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Improved Toughness and Stability of κ‑Carrageenan/Polyacrylamide Double-Network Hydrogels by Dual Cross-Linking of the First Network Hai Chao Yu, Chen Yu Li, Miao Du, Yihu Song, Zi Liang Wu,* and Qiang Zheng Ministry of Education Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou 310027, China

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ABSTRACT: It is highly desired yet challenging to develop hydrogels with a combination of excellent mechanical properties and good stability for potential applications. Here we report κ-carrageenan/polyacrylamide double-network (DN) hydrogels with remarkable mechanical performances and high stability in water, which are achieved using zirconium ions to further crosslink the first physical network of κ-carrageenan by forming coordination complexes. Thus, obtained DN hydrogels in equilibrated state with water content of 83−91 wt % were highly transparent and showed tensile breaking stress of 1.5−3.2 MPa, breaking strain of 300−2200%, Young’s modulus of 0.2−2.2 MPa, and tearing fracture energy of 0.4−18.5 kJ/m2. We found that dual-cross-linking of the κ-carrageenan network, i.e., the coiled-coil junctions and the metal-coordination bonds, was indispensable for the combined mechanical properties and stability of these gels. Essential reasons were rationally discussed based on the results of control experiments. The strategy we described should be applicable to other biopolymer-based hydrogels toward improved mechanical properties and stability, which may promote the applications of tough hydrogels in diverse areas. and tearing fracture energy G of 100−4400 J/m2. These DN hydrogels were prepared by two-step polymerization to synthesize a highly cross-linked rigid polyelectrolyte as the first network and a loosely cross-linked flexible polymer as the second network. During the loading process, the first network fragmented into small clusters to dissipate vast energy, whereas the second network entangled with the clusters and maintained the integrity of the gel.10,24,25 Because the energy dissipation relied on the fracture of the first brittle network, the permanent damage severely reduced the strength of DN gel after the first loading process. To address this issue, dynamic noncovalent bonds are used to physically cross-link the first network to afford the DN hydrogel self-recovery ability at specific conditions.26−35 For example, Suo and co-workers synthesized a family of tough and

1. INTRODUCTION Hydrogels are usually recognized as soft and weak materials, and their poor mechanical properties greatly limit the applications as structural elements in biomedical and engineering fields.1−3 In contrast, some biotissues such as cartilages and tendons are in a gel state but possess excellent mechanical properties.4−6 There are of both fundamental and practical significance to design mechanically robust hydrogels. In recent years, scientists have developed various tough hydrogels with specific network structure and energy dissipation mechanism.7−21 Among these tough hydrogels, double-network (DN) gels developed by Gong and co-workers have received tremendous attention because of their high water content, outstanding mechanical performances, and a typical toughening mechanism.10,22,23 For example, the poly(2-acrylamido-2methyl-1-propanesulfonic acid)/polyacrylamide (PAMPS/ PAAm) DN hydrogels with water content of ∼90 wt % showed a tensile breaking stress σb of 1−10 MPa, breaking strain εb of 1000−2000%, Young’s modulus E of 0.1−1 MPa, © XXXX American Chemical Society

Received: October 22, 2018 Revised: December 26, 2018

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DOI: 10.1021/acs.macromol.8b02269 Macromolecules XXXX, XXX, XXX−XXX

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Figure 1. (a) Schematic for the synthesis of Zr4+ ion-reinforced κ-CG/PAAm DN hydrogel. Pregel solution containing κ-CG, AAm, chemical crosslinker, and photoinitiator (cross-linker and initiator are omitted for simplicity) (i) was cooled to room temperature, resulting in sol-to-gel transition of κ-CG to form the first network (ii). After irradiation under UV light, AAm was polymerized to form the second network of the DN hydrogel (iii). The as-prepared DN gel was incubated under aqueous solution of ZrOCl2 to from sulfate−Zr4+ coordination complex and then in pure water to achieve the equilibrated state (iv). (b, c) Transmittance (b) and tensile stress−strain curves (c) of the as-prepared and the equilibrated DN gels without reinforcement by Zr4+ ions (DN-30-0-3-0.01) and the equilibrated DN gel reinforced by Zr4+ ions (DN-30-0.1-3-0.01). The inset image showed a high transparence of the DN-30-0.1-3-0.01 hydrogel.

bonds between Zr4+ ions and sulfate groups of κ-CG. These tough hydrogels with excellent mechanical performances and good stability should be an ideal material to construct structural elements. The method by using Zr4+ ions to strengthen the mechanical properties of hydrogels by forming coordination complexes should be applicable to other natural or synthetic polymers and broaden the applications of tough hydrogels in different areas.

