Article pubs.acs.org/Langmuir
Multidimensional Self-Assembled Structures of Alkylated Cellulose Oligomers Synthesized via in Vitro Enzymatic Reactions Yusuke Yataka,† Toshiki Sawada,‡ and Takeshi Serizawa*,‡ †
Department of Organic and Polymeric Materials, Graduate School of Science and Engineering, Tokyo Institute of Technology, 2-12-1 Ookayama, Meguro-ku, Tokyo 152-8550, Japan ‡ Department of Chemical Science and Engineering, School of Materials and Chemical Technology, Tokyo Institute of Technology, 2-12-1 Ookayama, Meguro-ku, Tokyo 152-8550, Japan S Supporting Information *
ABSTRACT: The self-assembly of biomolecules into highly ordered nano-to-macroscale structures is essential in the construction of biological tissues and organs. A variety of biomolecular assemblies composed of nucleic acids, peptides, and lipids have been used as molecular building units for selfassembled materials. However, crystalline polysaccharides have rarely been utilized in self-assembled materials. In this study, we describe multidimensional self-assembled structures of alkylated cellulose oligomers synthesized via in vitro enzymatic reactions. We found that the alkyl chain length drastically affected the assembled morphologies and allomorphs of cellulose moieties. The modulation of the intermolecular interactions of cellulose oligomers by alkyl substituents was highly effective at controlling their assembly into multidimensional structures. This study proposes a new potential of crystalline oligosaccharides for structural components of molecular assemblies with controlled morphologies and crystal structures.
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INTRODUCTION The self-assembly of biomolecules into highly ordered nano-tomacroscale structures on the basis of intra- and intermolecular interactions is essential in the construction of biological tissues and organs. Biomolecular assemblies have drawn attention as the driving force for producing artificial soft materials through low-energy processes under aqueous conditions.1−3 In fact, certain biomolecules such as hybridized DNA strands,4,5 α-helix bundles, and β-sheets of peptides6−8 as well as lipid bilayers9−11 have been used as structural components of self-assembled materials. However, representative biological assemblies composed of crystalline polysaccharides (e.g., cellulose and chitin) have rarely been investigated as components of regularly structured molecular assemblies,12,13 possibly because their precise organic synthesis, solubilization in ordinary solvents, and control of crystal structures are difficult. Nevertheless, crystalline polysaccharides have unique physicochemical and functional properties, such as chemical/thermal stability, mechanical stiffness, and biocompatibility.14−16 Therefore, the incorporation of crystalline polysaccharide units into molecular assemblies in a designable and controllable manner has the potential to lead to a new field of soft materials. In vitro enzymatic synthesis is a biomimetic and promising approach to produce synthetic/biological polymers and their assemblies in a single step under mild aqueous-based conditions.17−19 Cellulose oligomers have successfully been synthesized by cellulase or cellodextrin phosphorylase (CDP) © 2016 American Chemical Society
from adequate monomers without any protection/deprotection processes, which are essential for their organic synthesis.20−23 In most cases (except for one unusual example24), the synthesized cellulose oligomers form an antiparallel cellulose II allomorph, which is thermodynamically more stable than the parallel cellulose I allomorph composed of naturally driven cellulose. For example, when α-D-glucose 1-phosphate (αG1P) monomers are oligomerized from D-glucose primers by CDP in a buffer solution, cellulose oligomers with an average degree of polymerization (DP) of 9−10 self-assemble into unique rectangular crystalline nanosheets, in which the cellulose oligomers align perpendicularly to the base plane and pack in an antiparallel manner.23 It has been revealed that not only D-glucose but also β-Dglucose derivatives with anomeric substituents are recognized by CDP (from Clostridium thermocellum) as primers for enzymatic cellulose synthesis because of the poor substrate specificity of the CDP.21,25−27 Therefore, the CDP-catalyzed reaction has the potential to synthesize cellulose oligomer derivatives with designed substituents at the reducing end. In addition, the appropriate substitution of cellulose oligomers may modulate their intermolecular interactions for assembly processes. In this study, we describe multidimensional selfReceived: July 19, 2016 Revised: September 6, 2016 Published: September 8, 2016 10120
DOI: 10.1021/acs.langmuir.6b02679 Langmuir 2016, 32, 10120−10125
