Salt-induced thermal gelation of xyloglucan in aqueous media

The influence of Na2SO4 as a kosmotropic salt on the thermogelation of xyloglucan (XG) solutions was measured by rheology. The gelation occurred at lower temperatures and shorter times when the salt concentration was increased above 0.5 mol.L−1. For Na2SO4 concentrations equal to 1 mol.L−1, a not thermoreversible elastic hydrogel was obtained.

Carbohydrate Polymers 223 (2019) 115083 Contents lists available at ScienceDirect Carbohydrate Polymers journal homepage: www.elsevier.com/locate/carbpol Salt-induced thermal gelation of xyloglucan in aqueous media a a a Caroline Novak Sakakibara , Maria Rita Sierakowski , Romelly Rojas Ramírez , ⁎ Christophe Chassenieuxb, Izabel Riegel-Vidottic, Rilton Alves de Freitasa, a b c T BioPol, Chemistry Department, Federal University of Paraná, 81531-980, Curitiba, PR, Brazil IMMM, UMR CNRS 6283, Polymers, Colloids, Interfaces Department, Le Mans Université, 72085, Le Mans Cedex 9, France Macromolecules and Interface Group, Chemistry Department, Federal University of Paraná, 81531-980, Curitiba, PR, Brazil ARTICLE INFO ABSTRACT Keywords: Xyloglucan Hydrogel Gel Conformation Temperature Kosmotropic salt The influence of Na2SO4 as a kosmotropic salt on the thermogelation of xyloglucan (XG) solutions was measured by rheology The gelation occurred at lower temperatures and shorter times when the salt concentration was increased above 0.5 mol.L−1 For Na2SO4 concentrations equal to mol.L−1, a not thermoreversible elastic hydrogel was obtained Salts containing various types of anions were used, and it was observed that SO42−, HPO42− and H2PO4− promoted the formation of a gelled network The gel structure was observed using confocal laser scanning microscopy and scanning electron microscopy In XG containing SO42 at mol.L−1aggregates and gels were formed by interconnected sub-micrometer XG particles Increasing the concentration of SO42− led to conformation changes in the XG, from a twisted/helical to an extended/flat conformation, as observed using circular dichroism The naturally occurring hydrophobic sequences promoted an economically feasible XG gelling that may produce thermo and kosmo-sensitive hydrogels Introduction Xyloglucan (XG) is a neutral biopolymer extracted from legume seeds and formed by 1→4 linked β-D-glucopyranose (Glc) units with some glucose units substituted at O-6 by α-D-xylopyranose (Xyl), in which some units can be substituted at O-2 by β-D-galactopyranose (Gal) (Carpita & McCann, 2000) In water, XG forms a viscous fluid It is commonly employed in the food industry as an emulsifier, thickener and emulsion stabilizer Due to its biodegradability, biocompatibility, bioadhesion and low-toxicity, XG is also used in the pharmaceutical industry and in biomedical applications (Ghelardi et al., 2004; Sano et al., 1996; Suisha et al., 1998) These features also allow XG to be used as an in-situ gelling polymer An efficient way to produce hydrogels is by using partially degalactosylated XG, in which the galactose is enzymatically removed from the lateral chain (Brun-Graeppi et al., 2010; Nisbet et al., 2006; Shirakawa, Yamatoya, & Nishinari, 1998; Sakakibara, Sierakowski, Chassenieux, Nicolai, & de Freitas, 2017) Other researchers have reported the formation of thermosensitive gels from XG using eriochrome black T (Hirun, Tantishaiyakul, & Pichayakorn, 2010), alcohols ⁎ (Yuguchi, Kumagai, Wu, Hirotsu, & Hosokawa, 2004), epigallocatechin gallate (Nitta, Fang, Takemasa, & Nishinari, 2004), gallic acid (Hirun, Bao, Li, Deenc, & Tantishaiyakul, 2012; Hirun, Tantishaiyakul, Sangfai, Rugmai, & Soontaranon, 2016) and Congo red (Yuguchi, Hirotsu, & Hosokawa, 2005) Yuguchi, Fujiwara, Miwa, Shirakawa, and Yajima (2005) observed color formation and gelation of XG in mixture with iodine (I5−) solutions The authors assumed that two side-by-side XG chains were involved in the association with I5− As previously observed by Freitas et al (2015), XG naturally presents some hydrophobic domains associated with Gal