stretchable hydrogels by combining an ionically cross-linked alginate network and a covalently cross-linked PAAm network.26 The Ca-alginate/PAAm hydrogels showed excellent mechanical properties with σb of 0.05−0.2 MPa, εb of 400− 2100%, and G of 200−9000 J/m2. Zheng et al. developed agar/ PAAm DN hydrogels with σb and εb up to 1 MPa and 2000%, respectively.29,30 Liu et al. fabricated κ-carrageenan/PAAm DN hydrogels with E of 280 kPa and G of 6150 J/m2.31,32 These DN hydrogels exhibited excellent self-recovery and self-healing capacities due to the dynamic physical cross-linking of the first network. Although the biopolymer-containing DN hydrogels had better biocompatibility and showed excellent mechanical properties in the as-prepared state,34−36 they were not stable or became highly swollen after being incubated under water,26,29 resulting in drastically reduced mechanical properties, which greatly limited their potential applications. Increasing the strength of noncovalent bonds should be an effective strategy to stabilize the first network and thus to maintain the mechanical robustness of the DN hydrogels in the equilibrated state. Herein we report κ-carrageenan/polyacrylamide (κ-CG/ PAAm) DN hydrogels with remarkable mechanical performances and good stability by using Zr4+ ions to further cross-link the first network of κ-CG. Thus, the obtained DN hydrogels with water content of 83−91 wt % showed excellent mechanical properties, with σb of 1.5−3.2 MPa, εb of 300− 2200%, E of 0.2−2.2 MPa, and G of 0.4−18.5 kJ/m2. The excellent properties of these DN gels were associated with the dual-cross-linking of the first network, i.e., double-helical junctions between κ-CG molecules and metal coordination

2. EXPERIMENTAL SECTION 2.1. Materials. κ-Carrageenan (κ-CG), zirconyl chloride octahydrate (ZrOCl2·8H2O), and samarium chloride hexahydrate (SmCl3· 6H2O) were used as received from Aladdin Chemistry Co., Ltd. Aluminum chloride hexahydrate (AlCl3·6H2O) and iron chloride hexahydrate (FeCl3·6H2O) were used as purchased from Sinopharm Chemical Reagent Co., Ltd. Acrylamide (AAm), N,N′-methylenebis(acrylamide) (MBAA, chemical cross-linker), and α-ketoglutaric acid (KA, photoinitiator) were purchased from Sigma-Aldrich and used without further purification. Millipore deionized water was used in all the experiments. 2.2. Gel Synthesis. Figure 1a shows the protocol of the synthesis of DN hydrogels. Prescribed amounts of κ-CG, AAm, MBAA, and KA were dissolved in water at 70 °C to obtain a homogeneous and transparent solution. The precursor solution with high viscosity was transferred to a reaction cell, which was placed at 4 °C for 2 h to induce sol-to-gel transition of κ-CG to form the first network and then irradiated under UV light at room temperature for 7 h to form the second network of PAAm. The as-prepared DN hydrogel was incubated under 0.1 M ZrOCl2 aqueous solution for 3 days to form coordination complexes between the Zr4+ ions and the sulfate groups of κ-CG and then transferred into a large amount of pure water for another 3 days to remove the residual Zr4+ ions and achieve the B

