Coassembly of Short Peptide and Polyoxometalate into Complex

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Co-assembly of short peptide and polyoxometalate into complex coacervate adapted for pH and metal ions triggered underwater adhesion Xiangyi Li, Tingting Zheng, Xiaohuan Liu, Zhanglei Du, Xiaoming Xie, Bao Li, Lixin Wu, and Wen Li Langmuir, Just Accepted Manuscript • DOI: 10.1021/acs.langmuir.9b00273 • Publication Date (Web): 20 Mar 2019 Downloaded from http://pubs.acs.org on March 21, 2019

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Co-assembly of short peptide and polyoxometalate into complex coacervate adapted for pH and metal ions triggered underwater adhesion Xiangyi Li, Tingting Zheng, Xiaohuan Liu, Zhanglei Du, Xiaoming Xie, Bao Li, Lixin Wu, Wen Li* State Key Laboratory of Supramolecular Structure and Materials, College of Chemistry, Jilin University. Qianjin Avenue 2699, Changchun 130012, China. KEYWORDS. peptide assembly, coacervate, responsive, phase transition, adhesion

ABSTRACT. The fabrication of peptide assemblies to mimetic the functions of natural proteins represents an intriguing aim in the fields of soft materials. Herein, we present a kind of novel peptide-based adhesive coacervates for the exploration of the environment-responsive underwater adhesion. Adhesive coacervates are designed and synthesized by self-assembled condensation of a tri-peptide and polyoxometalates in aqueous solution. Rheological measurements demonstrate that the adhesive coacervates exhibit shear thinning behaviour, which allows them to be conveniently delivered for interfacial spreading through a narrow gauge syringe without high pressure. The complex coacervates are susceptible to pH and metal ions, resulting in the occurrence of phase transition from fluid phase to gel state. Scanning electron microscopy demonstrats that the microscale structures of the gel-like phases composed of

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interconnected three-dimensional porous networks. The rheological study reveals that the gellike assemblies exhibited mechanical stiffness and self-healing property. Interestingly, the gellike samples show the capacity to adhere various wet solid substrates under the water line. The adhesion strength of the peptide-based gel is quantified by lap shear mechanical analysis. The fluid coacervate is further exploited in the preparation of “on-site” injectable underwater adhesives triggered by environmental factors. This finding is exciting and serves to expand our capability of the fabrication of peptide-based underwater adhesive in controllable way.

INTRODUCTION Recently, peptide assembly has driven substantial advancement in the creation of hierarchical nanostructures,1-3 sensors4 and functional materials5-9. One of the ultimate goals is to rationally design peptide assemblies that simulate the activity or functionality of natural proteins.10-12 Adhesive proteins secreted by marine organisms are impressive because of their unique ability to adhere on diverse submerged substrates in seawater.13,14 The wet adhesion capacity of that kind of proteins has inspired much research in developing biomimetic glue towards realizing ambitious applications, such as wound dressing, surgery glue, bone fixing and others.15-17 However, most of the biomimetic adhesives have centred on the covalent polymers.18,19 In great contrast, peptide-based adhesives have not intensely considered in most design efforts although peptide segments hold salient advantages in the development of biomedical glue, including biocompatibility, biodegradability, molecular diversity, and tunable bioactivity.20 In particularly, peptide with short amino acid sequences may serve as relatively simple model to understand or assess the complicated synergy of various residues of adhesive proteins at molecular level, and provide new insight into the rational design of biomimetic adhesives in wet environments.21,22


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The main concern on the peptide-based underwater adhesives is their poor cohesion or bulk mechanical strength attributed from the short peptide segments.23,24 To address this topic, our group have fabricated a kind of peptide-based supramolecular polymer by introducing anionic polyoxometalates (POMs) into cationic peptide matrix via ionic self-assembly strategy.25 The resultant peptide/POM adhesives exhibited high cohesion underwater line. Success in that endeavor critically relies on the multivalent electrostatic interactions between cationic peptide segments and anionic POMs. We proposed that the inorganic POM nano-clusters not only acted as cross-linkers to joint peptide segments together forming extend and robust 3D network structures, but also served as rigid fillers to improve their bulk mechanical strength.25 Despite the success in enhancing the cohesion of peptide-based adhesive, new challenge is now needed to be seriously confronted because a high cohesion, which is necessary to reach an adequate mechanical strain, normally causes poor interfacial adhesion in water. Fortunately, natural systems have evolved adaptable way to solve the aforementioned competition. As reflected in several reports,13,14,26-28 mussel or sandcastle worm first produced adhesive protein coacervate, which exhibited fluid-like property, low interfacial energy, excellent spreading capacity and interfacial bonding contact onto wet surfaces. After spreading and bonding, the adhesive coacervate could be cured and solidified quickly to improve their cohesion through covalent and/or non-covalent bonds.29,30 These natural systems have presented a captivating insight that the realization of “on-site” peptide adhesives with improved adhesion performance requires the rational design of peptide coacervate with controllable gelation or curing behavior. With this information in mind, we tried to explore a kind of complex coacervate (labelled as Pep1/SiW11) consisting of cationic peptide 1 (Pep1) and anionic K8[α-SiW11O39] (SiW11). As shown in Fig. 1a, Pep1 contains chemically versatile histidine residue and carboxyl group, which is highly