Article
Langmuir assembled structures of alkyl β-cellulosides synthesized via CDP-catalyzed oligomerization of αG1P monomers against alkyl β-D-glucoside primers with different alkyl chain lengths (Figure 1a). Depending on the alkyl chain length, unique
pH 7.5) containing 0.02% sodium azide. The enzymatic activity was determined by quantifying the amount of inorganic phosphate produced from 10 mM αG1P in the presence of 10 mM cellobiose in MOPS-sodium buffer (50 mM, pH 7.5) at 37 °C. One unit of activity was defined as the amount of enzyme that produced 1 μmol of inorganic phosphate per minute from αG1P at 37 °C, as previously described.23 CDP-Catalyzed Synthesis of Alkyl β-Cellulosides. Alkyl βcellulosides were synthesized using CDP according to previously reported methods.26−28 Purified CDP (0.2 U mL−1) was incubated with αG1P (200 mM) as a monomer and ethyl, butyl, hexyl, or octyl β-D-glucoside (50 mM) as a primer in 4-(2-hydroxyethyl)-1piperazineethanesulfonic acid (HEPES) buffer (500 mM, pH 7.5) for 3 days at 60 °C. The water-insoluble products were washed with ultrapure water in centrifugation/redispersion cycles (15 000 rpm in a TOMY MX-301 and MX-305) that were performed more than five times. When the reaction solution gelled, the products were lyophilized and then washed in the same manner for spectroscopic characterization. The water dispersions of the products were heated to 100 °C for 10 min to inactivate residual CDP. The resultant products were stored at 4 °C until use. 1 H Nuclear Magnetic Resonance (NMR) Spectroscopy. The solvents of the products were exchanged from ultrapure water to deuterated water through three centrifugation/redispersion cycles (15 000 rpm in a TOMY MX-301 and MX-305). The dispersion volume was adjusted to 405 μL; then, 45 μL of 40% NaOD/D2O was added to dissolve the disperse materials. The 1H NMR spectra of the product solutions (3% (w/v)) were recorded on a Bruker DPX-300 spectrometer operated at 300 MHz. The chemical shifts were recorded relative to the residual H2O (δ 4.79). The average DP was calculated using the following equation DP
Figure 1. (a) Reaction scheme for the CDP-catalyzed synthesis of alkyl β-cellulosides and (b) a schematic illustration of the selfassembled structures of the alkyl β-cellulosides with different alkyl chain lengths.
∑i = b Hi
where Nalkyl represented the number of protons in alkyl groups in the alkyl β-celluloside. Attenuated Total Reflection-Fourier Transform Infrared (ATR-FTIR) Absorption Spectroscopy. The water-dispersions of the products were lyophilized for 1 day. The ATR-FTIR absorption spectra of the lyophilized products were obtained with the cumulative number of 100 under ambient conditions using wavelengths between 350 and 7800 cm−1 with a resolution of 2.0 cm−1 on a JASCO FT/IR4100 spectrometer. X-Ray Diffraction (XRD) Measurements. The water dispersions of the products were lyophilized for 1 day. The XRD measurements of the resulting powders were performed under ambient conditions using a Rigaku MiniFlex with Cu Kα radiation (λ = 0.154 nm). Matrix-Assisted Laser Desorption/Ionization Time-of-FlightMass Spectra (MALDI-TOF-MS) Measurements. Mixed suspensions of 0.033% (w/v) products and 1.66 mg mL−1 DHBA in 50% acetonitrile/0.1% (v/v) trifluoroacetic acid (1 μL) were spotted on an AXIMA 384-well, 2 mm thick sample plate 1 time or 10 times. The MALDI-TOF-MS were recorded on a Shimadzu AXIMA-performance mass spectrometer with a nitrogen laser (λ = 337 nm) and pulsed ion extraction, which was operated at an accelerating potential of 20 kV with a linear-positive ion mode. The spectra were calibrated externally using standard samples with molecular weights of 757.4, 1533.9, and 2465.2 Da. Scanning Electron Microscopy (SEM). The solvent of the gel samples was gradually exchanged from ultrapure water to tert-butyl alcohol by immersing in 10, 20, 30, 40, 50, 60, 70, 80, 90, and 99.5% ethanol, 99.5% ethanol/tert-butyl alcohol, and 99% tert-butyl alcohol. The gel samples were frozen in liquid nitrogen, immediately fractured by using a razor blade, and then lyophilized. The resultant gel pieces were mounted on a specimen mount with a carbon conductive tape and coated with osmium using a Meiwafosis Neoc-Pro at 10 mA for 12 s. The SEM images were taken with a JEOL JSM-7500F operated at 5 kV and a working distance of 7.9 to 8.1 nm.
morphologies, such as nanoribbons, helical nanorods, and distorted nanosheets, were observed, and the crystal structures of the cellulose moieties were varied (cellulose I vs II allomorphs) (Figure 1b). It was found that the incorporation of crystalline oligosaccharide units into molecular assemblies potentially controlled their morphologies and crystal structures.