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Macromolecules equilibrated state. The DN hydrogels are coded as DN-CCG-CZr-CAAmCx, where CCG, CZr, CAAm, and Cx are the concentration of κ-CG in mg/mL, concentration of Zr4+ ion in M, concentration of AAm in M, and concentration of MBAA in mol % (relative to the AAm), respectively. The concentration of photoinitiator was kept as 0.1 mol % (relative to the AAm). The as-prepared DN hydrogel can also be further cross-linked by incubation in aqueous solution of AlCl3, FeCl3, or SmCl3 and then in pure water to obtain the reinforced equilibrated DN hydrogel. The DN hydrogels refer to the equilibrated state if there is no special statement. Zr4+ ion-reinforced κ-CG hydrogel was prepared in a similar way, as schemed in Figure S1. 2.3. Characterizations. Attenuated total reflectance Fourier transform infrared spectroscopy (ATR-FTIR; Nicolet iS10, Thermo Scientific, USA) was performed to the hydrogels with different compositions. The spectra were obtained at room temperature with 32 scans and a resolution of 4 cm−1 in the range 4000−400 cm−1. The microstructure of the gels was observed by a Hitachi S4800 field emission scanning electron microscope (SEM). The samples were prepared by freeze-drying and then cryogenically fractured in liquid nitrogen. The fractured surface was coated with a thin layer of platinum by sputtering before SEM observation. The accelerating voltage for SEM observation was 3 kV. The transmittance of the hydrogel was measured using a UV−vis spectrophotometer (Shimadzu, UV 1800). The transmittance of the hydrogel sheets with different thickness was normalized to the thickness of 1 mm according to the Beer−Lambert law. The water content of as-prepared and equilibrated gels, q, was calculated according to q = (ws − wd)/ws, where ws and wd are the mass of gels in wet and dried state, respectively. Tensile tests were performed on the hydrogels using a commercial tensile tester (Instron 3343) with a 50 N load cell. The samples were cut into dumbbell shape with an initial gauge length of 12 mm and a width of 2 mm. The tensile tests were performed at room temperature (25 °C) with a stretch rate of 100 mm/min. Young’s modulus E was calculated from the initial slope of the stress−strain curve with a strain below 10%; the corresponding breaking stress σb and breaking strain εb were extracted from the stress−strain curves for at least three separate tests. To characterize the stability of DN hydrogels in water, the gel samples of DN-30-0.1-3-0.01 were incubated under pure water, which was changed every day, and measured every 2 weeks at room temperature. Cyclic tensile tests were performed to the sample at room temperature by sequentially loading to a predetermined strain and then unloading to zero strain. Tearing tests were also performed to the hydrogels at room temperature to characterize the tearing fracture energy. The samples were cut into rectangle shape (35 mm × 12 mm) with a notch (10 mm) in the middle of the short edge. Two arms of the specimen were clamped, and the upper arm was pulled upward with a stretch rate of 100 mm/min. The tearing fracture energy G was calculated according to the equation G = 2F/w, in which F and w are the steady tearing force and the gel thickness, respectively.16 Rheological behaviors of the hydrogels were analyzed by using a discovery hybrid rheometer (TA Instruments, USA). The equilibrated hydrogel DN-30-0.1-3-0.01 was cut into a disc shape with diameter of 20 mm (thickness: ∼1 mm), which was adhered to the parallel plates with glue. Strain sweeps were performed to the gel sample from 0.01% to 10% at a frequency of 1 Hz at room temperature. Frequency sweeps were performed to the sample at different temperature with a strain amplitude of 0.1%. The storage modulus G′, loss modulus G″, and loss factor tan δ were recorded. Temperature sweeps were performed to the pregel solution of κ-CG/AAm from 80 to 20 °C with a cooling rate of 1 °C/min; the strain amplitude and frequency were kept as 0.1% and 1 Hz, respectively. The stability of DN hydrogel in different conditions was characterized by their variations of dimensions and mechanical properties. The hydrogel samples of DN-30-0.1-3-0.01 were incubated under solutions with different pH, saline solutions with different concentration of NaCl, or a water bath with different temperatures to achieve the equilibrated state before the measurements. For the

characterization of long-time stability, the DN hydrogel was incubated under pure water at room temperature, which was changed every day.

