elastic moduli (G′, filled symbols) and loss moduli (G″, open symbols) and (b) tan δ of KC gels as a function of temperature.

Fig. 6. CPMG relaxation time of KC gels in the range 0.01–10000 ms at PLL concentrations of 0.05 (KCP1), 0.1 (KCP2), 0.15 (KCP3), 0.2 (KCP4) and 0.3% (KCP5).

Fig. 5. The gel-sol transition temperature of KC gels as a function of PLL concentration.

state. However, beyond 35 °C they decrease with a crossover (tan δ = 1) of G′ and G″, and G″ is over G′ with tan δ > 1 and the overall values decrease progressively. The reduction in the G′ and G″ values is due to the breakdown of the cross-linked KCP network leading to the solutionlike state predominantly caused by the elevated temperatures (Mangione, Giacomazza, Bulone, Martorana, & Biagio, 2003). The crossover temperature suggests the melting temperature (Ts) and could be considered as an intuitive index to evaluate the gel-sol transition process. Interestingly, Ts of KC shifts gradually from 31.5 to 36.6 °C (Fig. 5) with the incorporation of PLL signifying the synergistic interactions between KC and PLL. Overall, gel network stability of KC increases with the addition of PLL.

which is located outside of the cross-linked network and possesses good mobility. This clearly suggests that free water is important and prominent part of the gel systems. Similar water distribution has been observed in starch gels (Long, Tian, Tong, Zhang, & Jin, 2017). The relaxation time and peak areas of free water are summarized in Table 1. The T23 of KC is 1934.94 ms but decreases with PLL addition, for example, to 1686.73 and 1573.60 ms for KCP4 and KCP5, respectively. This indicates that high PLL levels decrease the degree of water freedom and further restrict the water mobility resulting in low T23 values. In general, water content is proportional to the peak area of relaxation curves (Tang, Godward, & Hills, 2000). However, there is no significant difference among the peak areas (A23) suggesting that there is no water exchange occurring and PLL has subtle restricting ability on the free water content. Overall, water mobility weakens and water distribution changes with the PLL incorporation in the KC gels.

3.2. Water mobility Water is an important component of gels. Its mobility and distribution represent, indirectly, gel properties. LF-NMR is a fast and nondestructive tool for characterizing water properties by measuring the spin-spin relaxation time (T2). Water in different state shows various degrees of freedom depending on the surrounding environment, thus T2 will also be different. For the water molecules with high degree of freedom, their frequency of motion is much higher than the resonance frequency of hydrogen protons, resulting in the slower relaxation and the longer T2. As shown in Fig. 6, the first weak peak with the T2 range of 0.01–1 ms (T21) corresponds to the water associated within the highly organized double helix structures of gel, which is characterized by the worst mobility. The second weak peak with the T2 range of 1–100 ms (T22) water represents water located in the hydrogel network with weak mobility (Li et al., 2017). However, corresponding signal intensity is far less than the free water in the range 100–10000 ms (T23),

Table 1 Relaxation time (T23) and peak area (A23) of KC gels at PLL concentrations of 0.05 (KCP1), 0.1 (KCP2), 0.15 (KCP3), 0.2 (KCP4) and 0.3% (KCP5). T23 KC KCP1 KCP2 KCP3 KCP4 KCP5

1934.94 1847.41 1805.16 1805.16 1686.73 1573.60

A23 ± ± ± ± ± ±

a

78.43 73.17ab 73.17ab 73.17ab 131.95bc 123.10c

1046.73 1056.79 1067.05 1064.71 1065.68 1064.91

± ± ± ± ± ±

2.88a 9.52a 10.15a 7.00a 18.39a 9.87a

All data represent the mean of triplicates. a, b and c represent significant differences (p < 0.05). 215

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Fig. 7. The DSC thermograms of (a) KC with the addition of PLL and (b) pure PLL. The inset in Fig. 7a highlights the thermograms in the temperature range of 50–150 °C.

3.3. Thermal stability The thermograms of KC, KCP along with PLL are depicted in Fig. 7. The incorporation of PLL results in the shift of the endothermic and exothermic peaks (Fig. 7a). In KC, the endothermic peak occurs at 112 °C, mainly due to the evaporation of water (Alnaief, Obaidat, & Mashaqbeh, 2018; Derkach et al., 2015; Zhu, Guo, Zheng, & Matsuo, 2014). It increases to 132 °C even with a small amount of PLL addition. This trend continues and stabilizes at around 141 °C for KCP5. Indeed, shift of the endothermic peak indicates the increased amount of moisture absorbed in the samples with the PLL addition. On the other hand, two endothermic peaks at 127 and 288 °C are noticed for the PLL (Fig. 7b). The absence of PLL endothermic peaks in KCP suggests synergistic interaction between the KC chains and PLL molecules along with the formation of a homogeneous system (Zhang et al., 2015). The sharp exothermic peak observed at 223 °C for KC could be ascribed to the thermal decomposition (Tanaka, Lu, Yuasa, & Yamaura, 2001). The incorporation of PLL subsequently pushes it to higher temperature of 260, 264, 267, 280 and 281 °C with PLL of 0.05, 0.1, 0.15, 0.2 and 0.3% concentration, respectively. This indicates that association of PLL improves the thermal stability of KCP. These observations further demonstrate the compatibility between KC chains and PLL molecules toward augmenting the thermal stability of the KG gels.