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(Nalkyl − 2)(H1 + H1′ + H1″)
EXPERIMENTAL SECTION
Materials. αG1P disodium salt n-hydrate and 40% NaOD/D2O were purchased from Wako Pure Chemical Industries. Ethyl, butyl, and hexyl β-D-glucoside were purchased from Carbosynth Limited. Octyl β-D-glucoside was purchased from Dojindo Laboratories. EM stainer and a carbon conductive tape were purchased from Nissin EM Corporation. A collodion-coated copper EM grid with 200 meshes was purchased from EMJapan Corporation. ProteoMass Peptide & Protein MALDI-MS Calibration Kit, 2,5-dihydroxybenzoic acid (DHBA), and D2O were purchased from Sigma-Aldrich. All other reagents were purchased from Nacalai Tesque. Ultrapure water (>18.2 MΩ·cm) was supplied by a Milli-Q system (Merck Millipore) and was used throughout all the experiments. Preparation and Activity Assay of CDP. The preparation and purification of CDP from Clostridium thermocellum YM4 and the determination of its enzymatic activity were performed according to an established method.23 CDP was prepared using an Escherichia coli BL21-Gold (DE3) strain containing a plasmid including the cdp gene and was purified by a Ni-NTA column (GE Healthcare) using its fused His-tag. Then, the buffer of the CDP solution was exchanged to 3morpholinopropane-1-sulfonic acid (MOPS)-sodium buffer (20 mM, 10121
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solvent (Figure 3a). The 1H signals between 3.0 and 4.5 ppm and 0.5−1.5 ppm were assignable to the cellulose moieties30,31
Transmission Electron Microscopy (TEM). A glow-discharged collodion-coated copper EM grid was prepared using a Hitachi E-1010 ion sputterer. A nontreated grid was placed on a droplet of 0.2% (w/v) ethyl and butyl β-celluloside dispersions for 1 h, while the glowdischarged grid was placed under a droplet of 0.2% (w/v) hexyl and octyl β-celluloside dispersions for 1 h. The samples were stained using an undiluted EM stainer for 30 min. The prepared grid was dried in a desiccator for at least 12 h. The TEM images were taken with a Hitachi H-7650 Zero A microscope operated at 100 kV. Atomic Force Microscopy (AFM). A droplet of the product dispersion in ultrapure water was mounted on a mica substrate and then dried in a desiccator for at least 12 h. The AFM images were taken with a Shimadzu SPM-9600 in the tapping mode in air at ambient temperature using an aluminum reflex-coating cantilever. Critical Micelle Concentration (CMC) Measurements. A pyrene solution dissolved in methanol (5 μL) and an alkyl β-Dglucoside primer solution dissolved in HEPES buffer (500 mM, pH 7.5) with αG1P (300 μL) were mixed to produce a final concentration of 500 nM pyrene, 5−500 mM primer, and 200 mM αG1P in HEPES buffer (500 mM, pH 7.5). After incubation for 5 min at 25 °C, a fluorescent spectrum of the solution was recorded on a JASCO FP6500. The measurements were conducted by excitation at 334 nm. All measurements were performed at 25 °C in a wavelength range between 360 and 420 nm with a resolution of 0.2 nm, an excitation slit of 5 nm, and an emission slit of 3 nm. The ratio of the emission intensities (I1/I3), which is dependent on the solvent environment, was calculated using a peak intensity of 373 and 384 nm as I1 and I3, respectively.29
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RESULTS AND DISCUSSION CDP-Catalyzed Synthesis of Alkylated Cellulose Oligomers. The enzymatic synthesis of alkyl β-cellulosides was performed according to our previous reports.26−28 In brief, monomers (200 mM) and primers (50 mM) were incubated with CDP (0.2 U mL−1) in a HEPES buffer solution (500 mM, pH 7.5) at 60 °C for 3 days. Then, the products were adequately purified and characterized. After the reactions, colorless products were observed in all cases (Figure 2), thus
Figure 3. (a) NMR spectra and (b) MALDI-TOF-MS of the products obtained by alkyl β-D-glucoside primers with different alkyl chain lengths (m = 2, 4, 6, and 8).