3. RESULTS AND DISCUSSION 3.1. Synthesis of DN Hydrogels. κ-CG is a water-soluble biopolymer and contains one sulfate group per disaccharide unit (Figure 1a). At high concentration, κ-CG aqueous solution showed sol-to-gel transition when the temperature decreased to room temperature due to the formation of double-helix junctions between κ-CG molecules.37,38 Temperature sweeps of rheological measurement showed this sol-togel transition occurred at ∼70 °C during the cooling process (Figure S2). The κ-CG/PAAm DN hydrogel was synthesized according to the protocol schemed in Figure 1a. The asprepared DN hydrogel, consisting of physically cross-linked κCG as the first network and chemically cross-linked PAAm as the second network, was transparent and mechanically robust. The hydrogel became highly swollen and weakened after being incubated under water. A similar phenomenon was found in the pure κ-CG hydrogel because of the instability of the double-helix junctions against the osmotic pressure during the swelling process. However, the DN hydrogel reinforced by Zr4+ ions was mechanically robust and did not inflate after incubation in water. The as-prepared and equilibrated DN hydrogels were highly transparent, as shown in Figure 1b. Representative tensile stress−strain curves of the as-prepared and equilibrated DN hydrogels are shown in Figure 1c, indicating the remarkable improvement of mechanical properties of the DN gel after further cross-linking with Zr4+ ions. The as-prepared DN hydrogel (DN-30-0-3-0.01) showed σb of 790 kPa, εb of 2500%, and E of 103 kPa, whereas the equilibrated DN hydrogel without further cross-linking was much weaker, with σb of 58 kPa, εb of 870%, and E of 7 kPa. In contrast, the equilibrated DN hydrogel (DN-30-0.1-3-0.01) with further cross-linking by Zr4+ ions possessed improved mechanical properties, with σb of 3.2 MPa, εb of 1870%, and E of 1.6 MPa. The improved stability and mechanical properties were apparently associated with the interaction between Zr4+ ions and sulfate groups of κ-CG chains, as confirmed by FTIR measurements (Figure 2). In the FTIR spectrum of κ-CG hydrogel, the peak at 1220 cm−1 was assigned to the stretching vibration band of SO (−OSO3−),39 which shifted to 1212 cm−1 in the spectrum of reinforced κ-CG hydrogel, indicating the formation of the sulfate−Zr4+ coordination complex. In the spectrum of PAAm gel, the characteristic absorption peaks at 1667 and 1612 cm−1 corresponded to amide I (CO stretching vibration) and amide II (N−H bending vibration), respectively. In addition, the FTIR spectrum of DN gel was similar to that of PAAm gel because PAAm was the dominant component in DN gel. The mass ratio of κ-CG to PAAm in DN-30-0.1-3-0.01 gel was around 1:7. We should note that the dominant form of zirconium ions in water was the tetranuclear complex [Zr4(OH)8(H2O)16]8+,40,41 which formed a coordination complex with the sulfate groups of κ-CG. Zr4+ was used in the following section instead of the tetranuclear complex for simplicity.42 The microstructure of the as-prepared and equilibrated DN hydrogels was characterized by SEM. As shown in Figure 3, a typical porous structure was observed in the gels, although the network structure of gel in wet state was influenced by the freeze-drying to some extent. The pore size of equilibrated DN-30-0.1-3-0.01 gel was smaller than that of as-prepared DNC

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decreased from 3.2 MPa and 1870% to 2.8 MPa and 1500%, respectively. When CZr = 0.1 M, the DN gel possessed the optimal mechanical properties with σb of 3.2 MPa, E of 1.6 MPa, and G of 15.5 kJ/m2. Therefore, CZr was kept as 0.1 M in the following experiments. As shown in Figures 4e and 4f, the concentration of AAm, C AAm , also affected the mechanical properties of the equilibrated DN hydrogels (DN-30-0.1-CAAm-0.01). When CAAm was lower than 1 M, the gel was fragile with εb lower than 310%; when CAAm ≥ 2 M, the DN gels became stretchable with εb larger than 1200%. As CAAm increased from 0 to 6 M, σb, εb, and G increased first and then decreased with the maximum values, i.e., σb of 3.2 MPa, εb of 1870%, and G of 18 kJ/m2, when CAAm = 2.5−3 M. As CAAm increased from 0 to 3 M, the mechanical properties of the second network increased due to the increased polymer density and chain entanglement, which can sustain better the force after the fragment of the brittle first network of κ-CG, thus improving the performances of the integrated gels. As CAAm increased further, the enhanced entanglement of PAAm chains resulted in decrease in the stretchability of the DN gel, which weakened the efficiency of energy dissipation around the crack tip. Therefore, the DN gels with moderate amount of the second network showed the optimal mechanical properties.22,43 It was worth noting that E of DN gels decreased from 3.8 to 1.1 MPa with the increase in CAAm from 0 to 6 M. This was because E of the DN hydrogels was mainly contributed by the first network, and the existence of dense PAAm chains may destroy the dual-cross-linked first network of κ-CG. These tough DN gels had high water content, which only slightly decreased from 94 to 84 wt % with the increase in CAAm. The effect of the concentration of chemical cross-linker, Cx, on the properties of DN gels (DN-30-0.1-3-Cx) is shown in Figures 4g and 4h. As Cx increased from 0 to 0.1 mol %, εb decreased from 2200% to 600%, whereas E and q maintained almost constant values, 1.5 MPa and 82 wt %, respectively. With the increase in Cx, σb and G increased first and then decreased with the maximum values of 2.3 MPa and 1.5 kJ/m2, respectively, at Cx = 0.01 mol %. We should note that the DN gel prepared without chemical cross-linker (DN-30-0.1-3-0) also had good stability and excellent mechanical properties. In this DN gel, the PAAm chains might be physically cross-linked by forming weak coordination bonds with the Zr4+ ion,44 which should have a positive contribution to the excellence of mechanical properties (Figure S3). However, this DN gel without chemical cross-linking can be fully dissolved in highly alkaline solution. As described above, Zr4+ ion-reinforced κ-CG/PAAm DN hydrogels possessed excellent mechanical properties, superior

Figure 2. FTIR spectra of κ-CG hydrogel, Zr4+ ion-reinforced κ-CG hydrogel, PAAm hydrogel, and Zr4+ ion-reinforced DN hydrogel (DN-30-0.1-3-0.01).