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sensitive to pH and metal ions. It is expected that the environment-responsive functional units encoded in the sequence of Pep1 allows one to mediate the adhesion and cohesion of the Pep1/SiW11 coacervate. For comparison purpose, two analogous peptides (Figure 1a) Pep2 and Pep3 were designed through replacing the histidine residue of Pep1 by phenylalanine and valine, respectively.

Figure 1. Schematic drawing of the designed short peptides (a), the topology structures of the polyoxometalates (b), and the packing model of the Pep1/SiW11 coacervate (c).

EXPERIMENTAL SECTION Materials. Three polyoxometalates (POMs), such as K8[α-SiW11O39] (labelled as SiW11), Na9[PW9O34] (labelled as PW9) and K6CoW12O40 (labelled as CoW12), were synthesized according to reported procedures.31-33 Co(CH3COO)2, Ni(CH3COO)2, Mn(CH3COO)2,


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Mg(CH3COO)2 and Ca(CH3COO)2 were purchased from Macklin. Short peptides, such as Pep1 (GHK), Pep2 (GFK) and Pep3 (GVK), are commercial compounds, which were purchased from Bide Pharmatech Ltd. The corresponding purity of the peptides was supported by mass spectra (Figure S1) and High Performance Liquid Chromatography (Figure S2). All the commercial reagents were used as received without any further purification. The deionized water was utilized in all the experiments. Measurements. The Fourier transform infrared (FT-IR) spectrum of all the lyophilized samples were recorded on a Bruker Optics Vertex 80 V FT-IR spectrometer equipped with a DTGS detector (32 scans) with a resolution of 4 cm−1 using KBr pellet. Electrospray ionization mass spectra (ESI-MS) data was acquired on a Bruker Daltonics Esquire 6000 spectrometer system. The solutions were injected directly into the evaporation chamber. The mass spectrometer was operated in the positive ion reflector mode. The elemental analysis (C, H, N) was carried out on Elementar vario MICRO cube (Germany). X-ray photoelectron spectroscopy (XPS) was performed on ESCALAB Mark (VG Company, UK) 250 spectrometer with a monochromic Xray source. XPS measurements were carried out using Al-K X-rays (1489.6 eV) and the binding energy of C (1s) at 284.6 eV was taken as a standard. Analysis of the data was carried out with XPS PEAK (version 4.1) software. The background was subtracted using a Shirley function. The peaks were fitted using a nonlinear, least squares routine with a mixture of GaussLorentz functions for the C 1s and N 1s spectra. The subtracted background was indicated at the bottom, whereas the sum of the kernels of the curve fit was drawn at the top. Peak widths (FWHMs) were not fixed, to account for variation between different chemical states. Scanning electron microscopy (SEM) images were acquired on a JEOL FESEM 6700F electron microscope with an accelerating voltage of 15 kV. SEM samples were prepared by casting the