free XG zones Our hypothesis is that such hydrophobic intermolecular interactions are very sensitive to the ionic strength and can be promoted by adding salt They can also be combined with a salting out effect, which is a competition between the polymer and the salt for water Several manuscripts are published about the effect of salts in the polysaccharide gelation For example, konjac glucomannan (KGM), a naturally gelling and acetylated polymer, forms gel induced by salts (Yin, Zhang, Huang, & Nishinari, 2008) According to them, higher the temperature or salt concentrations, stronger is the salting out effect, Corresponding author E-mail address: rilton@quimica.ufpr.br (R.A de Freitas) https://doi.org/10.1016/j.carbpol.2019.115083 Received 23 April 2019; Received in revised form 25 June 2019; Accepted 12 July 2019 Available online 19 July 2019 0144-8617/ © 2019 Elsevier Ltd All rights reserved Carbohydrate Polymers 223 (2019) 115083 C.N Sakakibara, et al Fig Time dependence of G’ and G” for solutions of wt% XG with (A) 0.5 mol.L−1, (B) 0.65 mol.L−1 (C) 0.75 mol.L−1 and (D) 1.0 mol.L−1 Na2SO4 The samples were kept for 16 h at 50 °C (E) tg−1 (s−1) was plotted as a function of Na2SO4 concentration The lines are guides for the eye promoting polymer aggregation and gelation Based on circular dichroism (CD) there is no evidence of conformational changes and the gelation was associated to Na2SO4 effect on intermolecular association of KGM rather than to a chain conformation change The same authors observed that salts as NaCl, NaNO3 and NaSCN have no effect on KGM gelation even at higher salt concentration (4 mol.L−1) and high temperatures Other salts as Na2CO3 induced the formation of thermoreversible gels by deacetylation and salting-out Carbohydrate Polymers 223 (2019) 115083 C.N Sakakibara, et al Friedrich, & Thomann, 2009) For example, Paţachial et al (2009) observed an increase in the storage modulus (G’) when adding a kosmotropic salt, Na2SO4, to poly(vinyl alcohol), evidencing a higher crosslinking density due to an increase in the polymer-polymer interaction Based on that, was proposed here the formation of gels combining the anions from Hofmeister series and XG, a non-ionic polysaccharide and presenting, very rarely, hydrophobic sites as published by Freitas et al (2015) The XG, differently of HPMC and KGM, is a non-gelling polysaccharide, and the effect of anions SO42−, HPO42−, H2PO4− Cl− and NO3−, maintaining the same cation will be studied Also, the ability of SO42− to induce both gelation and conformational transition on XG will be investigated Our goal is to demonstrate the formation of thermo-responsible hydrogels defined as a hydrogel that responds to temperature (IUPAC, 2006), induced by hydrophobic interactions sites naturally occurring in the XG from Hymenaea courbaril seeds In order to so, the classic Hofmeister series was compared through of the selection of kosmotropic to chaotropic salts possessing various anions The gelation process was investigated using dynamic oscillatory rheology, microscopy and CD spectroscopy Material and methods 2.1 Purification of xyloglucan Hymenaea courbaril seeds were obtained from the “Native Forests” Project Itatinga, São Paulo state, Brazil The xyloglucan (XG) was extracted as previously described by Freitas et al (2015) The polysaccharide was purified by dispersion at C = wt% in ultrapure (Millipore) water by stirring for 48 h, and the dispersion was subsequently centrifuged at 104g for 30 at 40 °C The polysaccharide in the supernatant was precipitated by adding volumes of ethanol, washed with pure ethanol and with acetone The purified XG was dried overnight at 40 °C using a vacuum oven (Vacuoterm 6030A) Fig Frequency dependence of the shear moduli G’ and G” for wt% XG after heating during 16 h at 50 °C with different Na2SO4 concentrations (no salt up to 1.00 mol.L−1) 2.2 Size exclusion chromatography (SEC) effect (Yin et al., 2008) Sol-gel transition of thermoreversible hydroxypropylmethylcellulose (HPMC) was evaluated by Almeida, Rakesh, and Zhao (2014) The authors observed that HPMC sol-gel temperature decreased in presence of NaCl and CaCl2 The gelation temperature depended directly of the salt (NaCl, KCl and CaCl2) concentration, independent of the cation valence or anion concentration (Almeida, Rakesh, & Zhao, 2014) According to Almeida et al (2014b) the bound water contents in HPMC increased directly with salt concentration, and the behavior of the water with salt is different at gelation temperature and at low temperatures However, further experiments are necessary, according to the authors, to provide insight on the structural changes of the HPMC solution with salts (Almeida et al., 2014b) In opposition, Liu, Joshi and Lam (2008) assumed NaCl, KCl and CaCl2 disrupted the water cage around HPMC groups inducing hydrophobic association, and weakened intermolecular hydrogen bonding between hydroxyl and water The studies of salt effect on gelling polysaccharides is well described, however only few studies have been reported concerning the thermal gelation of neutral and non-gelling polymers induced by salts (Curley, Hayesa, Rowana, & Kennedy, 2014; Paţachial, Florea, The mass-average molar mass (Mw) of native XG was determined using size exclusion chromatography with a Viscotek GPC system (Malvern, USA), composed of a VE1122 pump, a VE3580 differential refractometer and a 270 dual light scattering detector with a low angle photo-detector at 7° and a right angle photo-detector at 90° The samples were injected into the system, and elution proceeded through a SB806 M HQ column (Shodex, Japan) Analyses were performed using sodium nitrate (NaNO3) 0.1 mol.L−1 with 200 ppm of sodium azide (NaN3) at pH as the mobile phase with a flow rate of 0.4 ml.min−1 The measured value was Mw = 2.6 × 106 g.mol−1, in agreement with what was previously reported by Sakakibara et al (2017) 2.3 Preparation of the xyloglucan-salt dispersion The sample of XG was dispersed at C = wt% in ultrapure water with 200 ppm of sodium azide (NaN3) by overnight stirring Sodium sulfate was then added to the dispersion at concentrations of 0.1, 0.25, 0.5, 0.65, 0.75 and 1.0 mol.L−1, and the mixtures were stirred overnight under refrigeration prior to the investigation Carbohydrate Polymers 223 (2019) 115083 C.N Sakakibara, et al Fig G’ (1) and G” (2) as a function of pulsation for XG at wt% with 0.1 mol.L−1 (A); 0.5 mol.L−1 (B) and mol.L−1 (C) Na2SO4 at various temperatures between 50 °C and 10 °C The samples were kept at each temperature during 1.5 h after measurement 2.4 Rheological measurements the linear response regime (σ = Pa), and the oscillatory shear measurements were carried out at temperatures from 10 to 50 °C The sample dispersion was poured onto the instrument plate at 10 °C and heated to 50 °C, at which it remained for 16 h To avoid evaporation, the sample was covered with a layer of mineral oil The gelation time (tg), was determined at the intersection between G’ and G” Dynamic mechanical measurements of the XG-salt dispersion samples were performed using a Thermo Scientific HAAKE Rheostress system (Karlsruhe, Germany) equipped with a cone geometry (35 mm diameter, 2°) The shear modulus G’ and G” were measured at an angular frequency (ω) of rad.s−1 The imposed stress was chosen within Carbohydrate Polymers 223 (2019) 115083 C.N Sakakibara, et al 2.7 Circular dichroism The CD spectra were obtained with a Jasco J-815 spectropolarimeter (Jasco Instruments, Japan) The spectral scanning was from 195 to 250 nm, with a scanning speed of 20 nm.min−1 and two accumulations All the samples were maintained under nitrogen flow during the experiments The samples were used at 0.1 wt% with or without Na2SO4, the temperature ranging from 10 to 50 °C, with a heating rate of °C.min−1 Results and discussion 3.1 Influence of sodium sulfate on the XG gelation Increasing the Na2SO4 concentration (Fig 1A–D) caused a reduction in the tg value (Fig 1E) and an increase of G' at steady state after gelation This indicates that the higher the concentration of the kosmotropic salt, the