30-0-3-0.01 (Figures 3a and 3b), indicating that the gel matrix became more compact and robust after being further crosslinked by Zr4+ ions. In contrast, the equilibrated gel of DN-300-3-0.01 without further cross-linking had a much larger pore size (Figure 3c) due to the highly swollen state with reduced cross-linking density. 3.2. Mechanical Properties of DN Gels. Similar to other DN hydrogels, the mechanical properties of κ-CG/PAAm DN hydrogels depended on the compositions of the first and second networks.22,26,29 As shown in Figures 4a and 4b, the concentration of κ-CG, CCG, greatly influenced the mechanical properties of the DN hydrogels. As CCG increased from 10 to 30 mg/mL, the tensile breaking stress σb, breaking strain εb, Young’s modulus E, and tearing fracture energy G of the equilibrated DN gels (DN-CCG-0.1-3-0.01) increased from 0.2 MPa, 640%, 90 kPa, and 0.4 kJ/m2 to 3.2 MPa, 1870%, 1.6 MPa, and 15.5 kJ/m2, respectively. The water content q slightly decreased from 87 to 85 wt %. When CCG > 40 mg/mL, it was very difficult to form a homogeneous solution and to be transferred into the reaction cell because of the high viscosity. Therefore, CCG was kept as 30 mg/mL in the following experiments. Zr4+ ions were crucial for the stability of DN gels equilibrated in water. As shown in Figures 4c and 4d, the concentration of Zr4+ ions, CZr, also influenced the mechanical properties of DN hydrogels (DN-30-CZr-3-0.01). As CZr increased from 0.005 to 0.175 M, εb and q only slightly decreased from 2200% and 90 wt % to 1500% and 84 wt %, respectively. When CZr increased from 0.005 to 0.05 M, σb, E, and G increased from 1.2 MPa, 0.2 MPa, and 3.6 kJ/m2 to 2.9 MPa, 1.5 MPa, and 12.8 kJ/m2, respectively, and when CZr increased from 0.05 to 0.1 M, σb, E, and G only slightly increased. As CZr increased further, there was almost no significant change in E and G, while σb and εb slightly

Figure 3. SEM images of the cross section of as-prepared gel DN-30-0-3-0.01 (a), equilibrated gel DN-30-0.1-3-0.01 with further cross-linking by Zr4+ ions (b), and equilibrated gel DN-30-0-3-0.01 without further cross-linking (c). D

DOI: 10.1021/acs.macromol.8b02269 Macromolecules XXXX, XXX, XXX−XXX

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Figure 4. Tensile stress−strain curves (a, c, e, g) and corresponding mechanical parameters (b, d, f, h) of equilibrated DN hydrogels prepared with different CCG (DN-CCG-0.1-3-0.01) (a, b), different CZr (DN-30-CZr-3-0.01) (c, d), different CAAm (DN-30-0.1-CAAm-0.01) (e, f), and different Cx (DN-30-0.1-3-Cx) (g, h). The tearing fracture energy G and water content q are also summarized in the figure. Error bars represent the standard deviation of the mean.

destruction of the interior structure under loading.26,44 The areas under the loading curve and in the loading−unloading loop corresponded to the extension work We and the dissipated energy Γ , respectively. The hysteresis ratio hs was calculated by hs = Γ /We × 100%. As εm increased from 300% to 1500%, Γ increased from 2.9 to 21.0 MJ/m3, whereas hs slightly decreased from 90% to 88%, indicating the gradual fracture of internal structure with a high efficiency to dissipate energy. The slight decrease in hs might originate from the more evident resilience of PAAm network with increasing εm. In addition, typical yielding phenomenon was observed during the stretching of DN gel, which was more evident than that of the as-prepared DN gel without further cross-linking by Zr4+ ions. The dually cross-linked κ-CG network was strong yet brittle and started to fragment into small clusters at a strain of