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heated gel-like complex on glass slices, and then lyophilized under vacuum for 1 day. The optical photographs were taken on a Zeiss Axioskop 40 optical microscope before and after coalescence of coacervate droplets. Glass slides were used as a substrate for the coacervate for all microscopic observations. The viscosity behaviour of the coacervate was studied by rheological measurements using TA instrument AR2000 controlled-stress rheometer equipped with 8 mm stainless steel parallel plate geometry. A gap distance of 0.5 mm and a temperature of 25 oC were used for all the experiments. Frequency sweep data were collected in the range from 0.01 to 100 rad/s, and the strain amplitude was fixed at 0.1%. All the rheological measurements were repeated a minimum of three times. The self-healing behavior of the Pep1/SiW11 gel complexes were determined by time-dependent dynamic rheology. The gels were first broken by applying a 50% strain through a strain amplitude sweep, which caused the moduli values to diminish drastically. The healing of the gel complexes were then monitored over time by continuing to oscillate the adhesive at low (0.1%) strain amplitude, which was in the linear viscoelasticity region and did not disrupt the network. The self-healing behavior of the gel complexes were also tested by the time-dependent recovery measurements using alternating strains of 0.1% and 50%. The strains were applied in a cycle of 60 seconds each (each cycle included 60 seconds of 0.1%, 60 seconds of 50%, and 60 seconds of 0.1%) and repeated for several such cycles. Adhesion behavior was studied on Instron 5944 materials testing system. The as-prepared Pep1/SiW11 gel-like complexes were scraped from the bottom of the glass bottle and used to adhere two rectangle-shaped substrate surfaces, such as glass, titanium, polypropylene and stainless steel. A piece of gel-like complex was placed between two plates with compression and the compressed plates were quickly putted into deionized water for two hours with 35 kPa pressure to promote the gel to uniformly form a lap shear joint of 1.8 × 2 cm2.


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Then, the adhered plates were clamped into the grips of the materials testing system and immersed into a water holder at room temperature (25 oC). The force vs. displacement profile was recorded using a crosshead speed of 10 mm/min and a 100 N load cell. Each sample was tested on the basis of five replicate measurements. The shear adhesion strength was calculated from the maximum force at joint failure divided by the adhesion area and averaged. The detached gel samples from substrates were recompressed between two plates using the same procedure as in their initial adhesion process. The regenerated adhesion strength was quantified under the same condition. The UV/vis spectra were recorded at room temperature using an UVvisible spectrophotometer (Varian Cary 50) over a range of 200-800 nm. RESULTS AND DISCUSSION Formation of Pep1/SiW11 complex coacervates. Pep1 (340.38 mg, 0.8 mL deionized water) and K8[α-SiW11O39] (SiW11, 746.77 mg, 4 mL deionized water) aqueous solutions (pH = 6.5) were prepared, respectively. After the very first mixing of Pep1 and SiW11 at 25 oC, turbid aqueous solution containing colloidal complexes were formed. Subsequently, a liquid-liquid phase separation occurred in the time course of minutes, and water immiscible complex coacervate phase was observed at the bottom of the glass bottle (Figure 2a). The formation of Pep1/SiW11 complex coacervate is independent of the mixing procedures. The amount of Pep1/SiW11 coacervate scaled linearly with the concentration of the parent solutions. Further insight into the coacervation was gained by testing the -potential evolution and the phase transition upon the titration of Pep1 into aqueous solution of SiW11 at pH 6.5. As shown in Figure S3, stable SiW11 solution maintained low -potentials (-45 to -30 mV). With the addition of Pep1 to SiW11 solution, a dramatic rise in the -potentials was observed, which corresponded


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to the ionic interaction between cationic Pep1 and polyanionic SiW11. Once the Pep1:SiW11 molar ratio reached a critical value 6.5:1, a phase transition occurred and turbid solution was observed. The phase transition from transparent solution to coacervate attributed to the formation of ionically cross-linked Pep1/SiW11 coacervate at macroscopic level. With further increasing the amount of Pep1, the -potentials continued to grow (e.g.,-24 mV at 6:1 and -19 mV at 9:1) until the molar ratio of Pep1:SiW11 approached 11:1. Above this point, the -potentials increased slowly and a phase transition from coacervate state to transparent solution occurred.

Figure 2. (a) digital images of complex coacervate formed from the co-assembly of peptides and polyoxometaltes, (Pep1 1.25 M , SiW11 62.5 mM , CoW12 83.3 mM , PW9 55.6 mM. The charge ratio of peptide to POMs was kept at 1:1); (b) the pH and metal ions triggered gelation of Pep1/SiW11 coacervate at pH = 6.5.


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Inspection of the turbid solution of Pep1/SiW11 by optical microscopy revealed the presence of spherical dense droplets (Figure 3a) with polydisperse sizes. Over elapsed time, the droplets coalesce with each other and expand into space-spanning morphology (see Figure 3b, highlighted by colored arrows). The time dependent coalescence and morphological change of coacervate samples indicate the fluidic property of Pep1/SiW11 complexes. A higher viscous modulus (G) than elastic modulus (G) determined by dynamic rheology measurement in the entire investigated angle frequency range also demonstrates the liquid-like nature of Pep1/SiW11 coacervate (Figure 3c). Shear-dependent viscosity curve (Figure 3d) revealed a non-Newtonian fluid nature of Pep1/SiW11 complex based on the typical shear-thinning behavior.