stronger the hydrophobic interactions between the chains, leading to the formation of a denser polymer network from the point of view of their cross-links However, a limit value for Na2SO4 is needed in order to achieve such a gelation, as discussed below After heating the sample at 50 °C during 16 h within the rheometer, frequency sweeps were performed in order to measure G’ and G” at steady state with various concentrations of Na2SO4 (Fig 2) Gel formation was assessed, since G’ was much higher than G” and displayed no frequency dependence if the Na2SO4 concentration was higher than 0.5 mol.L−1 At lower salt concentrations, there was no influence of salt as compared to the solution of XG in plain water Subsequently, the samples remained at 50 °C, G' and G” values at rad s−1 were measured at different temperatures during cooling from 50 °C to 10 °C The concentrations of 0.1 mol.L−1 (Fig 3A) and 0.25 mol.L−1 (Fig 2) of Na2SO4 showed no significant effects on XG during heating at 50 °C These salt concentrations were clearly not enough to improve the interaction between XG chains For the samples with low salt concentrations, the values of G’ and G” decreased with temperature, suggesting that hydrogen bonds were broken Similar results were found by Freitas et al (2015) studying XG under heating and the authors described that the transient network in XG could be associated with hydrogen bond interactions The sample of XG with Na2SO4 at 0.5 mol.L−1 (Fig 3B) exhibited thermoreversible gel characteristics at 10 °C Thermoreversible gel was used here, according to IUPAC, as a swollen network with thermally reversible junction points (IUPAC, 2006) The same was observed for XG with Na2SO4 at 0.65 mol.L−1−1 and 0.75 mol.L−1 (data not shown) For Na2SO4 at mol.L−1 no thermo-reversion was observed (Fig 3C) The general rheological behavior of XG with kosmotropic salt is associated with hydrophobic interactions induced by heating (Sakakibara et al., 2017), together with weakening the hydrogen bonds of the XG The gelation of XG with other salts was achieved for purposes of comparison (Fig 4), the kosmotropic anions SO42− and HPO42− exhibiting a stronger influence on G’ It should be noted that H2PO4− (pKa 6.8) is much more chaotropic than Cl−, and theoretically cannot induce gel formation However, since the pH of the XG solution was 6.8, approximately 50% of H2PO4− was in equilibrium with HPO42−, presenting an intermediate kosmotropic behavior The chaotropic anions Cl− and NO3− had no influence on the shear modulus of XG in comparison with XG in purified water Fig Influence of Na2SO4, Na2HPO4, NaH2PO4, NaCl and NaNO3 at mol.L−1 on the shear moduli for XG at wt% after heating at 50 °C during 16 h 2.5 Confocal laser scanning microscopy analysis (CLSM) The images were obtained with a Nikon A1RSiMP confocal microscope (Tokyo, Japan), using lenses immersed in oil (20x, 60x with numerical apertures of 0.75 and 1.4 respectively and 60x with zoom of 4x) The Nis Elements 4.20 imaging program (Nikon, Tokyo, Japan) was used for visualizing the images XG was labeled with rhodamine B isothiocyanate (RITC) The XG-rhodamine was prepared using the method of De-Belder and Granath (1973) Briefly, 50 mg of XG was dispersed in 10 ml of DMSO, where drops of pyridine were added To this dispersion, mg of RITC and 20 mg of the catalyst dibutyltin dilaurate were added, and the mixture was heated at 95 °C during h The sample was precipitated and washed several times using ethanol and acetone, after which it was dried at 35 °C in a vacuum oven This XG-RITC was used at 10% of the total XG concentration for CLSM experiments 2.6 Scanning electron microscopy (SEM) The samples were maintained at 50 °C during 16 h, after which the gels were frozen using liquid N2 and immediately lyophilized The samples were placed in a double-faced copper tape and metalized with gold The SEM analyses were performed with a TESCAN VEGA3 LMU with magnification of 5kx, 20kx and 50 kx 3.2 Analysis of the structure of the gels using microscopy XG was labeled with isothiocyanate