to most tough hydrogels and comparable to tough soft biotissues (Figure 5). The influence of the compositions on the mechanical properties of κ-CG/PAAm DN hydrogels was similar to conventional DN hydrogels.22 Considering the combined mechanical performances, the equilibrated DN-300.1-3-0.01 hydrogel was selected to investigate the stability and toughening mechanism in the following section. 3.3. Hysteresis and Stability of DN Hydrogels. The excellent mechanical performances of these DN gels are closely related to the effective energy dissipation, which can be demonstrated by hysteresis of the loading−unloading curves of the hydrogels stretched to different maximum strain εm. As shown in Figure 6a, large hysteresis was observed during the loading−unloading process of the DN hydrogel (DN-30-0.1-30.01), indicating the vast energy dissipation through the E

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bonds hampered the re-formation of double-helix structure of κ-CG. 3.4. Stability of DN Hydrogels. These DN gels with excellent mechanical properties should be an ideal material to construct structural elements. For practical applications of these tough hydrogels, stability in different conditions was important. We investigated the variations of gel dimensions and mechanical properties at different pH, temperature, and ionic strength. As shown in Figures 7a and 7b, the concentration of NaCl, CNaCl, influenced the properties of DN-30-0.1-3-0.01 hydrogel to some extent. As CNaCl increased from 0 to 3 M, σb, εb, and E of the gel decreased from 3.2 MPa, 1870%, and 1.6 to 0.6 MPa, 1100%, and 0.1 MPa, respectively, whereas the swelling ratio in length, S, of the gel (relative to the as-prepared state) increased from 1.1 to 1.4. The ionicstrength-dependent properties of the DN gel was due to the shielding effect of salt, which weakened the Zr4+−sulfate coordination bonds. However, the hydrogel still maintained considerable mechanical strength when CNaCl ≤ 1 M. In artificial seawater, the hydrogel was stable for a long time and possessed good mechanical properties, with σb of 1.5 MPa, εb of 1900%, and E of 0.8 MPa. The effect of temperature on the mechanical properties of the DN gel is shown in Figures 7c and 7d. As temperature increased from 0 to 50 °C, σb, εb, and E moderately decreased from 3.7 MPa, 1800%, and 1.6 to 2.2 MPa, 1650%, and 1.5 MPa, respectively. The high stability of the gel over a wide range of temperature was related to the strong metalcoordination bonds, as confirmed by frequency sweeps of the gel at different temperatures (Figure S5). There were no evident variations of G′ and G″ of the gel with the frequency even at 90 °C. The stability of DN gel also depended on pH, which influenced the strength and equilibrium constant of the metalcoordination bonds.20 When 4 ≤ pH ≤ 8, the hydrogel maintained excellent mechanical properties (Figures 7e and 7f). However, the hydrogel showed reduced mechanical properties in strongly acidic or alkaline conditions. σb, εb, and E of the gel at pH = 0 were 0.5 MPa, 1250%, and 0.7 MPa, respectively. The decreased mechanical properties of the gel in strongly acidic condition were probably due to the hydrolysis of glycosidic linkages of κ-CG.46,47 When pH ≥ 12, the gel became highly swollen, accompanied by dramatically reduced mechanical properties. σb, εb, and E of the gel at pH = 12 were 40 kPa, 640%, and 4 kPa, respectively. This was because Zr4+

Figure 5. Material property chart of the tearing fracture energy versus Young’s modulus of various soft materials. Materials include the Zr4+reinforced DN gels in this work, poly(vinyl alcohol) (PVA) gel,15 double network (DN) gel,22,23 alginate/polyacrylamide (Alg/PAAm) gel,26 PVA−PAAm gel,27 polyampholyte gel,16 PAAm gel,26 poly(Nacryloyl glycinamide) (PNAGA) gel,17 alginate gel,26 and cartilage and skin.5,6

200%, corresponding to the onset of necking. The small clusters of κ-CG network connected by the dense and flexible PAAm chains and served as cross-linking junctions of the second network, which can sustain extremely high strain and strength.22,24 When one gel sample was cyclically stretched to different εm, the sample in the subsequent loading experienced reduced stress before the previous εm, yet it reached similar stress at εm; further loading led to increased stress (Figure 6b).25 The newly created curves in successive cyclic loading of DN gel converged into a typical stress−strain curve (dotted line in Figure 6b), indicating the continuous structural destruction of the gel during the cyclic loading−unloading process. We noticed that the subsequent loading curve to εm was slightly higher than the previous unloading curve, probably due to the partial selfrecovery of the physically cross-linked first network of κ-CG. Because the double-helix junctions and the coordination bonds were destroyed during the loading and cannot effectively reform at room temperature, the DN gel did not have good selfrecovery capacity. However, the as-prepared DN gel (DN-300-3-0.01) showed better self-recovery by incubating it at high temperature than that of Zr4+ ion-reinforced DN gel (DN-300.1-3-0.01) (Figure S4), in which the metal-coordination