Fig. 8. The FT-IR spectra of KC, KCP and PLL.

indeed, accentuate the favorable interactions between the negatively charged sulfate groups of KC with the positively charged amino groups of PLL.

3.5. Microstructure 3.4. Infrared spectra analysis

Cryo-SEM is an effective tool in characterizing the microstructure of hydrogels. In this technique, the sample is frozen in slush nitrogen and maintained within the microscope at low temperature and high vacuum, which can reduce the formation of ice crystals and protect samples from deformation, thus a better spatial structure is preserved (Sriamornsak, Thirawong, Cheewatanakornkool, Burapapadh, & SaeNgow, 2008). The microstructure differences among the gels with the PLL addition are quite evident (Fig. 9). The KC possesses irregular morphology with cavities of different size (Fig. 9a). The PLL incorporation, however, induces compact cavities of uniform size (Fig. 9b–f). The number of cavities per visual field is around 10 to 20 for KC and KCP1, 20 to 30 for KCP2, KCP3, KCP4, and more than 40 for KCP5. It is known that the size and shape of cavity correspond to the ice crystals formed during the measurement. Thus, the cavity density increase suggests the extent of ice formation changes induced by the PLL addition. Furthermore, PLL appears to be smeared in the cavities to strengthen the KC structure and corroborates the enhanced gel strength (section 3.1) and thermal stability (section 3.3). Suitable concentration of K+ ions could promote the cavity formation in KC with rectangular size (Thrimawithana, Young, Dunstan, & Alany, 2010). This investigation further suggests that PLL also has the required ability to induce

The infrared spectra of KC, KCP and PLL are depicted in Fig. 8. The board O-H absorption is observed at 3435 cm−1 along with a weak signal at 2924 cm−1 and correspond to the C-H stretching from the KC chains (Corvaglia, Rodriguez, Bardi, Torres, & Lopez, 2016). The peak at 1632 cm−1 represents the water present in the KC gels (Delval et al., 2002; Oun & Rhim, 2017). The signals at 844, 931 and 1256 cm−1 are from the C-O-S stretching vibration of galactose-4-sulfate, 3,6-anhydroD-galactose and sulfate group (O=S=O), respectively (Navikaite, Simanaviciute, Klimaviciute, Jakstas, & Ivanauskas, 2016). The PLL possesses a board peak at 3424 cm−1 that could be ascribed to the NH2 asymmetric stretching. The C-H stretching vibration occurs at 2924 and 2854 cm−1 (Sindhu & Temilia, 2008). The peaks at 1684 and 1593 cm−1 represent the amide I and II bands, respectively (Maeda, Kunimoto, & Sasaki, 2011). Incorporating PLL in KC shifts the sulfate groups absorption to a higher wavenumber of 1261 cm−1 for the KCP spectra whilst the water peak at 1632 cm−1 retreats to 1621 cm−1. The intensity of Amide I peak from PLL at 1684 cm−1 decreases and the Amide II peak at 1593 cm−1 disappears, and are consistent with the starch and PLL complex (Zhang et al., 2015). These observations, 216

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Fig. 9. The Cryo-SEM micrographs of KC (a), KCP1 (b), KCP2 (c), KCP3 (d), KCP4 (e) and KCP5 (f).

morphological changes in KC. This observation could hold good to other polypeptides and polysaccharides but warrants further investigation.

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4. Conclusions The addition of PLL to KC gels significantly influences the gel properties. Specifically, PLL improves the rheological properties with increased storage modulus, complex viscosity and melting temperature of gels. The PLL incorporation appears to restrict the free water mobility and alter the water distribution in the KC gels. The enhanced gel strengths coupled with thermal stability portray the synergistic interactions between the PLL and KC. In addition, higher water evaporation and decomposition temperature of KC-PLL binary mixture illustrates the beneficial effect of PLL on KC. There are a few examples about the polypeptides influence on the polysaccharide functionality. Couple of known systems include complexes of polylysine hydrochloride with pectin, chitosan, alginate and starch as well as PLL-KC binary mixture at low pH conditions (Chang, Mclandsborough, & Mcclements, 2014; Guan, Ye, Liu, & Zhao, 2013). Our research about the influence of PLL on the physicochemical properties of KC gels provides one more important data point and indeed furthers research on the binary mixtures of polysaccharides and polypeptides. The outcome could aid in the design and development of carrier systems of bioactive compounds (Janaswamy & Youngren, 2012; Polowsky & Janaswamy, 2015) with suitable organoleptic properties and to meet the growing population demands. Acknowledgment The research was supported by the Dalian Polytechnic University Testing Center, the Scientific Research Special Fund of Marine Public Welfare Industry of China (No. 201505030), and the USDA National Institute for Food and Agriculture (HATCH project SD00H648-18). Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.foodhyd.2019.04.027. References Alnaief, M., Obaidat, R., & Mashaqbeh, H. (2018). Effect of processing parameters on preparation of carrageenan aerogel microparticles. Carbohydrate Polymers, 180, 264–275.

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