Figure 3. (a) optical micrograph of coacervate droplets of Pep1/SiW11 with a cover slide; (b) optical micrograph of coacervate droplets of Pep1/SiW11 from (a) after several minutes, the coalescence and morphological change of the coacervate droplets occurred; (c) plot of storage modulus and loss modulus as a function of angular frequency for the Pep1/SiW11 coacervate phase; (d) viscosity vs. shear rate profile of the Pep1/SiW11 coacervate phase.


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In order to better understand the driving forces behind the coacervation process of Pep1/SiW11 complex, detailed characterizations were performed. ESI-MS spectra (Figure S4) showed that the Pep1 segment did not decomposed during the coacervation process. The FT-IR spectra (Figure S5) of SiW11 alone in the low frequency-region displayed strong vibration bands at 995, 952, 885, 796, and 725 cm−1, which were assigned to νas(W=Od), νas(W-Ob-W), νas(W−Oc-W) stretching vibration modes, respectively.34 In the case of lyophilized Pep1/SiW11 coacervate (Figure S5), the stretching vibration modes of SiW11 slightly shift to 991, 943, 879, 790, 725 cm−1, respectively. The slightly shift arose from the interaction between Pep1 and SiW11 cluster.35 FT-IR spectra of lyophilized Pep1/SiW11 powder also showed that the amide I band at 1659 cm−1, suggesting that the Pep1 segments adopted random-coil conformation.36 Additionally, the lack of new band over 1700 cm−1 implied that the -COOH of Pep1 segment within the coacervate matrix adopted deprotonated form (carboxylate group).37 This is not a surprise since the pH value of the reaction solution is 6.5, which is higher than the pKa (~2.2) of

-COOH of Pep1. Elemental analysis (EA) revealed that the lyophilized Pep1/SiW11 powder possessed C 11.29%; H 2.04%; N 5.41%, implying that the average molar ratio of Pep1 to SiW11 within the adhesive matrix should be 2.4 : 1. XPS spectra of the lyophilized Pep1/SiW11 sample at pH =6.5 were shown in Figure 4. The N1s peak at 401.3 eV corresponds to the binding energy of protonated amine groups of both NH2 (glycine) and -NH2 (lysine), while the peak at 399.6 eV arises from the nitrogen atom of amide bond (N-C=O).38,39 The peaks at 400.4 and 398.7 eV are assigned to the nitrogen atoms of NH and N of neutral imidazole ring, respectively.40,41 It is plausible to infer that the coacervation is closely related to the electrostatic attraction between anionic SiW11 and protonated amine groups of Pep1 because the similar coacervates could be synthesized by mixing Pep1 with other


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anionic POMs, such as CoW12 and PW9 (see Figure 2a). To gain further insight into the driving forces behind the coacervation, we also prepared two analogous peptides (Figure 1) through replacing the histidine residue of Pep1 by phenylalanine in Pep2 and valine in Pep3, respectively. Control experiment performed by mixing Pep2 and SiW11 in aqueous solution also showed the formation of complex coacervate Pep2/SiW11 (Figure 2a). In great contrast, transparent solution was obtained when Pep3 and SiW11 cluster was mixed under the same condition (Figure 2a). The above results clearly corroborated that the complex coacervate Pep1/SiW11 was primarily governed by the electrostatic interactions (Figure 1c) but may involve other weak interactions such as hydrophobic association among neutral imidazole rings, and/or hydrogen bond between SiW11 and neutral imidazole ring.

Figure 4. XPS spectrum for N1s of Pep1/SiW11 complexes: (a) coacervate at pH = 6.5; (b) coacervate at pH = 5.5; (c) gel at pH = 4.5.


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pH dependent gelation and adhesion of Pep1/SiW11 complex coacervate. The side chain of histidine residue of Pep1 can change from neutral imidazole unit to positively charged one at low pH, which allows us to mediate the phase transition as well as the cohesion of Pep1/SiW11 coacervate. As the pH value decreased gradually from 6.5 to 4.5, the Pep1/SiW11 complex changed from fluid coacervate to adhesive gel state (Figure 2b). However, the gel became hard and lost it adhesive property once the pH value decreased to 2.5 (ie., to near the effective pKa of