Figure 6. Hysteresis curves of multiple samples with various strains (a) and cyclic tensile loading−unloading curves of one sample with different trains (b). Inset in (a) shows the corresponding dissipated energy Γ and hysteresis ratios hs of one loop at different maximum strain εm. The loading and unloading stretch rate was 100 mm/min. F

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Figure 7. (a, b) Tensile stress−strain curves (a, c, e) and corresponding mechanical properties (b, d, f) of DN-30-0.1-3-0.01 gel equilibrated in saline solution with different CNaCl (a, b), in pure water under different temperature (c, d), and in solution with different pH (e, f). The swelling ratio in length, S, was also presented along with the mechanical properties; the reference state was the hydrogel in pure water at room temperature. Error bars represent the standard deviation of the mean.

Figure 8. Tensile stress−strain curves of equilibrated DN-30-0.1-3-0.01 hydrogel incubated under water for scheduled time up to 150 days (a) and the corresponding mechanical parameters (b). Error bars represent the standard deviation of the mean.

strength, temperature, and pH, as well as long-time storage, afforded these tough hydrogels an ideal structural material with promising applications in biomedical and engineering fields. 3.5. Influence of Dual-Cross-Linking of κ-CG. As stated above, the improved mechanical properties and stability of DN hydrogels were closely related to the dual-cross-linking of the first network; i.e., the κ-CG molecules were physically crosslinked by metal-coordination complexes and the formation of

ions formed hydroxides with the hydroxyl groups, which destroyed the Zr4+−sulfate coordination complex. The DN hydrogel also maintained excellent mechanical stability after long-time incubation in water. As shown in Figure 8, there was no evident change of the mechanical properties of the DN gel (DN-30-0.1-3-0.01) after being incubated under pure water at room temperature for 150 days. The good stability of the DN gel over a wide range of ionic G

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Figure 9. (a, b) Tensile stress−strain curves (a) and corresponding mechanical parameters (b) of as-prepared κ-CG/PAAm hydrogels previously prepared at different temperatures. (c, d) Tensile stress−strain curves (c) and corresponding mechanical parameters (b) of DN hydrogels in equilibrated state previously prepared at different temperatures. The tensile tests were performed at room temperature. Error bars represent the standard deviation of the mean.

Figure 10. Tensile stress−strain curves (a) and corresponding mechanical parameters (b) of DN hydrogels DN-30-0.1-3-0.01 reinforced by different metallic ions. Error bars represent the standard deviation of the mean.

indicated that the existence of double helix of κ-CG had positive contribution to the toughening of DN gels, which can be understood by considering the different conformations of κCG at 85 and 25 °C (Figure S2).37,38 Before the polymerization of AAm, κ-CG molecules can form ordered double helixes after the temperature was back to room temperature. However, after the polymerization that produced dense PAAm chains, the mobility of κ-CG molecules was dramatically reduced. Accordingly, κ-CG molecules cannot form ordered double helix in the DN gel when the temperature was decreased from 85 to 25 °C. Therefore, dual-cross-linking of the first network was indispensable for the excellence of mechanical properties of κ-CG/PAAm DN hydrogels. Without sulfate−Zr4+ coordination bonds, the DN hydrogels showed poor mechanical properties and stability; without double-helix junctions of κ-CG, the DN hydrogel was stable in water, yet the mechanical properties were dramatically reduced. 3.6. Unique Feature of Sulfate−Zr4+ Coordination Bonds. The as-prepared κ-CG/PAAm DN gel can also be cross-linked by other multivalent metallic ions, such as Al3+,

double-helix junctions. The significance of sulfate−Zr4+ coordination bonds was demonstrated by the huge differences of mechanical properties and stability of the equilibrated gels prepared with and without Zr4+ ions (Figures 1c and 4c). The Zr4+-reinforced first network of κ-CG improved the stability and mechanical strength of the DN gels. To investigate the effect of double-helix structure of κ-CG on the properties of DN hydrogels, we polymerized the second network under UV light irradiation at different temperatures. After polymerization, the hydrogel was cooled to room temperature and then incubated in the Zr4+ ion solution and pure water. As shown in Figures 9a and 9b, the as-prepared DN-30-0-3-0.01 hydrogel polymerized at 25 °C showed higher σb, εb, and E than that polymerized at 85 °C. Yielding was observed in the former gel yet absent in the latter one. After further cross-linking in the solution of Zr4+ ions, both gels showed improved σb and E, yet reduced εb, when compared to the as-prepared gels (Figures 9c and 9d). However, the Zr4+ ion-reinforced DN gel previously polymerized at 25 °C still possessed much better mechanical performances than that polymerized at 85 °C. These results H