of rhodamine (RITC) forming Carbohydrate Polymers 223 (2019) 115083 C.N Sakakibara, et al Fig CLSM images of wt% XG-RITC heated during 16 h in presence of Na2SO4 at no salt (0 mol.L−1), 0.5 mol.L−1, 0.75 mol.L−1 and 1.0 mol.L−1, at different temperatures and magnification of 240x (50 x 50 μm) Excitation at 570 nm and emission at 595 nm the XG-RITC, and CLSM analysis was performed in order to observe the structure of the gel at various temperatures and Na2SO4 concentrations using images of 50 x 50 μm (Fig 5) and 200 x 200 μm (Fig S1) The red emission at 595 nm was associated to the presence of XG-RITC The results were compared with those of a solution of XG-RITC in pure water (Fig 5) of XG wt% and no Na2SO4 at 20 °C The labeling of XG with RITC has no effect on the rheological properties compared to XG and, consequently, the CLSM images were considered representative of the XG gelling behavior The CLSM images at Fig demonstrated the formation of a network at 20, 40 and 50 °C after heating at 16 h in presence of Na2SO4 At higher concentrations of Na2SO4, a clear formation of large polymeric clusters of aggregates associate and percolate all the system Only few aggregates of XG-RITC at concentration of wt% were observed in pure water (no Na2SO4) As temperature induced the formation the gelled network we expected it is associated to hydrophobic interactions Gelation kinetic studies using CLSM were obtained heating the XGRITC samples at 50 °C during 0, 1, 4, 10 and 24 h and immediately analyzed using CLSM were also performed using wt% XG with 0.5 and mol.L−1 Na2SO4 (Fig 6) Prior to analysis, the samples were prepared at °C and kept at °C until the experiments were carried out The simple addition of an amount of salt of mol.L−1 was significant Carbohydrate Polymers 223 (2019) 115083 C.N Sakakibara, et al Fig CSLM images of XG-RITC samples at wt% and with 0.5 mol.L−1 and mol.L−1 Na2SO4 concentration The images were obtained after heating at 50 °C the samples from to 24 h The magnification was of 60x (200 x 200 μm) enough to cause a greater interaction between the XG chains and the formation of large fibers, which were not observed in the native XG or at lower salt concentration at the same time/temperature as previously presented at Figs 5, and S1 Experiments were also performed using freeze-dried gels, analyzed using scanning electron microscopy (Fig 7) for the XG without salt (Fig 7A) and with 0.5 (Fig 7B), 0.75 (Fig 7C) and 1.0 mol.L−1 (Fig 7D) of Na2SO4 The presence of the salt induced the formation of fibrillar structures, which were also observed using CLSM (Figs 5, and S1), and sub-micrometer particles of XG aggregated are clearly seen at 1.0 mol.L−1 (Fig S2) The energy-dispersive X-ray spectroscopy (EDS) analysis was also performed in order to observe the distribution of SO42− ions in the gel structure as presented in Fig S3 The anions were homogeneously distributed in the same regions as carbon and oxygen of the polymer, suggesting a co-presence of polysaccharide and kosmotropic anions However, at that time, the authors can not confirm the helical/twistedlike structure transitions by the rheological experiments Gaillard, Thompson, and Morak (1969) classified tamarind XG as an amyloid molecule, and the helical/twisted molecule was associated with the interaction with iodine ions Related to XG from H courbaril seeds the conformation transition was macroscopically observed by Gouvêa, Ribeiro, de Souza, Marvila-Oliveira, and Sierakowski (2009) The authors visualize that XG in presence of starch and tetraborate ions present a deep blue color, similar to that of amylose, however only observed only in presence of XG and after shearing and heating This could indicate an amyloid structure in H courbaril XG and possibly a helical/twisted-like structure Jó, Petri, Beltramini, Lucyszyn, and Sierakowski (2010) studied the influence of temperature on XG from the conformation of Tamarind seeds using CD spectroscopy with phosphate buffer as solvent They observed the presence of a helical-like structure