-COOH). Time-dependent viscosity curves with constant shear rate (1%) confirmed a progressive increase in viscosities with the decrease of pH value. As detailed in Figure S6, the viscosity of Pep1/SiW11 complex increased from 3.59  0.61 Pas at pH = 6.5, through 14 0 .37 Pas at pH = 5.5, 20.2  0.48 Pas at pH = 5, to 73.4  0.39 Pas at pH = 4.5. XPS spectra revealed that the pH-dependent phase transition was directly related to the protonation of histidine residue of Pep1. As shown in Figure 4b, at pH = 5.5, the N1s peaks at 401.6, 400.3, 398.8 and 399.8 eV correspond to the nitrogen atom of -NH3+, -NH3+, NH and N of imidazole ring, N-C=O, respectively. A new peak appeared at 401.0 eV arose from the equivalent nitrogen atoms of protonated imidazole ring.40 With decreasing the pH value to 4.5, the peaks belong to the nitrogen atom of NH and N of imidazole ring disappeared (Figure 4c), suggesting that the completely protonation of histidine residue within the matrix of Pep1/SiW11 gel. There is good correspondence between the phase transition and the protonation of histidine residue. It is evident that the protonated histidine residues enhanced the ionic cross-linking density and binding strength between Pep1 and SiW11 cluster, leading to the formation of robust network structures. Additionally, the Pep1/SiW11 gel obtained at pH = 4.5 can contain only 15~17% water (weight %), which is lower than that of corresponding coacervate sample (23~26% water). This lower water content also implied very dense network structures. The microstructure of


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Pep1/SiW11 gel was investigated by scanning electron microscope (SEM). As represented in Figure 5a, the freeze-drying gel sample exhibited fibrous morphology, which entangled with each other to form extend and interconnected 3D networks.

Figure 5. SEM images of Pep1/SiW11 gel at pH = 4.5 (a), and Pep1/SiW11/Co2+ gel at pH = 6.5 (b).

The gel-like property of the Pep1/SiW11 complex at pH = 4.5 was confirmed by dynamic rheology, and both storage modulus (G) and loss modulus (G) were determined as a function of strain and frequency (Figure 6). The amplitude sweep was performed at a constant frequency of 1.0 rad/s to assess the linear viscoelastic range. Above the critical strain of 0.1%, the storage modulus decreased dramatically and crossover (structure breakdown) point was observed at 1.5% (Figure 6a). Frequency sweep studies at a constant strain of 0.1% showed that the storage modulus (G) is higher than the loss modulus (G) for the entire frequency range (Figure 6b), indicating a viscoelastic nature.42,43 Furthermore, the time kinetics experiment (Figure 6c) showed that the storage modulus (G) and the loss modulus (G) of Pep1/SiW11 kept no substantial change by continuing to oscillate the sample with low strain amplitude (0.1%) and angle frequency (1 rad/s), indicating the good stability of the three dimensional matrix of the gel. When the Pep1/SiW11 gel was first broken by applying a 50% strain through a strain amplitude sweep, it caused the moduli values to diminish drastically. And the healing of the adhesive was


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then monitored over time by continuing to oscillate the gel at low (0.1%) strain amplitude. As demonstrated in Figure S7, the Pep1/SiW11 gel sample recovered its original G value within 1215 min, implying a fast self-healing ability. The continuous step strain measurement was further conducted to study the self-healing behaviour of the Pep1/SiW11 gel (Figure 6d). Initially, the gel sample was subjected to a low strain (strain = 0.1%; angle frequency= 1 rad/s), as a result G and G showed no obvious changes. However, the G and G values immediately decreased after the gel was treated under higher strain of 50% and maintains for 60 seconds. At this point, G is lower than G, suggesting a collapsed state. Upon the strain returned to 0.1%, both G and G recovered quickly to the initial values without significant loss. This recovery behavior was totally reversible and reproducible during ten consecutive cycle tests. This rapid self-healing ability of Pep1/SiW11 gel arose from the dynamic and reversible non-covalent interactions, which is similar to the reported supramolecular adhesives.44,45


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Figure 6. Rheological behavior of the Pep1/SiW11 gel (pH = 4.5) at 25 °C: (a) strain sweep from 0.001 to 100 % at the frequency of 1.0 rad/s; (b) frequency sweep analysis from 0.1 to 100 rad/s with a constant strain of 0.1%; (c) time sweep for 1 h with frequency of 1 rad/s and strain of 0.1%; (d) self-recovery test with alternating oscillation forces (strain = 0.1% or 50%) for 10 consecutive cycles.