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Macromolecules Fe3+, and Sm3+ ions. The obtained DN hydrogels were stable in water, yet their mechanical properties were quite different. The DN-30-0.1-3-0.01 hydrogels cross-linked by 0.1 M metallic ions are coded as DN-M, in which M is the metallic ions used for further cross-linking. As shown in Figure 10, DN−Zr4+ hydrogel showed much higher σb and E than other gels. The differential mechanical properties of DN gels should be associated with the different strengths of coordination bonds between the metallic ions and sulfate groups of κ-CG. For the lanthanide Sm3+ ion, its outer layer had 5s25p6 electrons, and the sub-outer layer contained unfilled 4f electrons that can accept electrons of the chelating agents to form coordination bonds. However, the outer-layer electrons had a strong “occlusion effect” to sub-outer-layer unfilled electrons, resulting in a relatively small coordination field of the Sm3+ ion.48 The high coordination strength of the Zr4+ ion with the sulfate group of κ-CG was related to its high charge and electronic field to form coordination bonds. Because the 5s orbit of the Zr4+ ion was empty and the 4p orbit was partially empty, along with high charge and small radius (0.72 Å), Zr4+ ions can form strong coordination bonds with chelating agents.49 In the aqueous solution of ZrOCl2, Zr4+ ions formed a strong complex [Zr4(OH)8(H2O)16]8+ with OH− groups, resulting in very low pH of the solution (pH of 0.1 M ZrOCl2 aqueous solution was ∼1).41,42 In addition, [Zr4(OH)8(H2O)16]8+ was a hard acid because its central ion had high positive charge, small radius, and low conformation deformation ability. The sulfate group of κ-CG was a hard base because the coordination atom of O had a high electronegativity of 3.44. Based on the classic coordination theory, [Zr4(OH)8(H2O)16]8+ can form a stable coordination complex with the sulfate group of κ-CG. 40 The high strength of Zr4+− sulfate coordination bonds greatly improved the stability and mechanical properties of the resultant DN hydrogels. The radius of Fe3+ and Al3+ ions was 0.65 and 0.54 Å, respectively, slightly smaller than that of the Zr4+ ion.49 However, the charge of Fe3+ and Al3+ ions was less than that of the Zr4+ ion. The relatively weak mechanical properties of DN−Fe3+ and DN−Al3+ suggested that the strength of coordination bonds was severely influenced by the charge number of metallic ions.

or synthetic polymers and expand the applications of tough hydrogels in diverse areas.50,51

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.macromol.8b02269.

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Figures S1−S5 (PDF)

AUTHOR INFORMATION

Corresponding Author

*E-mail [email protected]. ORCID

Zi Liang Wu: 0000-0002-1824-9563 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank Dr. Riku Takahashi for helpful discussions. This work was supported by the National Natural Science Foundation of China (51773179) and Thousand Young Talents Program of China.

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REFERENCES

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4. CONCLUSIONS In summary, we have developed tough κ-CG/PAAm DN hydrogels with improved mechanical properties and stability by using Zr4+ ions to further cross-link the first network of κ-CG. Thus, obtained transparent hydrogels were stable in water and possessed good mechanical properties, with σb of 1.5−3.2 MPa, εb of 300−2200%, E of 0.2−2.2 MPa, and G of 0.4−18.5 kJ/m2, superior to most tough hydrogels and soft biotissues. The excellent mechanical performances and good stability of these hydrogels were important for their potential applications in biomedical and engineering fields as a structural material. We found that dual cross-linking of κ-CG was indispensable for the excellent mechanical properties of the DN hydrogels. The sulfate−Zr4+ coordination bonds effectively improved the strength and stability of the first network and the DN hydrogels. The high strength of sulfate−Zr4+ coordination bond was associated with the high charge and unique electron field of the Zr4+ ion to form the coordination complex. The facile approach to reinforce the hydrogels by Zr4+ ions to form the coordination complex should be applicable to other natural I

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