at lower temperatures, with a transition to a sheet-like or extended conformation at temperatures of 25 °C and 37 °C, respectively These results are in agreement with those of the present study, despite the different XG source used Umemura and Yuguchi (2005) using molecular dynamic simulation observed a XG folding mechanism dependent of the main chain condition For a flat ribbon-like conformation, the galactoxylose side chain interacts (stick) onto the flat surface by hydrophobic interactions, increasing the hydrophobicity When the XG chain is not restricted it presents a twisted conformation, loosing the folding of galactose, increasing the hydrophilicity In our opinion, the transition from a nonrestricted (twisted/helical-conformation) to a restricted (flat/expanded conformation), with exposure of hydrophobic sites is induced by temperature and SO42− concentration However much more attention need be done to confirm such hypothesis Koziol, Cybulska, Pieczywek, and Zdunek (2015) described, using atomic force microscopy, that a rod-like nanomolecules of XG was identified in a helical structure, corroborating with this twisted conformation of XG 3.3 Conformational transition of XG due to kosmotropic salts The CD analyses of 0.1 wt%, in the XG diluted regime according to Freitas et al (2015), at 0.5 and 1.0 mol.L−1 of Na2SO4 (Fig 8B and C) were compared with that of XG without salt (Fig 8A) The XG presented a transition from a twisted/helical structure at temperatures up to 40 °C with a maximum at 198 nm and minimum at 208 and 220 nm When the heating was greater than 40 °C, a more extended/flat conformation/ with maximum at 202 nm and minimum at 220 nm was observed The addition of kosmotropic salts also affected the conformational transition of XG, represented by a shift to a lower wavelength, indicating that at 0.5 mol.L−1 of Na2SO4, the twisted structure changed to an extended conformation (Fig 8B) In the presence of 1.0 mol.L−1 of Na2SO4 the same extended/flat conformation was observed with a significant shift of the CD signal to positive values, indicating almost complete loss of the helical structure with higher temperature and in the presence of Na2SO4 (Fig 8C) Increasing the temperature induced a conformational transition in the aqueous XG solution These results are, at some point, in agreement with previous results obtained by Freitas et al (2015), which indicated a quasi-permanent network in XG after the heating of this polymer, which was associated with the “exposure” of these hydrophobic groups Conclusion Kosmotropic salts are able to induce the formation of a gelled network in XG, induced by very sensitive hydrophobic domains naturally occurring in this polysaccharide We confirmed our hypothesis that the Carbohydrate Polymers 223 (2019) 115083 C.N Sakakibara, et al Fig Micrographs obtained using scanning electron microscopic of dried colloidal dispersions of XG at wt% in water/ no salt (A) and with 0.5 mol.L−1 Na2SO4 (B); 0.75 mol.L−1 Na2SO4 (C) and mol.L−1 Na2SO4 (D) using magnifications of 5kx and 20kx hydrophobic domains are sensitive to temperature and to salts due to a competition for water Another important consideration is that XG displayed a conformational transition from a helical structure to a more extended conformation during heating, sensitive to the presence of salt This induced the formation of sub-micrometric particles of XG responsible for the formation of gelling structures Acknowledgements We acknowledge the Brazilian funding agencies CNPq (Conselho Nacional de Pesquisa, process number 430451/2018-0) and CAPES (Coordenaỗóo de Aperfeiỗoamento de Pessoal de Nớvel Superior – Brasil – Finance Code 001) and CAPES/PrInt (88887.311748/2018-00) Carbohydrate Polymers 223 (2019) 115083 C.N Sakakibara, et al Fig CD spectra of 0.1 wt% XG in no salt (A), 0.5 mol.L−1 (B) and 1.0 mol.L−1 (C) Na2SO4 analyzed at different temperatures R.A.F (CNPq 301172/2016-1), M.-R.S (CNPq 306245/2014-0) and I.R.V (CNPq 306038/2017-0) are CNPq 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