The Pep1/SiW11 gel (pH = 4.5) exhibited enhanced cohesion and remarkably versatile adhesion to solid substrates (such as glasses, metals, polymers, and natural surfaces) under the water line (Figure 7a). These properties enabled the Pep1/SiW11 complex to serve as pressuresensitive underwater adhesives. The adhesion strength was performed using titanium (Ti), polypropylene (PP), glass and stainless steel (SS) as representative substrates. The adhesive application was performed under deionized water by applying a compressive pressure of 35 kPa and a contact time of 2 hours. After that, the adhered plates were pulled apart immediately by a material testing system equipped with a deionized water holder. The force versus displacement curves (Figure 7b) were obtained when the adhered plates were separated at rate of 10 mm/min.


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It should be noted that the detachment force of Pep1/SiW11 gel (pH = 4.5) did not rapidly decrease after the maximum point but instead exhibited a gradual decrease to the distance approximately several millimeter, indicating the extensive degrees of intermolecular interactions within the gel matrix. Maximum force at failure was divided by substrate overlap area to quantify the shear adhesion strength. As shown in Figure 7c, the average adhesion strengths for titanium, PP, glass and stainless steel substrates are 36.51 ± 3.00, 32 ± 3.69, 32.73 ± 4.11 and 34.81 ± 1.97 kPa, respectively.

Figure 7. Underwater adhesion behaviour of Pep1/SiW11 gel (pH = 4.5): (a) photographs for attaching various dissimilar substrates (glass, aluminium (Al), stainless steel (SS), polyether−ether−ketone (PEK), polypropylene (PP), titanium (Ti)); (b) a typical force vs displacement curve for lap shear joint of solid substrates glued by Pep1/SiW11 gel; (c) average shear adhesion strengths of Pep1/SiW11 gel bonded different substrates.

Metal ions triggered gelation and adhesion of Pep1/SiW11 complex coacervates. Another significant character of the Pep1/SiW11 coacervate is its ability to coordinate with metal ions. As shown in Figure 2b, phase transition was seen to happen and colored adhesive gel sample was


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observed when the coacervate sample were subjected to metal ions (such as Co2+, Ni2+ or Mn2+ with ionic concentration of 100 mM) in aqueous solution at pH = 6.5. UV-vis spectra of Co2+ aqueous solution in the presence of Pep1/SiW11 coacervate was performed. As shown in Figure S8, the peak intensity at 513 nm, corresponding to the absorbance of Co2+ in aqueous solution decreased with an increase of the amount of Pep1/SiW11 coacervates, which supports the Co2+ uptake of Pep1/SiW11 coacervate. XPS data (Figure S9) provide enough evidence that both the imidazole and carboxyl groups coordinated with Co2+ ions within the matrix of the Pep1/SiW11/Co2+ gel. This metal ion triggered gelation process (Figure S10) was also observed in the case of Pep1/CoW12 and Pep1/PW9 coacervates, respectively. However, no gelation process (Figure S10) was observed according to the control experiment performed by mixing the Pep1/SiW11 coacervate with Ca2+ or Mg2+, indicating the selective metal coordination of Pep1 components. Interestingly, the adhesive gels can tolerate the salt variety (Figure S11). The above results confirmed the fact that the coordination interactions between metal ions and Pep1 contribute to the increased cross-linking density of the resultant gels. The formation of crosslinking network structure was identified by SEM. As shown in Figure 5b, the microscopic morphology of the freeze-dried Pep1/SiW11/Co2+ gel contained sheet-like structures, which connected with each other to form porous 3D networks with a mesh size from several to tens micrometers. The viscoelastic characteristic of the adhesive Pep1/SiW11/Co2+ gel was investigated from Figure 8 through dynamic rheology. Frequency sweep data (Figure 8a) revealed that the values of G are greater than G for Pep1/SiW11/Co2+ gel, demonstrating the gel-like behaviour.42,43 The self-healing ability was further identified by subjecting gels to varying strains of 0.1 to 50%, for a cycle of 60 sec each (Figure 8b). Upon the oscillatory strain with large amplitude (50%), the storage modulus (G) immediately dropped and became


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instantaneously lower than G, indicating the destruction of the network.46,47 When the applied strain was returned to 0.1%, the Pep1/SiW11/Co2+ gel exhibited the recovery of both G and G without obvious changes. The G value was found to be constant for twenty consecutive cycles, suggesting that the gel regained its stiff structure and cohesion after getting deformation at higher strain.

Figure 8. Rheological behavior of the Pep1/SiW11/Co2+ gel (pH = 6.5) at 25 °C: (a) frequency sweep analysis from 0.1 to 100 rad/s at a constant strain of 0.1%; (b) self-recovery test for twenty consecutive cycles with alternating oscillation forces (strain = 0.1% or 50%).

Water blasting experiment further supported the mechanical stiffness of the adhesive Pep1/SiW11/Co2+ gel. The gel sample was coated onto the surface of watch glass without applied compressive force. After setting 20 s in water, the coating achieved sufficient adhesion to glass surface could resist water blasting. This is well visualized by a series of photographs at setting time intervals, as in Figure 9a (also see supporting information Video 1 for the water blasting result). The increased size of the Pep1/SiW11/Co2+ coating with water blasting time indicates the soft state of the metal ion-triggered gel. However, the parent Pep1/SiW11 coacervate could be erasable under the same blasting condition within 3 seconds (Figure 9b and Video 2).


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Figure 9. Photographs of Pep1/SiW11/Co2+ gel (a) and Pep1/SiW11 coacervate (b) subjected to water blasting.

The higher mechanical property of the gel structure means enhanced cohesion. As demonstrated in Figure 10a, the glass slides jointed by Pep1/SiW11/Co2+ gel could withstand a 100 g load, however, adhesion failure was observed for Pep1/SiW11 coacervate with a 10 g load (Figure 10b). These properties suggest that the Pep1/SiW11 coacervate has potentials in the development of metal ions-triggered underwater coating and glue. The quantitative lap shear mechanical analysis of Pep1/SiW11/Co2+ gel against different types of substrates was further performed under the water line. The shear strength, defined as a maximum adhesion force divided by a contact area, is almost independent of the substrate type (see Figure 10c, 15.45± 2 for PP, 16.46 ± 2.2 kPa for glass, 21.1 ± 2.5 kPa for stainless steel, and 17.1 ± 2.7 kPa for titanium). Remarkably, the Pep1/SiW11/Co2+ gel exhibited similar shear strength for the substrates. Additionally, the self-healing ability of the Co2+ triggered gel allows the generation of reversible bonding after detachment. As shown in Figure 10d, after the initial gel detachment and recompression,

the

gel

recovered

its

original

adhesion

strength

in

the

third


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attachment/detachment cycle. This recovered shear strength upon reattachment should attribute to the reversibly non-covalent bonds and the excellent self-healing property of the Pep1/SiW11/Co2+ gel.

Figure 10. (a) underwater adhesion behaviour of Pep1/SiW11/Co2+ gel (pH = 6.5) compressed between two glass slides with a 100 g load; (b) underwater adhesion failure of Pep1/SiW11 coacervate (pH = 6.5) compressed between two glass slides with a 10 g load; (c) underwater shear adhesion strengths of Pep1/SiW11/Co2+ gel bonded different substrates (PP, glass, SS, and Ti); (d) the underwater shear strength of Pep1/SiW11/Co2+ gel as a function of the attachment/detachment cycles (obtained from SS substrates).

This metal ions triggered gelation of the Pep1/SiW11 coacervate was further exploited to fabricate injectable underwater adhesive. To demonstrate this, a piece of conch was first immersed into a watch-glass containing an aqueous solution of Co2+ ion, then the low-viscosity Pep1/SiW11 coacervate was injected onto target site through a fine needle (see Video 3). Photographs were recorded in Figure 11, the coacervate droplets around the conch did not disperse in the Co2+ aqueous solution after injecting, and quickly changed into adhesive gel-like phase within 30 min. After 2 hours, the completely cured gel can ensure the conch to be adhered


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onto the bottom of the watch-glass. Thus, the metal ions triggered phase transition and curing of the Pep1/SiW11 coacervate can be utilized to develop “on-site” delivering underwater adhesive.

Figure 11. Photographs illustrating the “on-site” delivery and adhesion experiments of Pep1/SiW11 coacervate in the aqueous solution of Co2+ ions: (a) conch inside a watch-glass containing Co2+ aqueous solution; (b) injection of Pep1/SiW11 coacervate through a fine needle; (c) the coacervate droplets being injected into the Co2+ aqueous solution; (d) injected coacervate droplets adhering around the conch; (e) droplets after injection; (f) the droplets changing into gel phase after 30 min; (g) removing the Co2+ aqueous solution after the gel phase being kept for 2 hours; (h) tilt test demonstrating the conch to be adhered to the original site of the watch-glass.

CONCLUSIONS We reported a new kind of adhesive coacervates, consisting of short peptides and polyoxometalates, driven by electrostatic interactions and possible hydrogen bond or hydrophobic effect. These condensed coacervates could be considered as a new kind of softstate polyoxometalates as descripted in recent publications.48,49 The phase transition from fluid coacervate to gel state was achieved by adjusting pH value or metal ions species, which indicated the possibility to conveniently improve the cohesion and mechanical property of the peptidebased adhesive coacervates. We demonstrated how the adhesive coacervate can be exploited to


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prepare “on-site” deliverable underwater adhesive composed of low-viscosity coacervate that solidified into gel-like glue with environmental factors upon injection into target site. Our preliminary experiments suggest the possible advantage that the relatively simple sequences of short peptides enable such system to be truly ideal model in the evaluation of the synergistic effects of amino acid residues at molecular level and in the development of biomimetic adhesive materials with convenient delivery and controllable curing. ASSOCIATED CONTENT Supporting Information. ESI-MS spectra and HPLC data of peptides, FT-IR, ESI-MS, and viscosity data of Pep1/SiW11 coacervate, and XPS spectra, the photographs of various peptides/POMs coacervates subjected to metal ions (PDF). Supporting videos (AVI). AUTHOR INFORMATION Corresponding Author. *E-mail: [email protected] Author Contributions. The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. Notes. The authors declare no competing financial interest. Funding Sources. This work was funded by National Natural Science Foundation of China (NSFC) (21822201, 21573091). ACKNOWLEDGMENT The current research was supported by NSFC (21822201, 21573091).


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ABBREVIATIONS Polyoxometalate (POM), K8[α-SiW11O39] (SiW11), Na9[PW9O34] (PW9) and K6CoW12O40 (CoW12), Fourier transform infrared (FT-IR), Electrospray ionization mass spectra (ESI-MS), Xray photoelectron spectroscopy (XPS), Scanning electron microscopy (SEM), titanium (Ti), polypropylene (PP), stainless steel (SS) REFERENCES (1) Makam, P.; Gazit, E. Minimalistic Peptide Supramolecular Co-Assembly: Expanding the Conformational Space for Nanotechnology. Chem. Soc. Rev. 2018, 47, 3406−3420 (2) Wang, D.; Li, Z.; Hu, X.; King, S. M.; Rogers, S. E.; Cox, H.; Waigh, T. A.; Yang, J.; Lu, J. R.; Xu, H. Nanoribbons Self-Assembled from Short Peptides Demonstrate the Formation of Polar Zippers between β-Sheets. Nat. Commun. 2018, 9, 5118. (3) Guyon, L.; Lepeltier, E.; Passirani, C. Self-Assembly of Peptide-Based Nanostructures: Synthesis and Biological Activity. Nano Res. 2018, 11, 2315−2335. (4) Hauser, C. A. E.; Maurer-Stroh, S.; Martins, I. C. Amyloid-Based Nanosensors and Nanodevices. Chem. Soc. Rev. 2014, 43, 5326−5345. (5) Zhan, J.; Cai, Y.; He, S.; Wang, L.; Yang, Z. M. Tandem Molecular Self-Assembly in Liver Cancer Cells. Angew. Chem. Int. Ed. 2018, 57, 1813−1816. (6) Zhou, J.; Du, X.; Chen, X.; Wang, J.; Zhou, N.; Wu, D.; Xu, B. Enzymatic Self-Assembly Confers Exceptionally Strong Synergism with NF-κB Targeting for Selective Necroptosis of Cancer Cells. J. Am. Chem. Soc. 2018, 140, 2301−2308. (7) Sato, K.; Hendricks, M. P.; Palmer, L. C.; Stupp, S. I. Peptide Supramolecular Materials for Therapeutics. Chem. Soc. Rev. 2018, 47, 7539−7551. (8) Zozulia, O.; Dolan, M. A.; Korendovych, I. V. Catalytic Peptide Assemblies. Chem. Soc. Rev. 2018, 47, 3621−3639.


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(49) Barman, S.; Das, S.; Sreejith, S.; Garai, S.; Pochamoni, R.; Roy, S. Selective light driven reduction of CO2 to HCOOH in water using a {MoV9}n (n = 1332–3600) based soft-oxometalate (SOM). Chem. Comm, 2018, 54, 2369–2372.

Entry for the Table of Contents Peptide assembled coacervate was designed and synthesized to mimetic the “on-site” delivery and underwater adhesion behavior of adhesive proteins secreted by natural sessile organisms.


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Coassembly of Short Peptide and Polyoxometalate into Complex

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