and alkyl groups, thus suggesting the successful production of alkyl β-cellulosides. The average DP values for the cellulose moieties were estimated to be approximately 8, 8, 7, and 7 for the primers with m = 2, 4, 6, and 8, respectively, on the basis of the ratios of the 1H signals for the anomeric positions and alkyl groups, thereby indicating that the DP values tended to decrease with increasing alkyl chain length. Because the longer alkyl chains should promote self-assembly because of greater hydrophobic interactions, products with smaller DP values tended to be obtained from primers with greater alkyl chain lengths. In fact, the DP values were smaller than those for pure cellulose oligomers obtained by using D-glucose primers under the same reaction conditions.28 Furthermore, MALDI-TOFMS of the products further supported the production of alkyl βcellulosides with a certain degree of DP distribution (Figure 3b). The peak-to-peak mass differences were estimated to be 162 Da, a value consistent with that of a single glucosyl repeating unit. The DP values obtained by MALDI-TOF-MS were comparable to those obtained by 1H NMR spectra. Notably, the conversion ratios of the monomers to waterinsoluble products were estimated to be 60−70% on the basis of the average DP values obtained from the 1H NMR spectra and were independent of the primers. Morphological and Crystal Structural Characterization of Hydrogels for Ethyl and Butyl β-Cellulosides. Interestingly, SEM observations revealed that the hydrogels
Figure 2. Photos of the reaction solutions of the products obtained by alkyl β-D-glucoside primers with different alkyl chain lengths (m = 2, 4, 6, and 8).
suggesting that αG1P monomers were oligomerized from all primers for the production of water-insoluble cellulose derivatives. Hence, primers with different alkyl chain lengths were recognized by CDP as substrates. The reaction solutions obtained from primers with relatively smaller alkyl chain lengths (m = 2 and 4) transformed into hydrogels, thereby indicating the formation of 3D network structures. In contrast, those obtained from primers with greater lengths (m = 6 and 8) became dispersions, thereby indicating the formation of aggregates. Hence, the introduction of alkyl chains to β-Dglucose primers at their anomeric positions drastically modulated the solution states after the enzymatic reactions. Molecular-Level Characterization of Alkylated Cellulose Oligomers. The chemical structures of the products were analyzed through 1H NMR spectra with a 4% NaOD/D2O 10122
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Langmuir obtained by using the primers with m = 2 and 4 were made of extremely well-grown 1D nanoribbons with submicrometer widths (Figure 4). Branched objects were not observed in the
were representative of stretching vibration bands of the OH groups in the cellulose II allomorph (Figure 5b).32 Therefore, the alkyl β-cellulosides with smaller alkyl chain lengths (m = 2 and 4) may have assembled into nanoribbons with monolayer structures packed in an antiparallel manner, as illustrated in Figure 1b. The nanoscale structures of the nanoribbons were similar to those of the rectangular nanosheets of pure cellulose oligomers obtained by CDP-catalyzed synthesis with D-glucose primers.28 This result suggested that the nanosheets grew into nanoribbons without aggregation, similarly with oligo(ethylene glycol)bearing cellulose oligomers synthesized via the same enzymatic reaction.22 However, it is difficult to reasonably explain the reason why the alkyl β-cellulosides with smaller alkyl chain lengths grew into nanoribbons even though those molecules have hydrophobic alkyl groups, which may promote aggregation because of hydrophobic interactions with aqueous reaction solutions. Because the conversion ratios for the aforementioned primers were much greater than those for the D-glucose primers (approximately 35%),28 the generation of more precursors in the reaction solutions and the subsequent provision of products might promote growth into nanoribbons rather than aggregation of nanosheets. Morphological and Crystal Structural Characterization of Dispersions for Hexyl and Octyl β-Cellulosides. Next, the dispersions obtained by the primers with m = 6 and 8 were analyzed microscopically and spectroscopically. TEM observations revealed that the dispersion obtained by the primer with m = 6 predominantly contained 1D left-handed helical nanorods with lengths of less than several micrometers and a periodical pitch of 290 ± 50 nm (Figure 6a and Figure S2 in the Supporting Information). The AFM observations estimated the thickness of the nanorods to be 9.8 ± 0.5 nm (Figure 6a), a value comparable to twice the length of hexyl βcelloheptaose (Figure S1c in the Supporting Information). The XRD measurements revealed three diffraction peaks for a d spacing of 0.60, 0.54, and 0.40 nm (Figure 7a), which were
Figure 4. SEM images of the xerogels (top) and AFM images of the mechanically crushed products (bottom) for (a) ethyl (m = 2) and (b) butyl (m = 4) β-cellulosides. The insets of SEM and AFM images are magnified and cross-sectional images, respectively.
SEM images; therefore, it was suggested that hydrogels were produced by the physical entanglement of nanoribbons. AFM observations of mechanically crushed products with different alkyl chain lengths (m = 2 and 4) revealed nanoribbon thicknesses of 5.4 ± 0.2 and 5.4 ± 0.4 nm, respectively (Figure 4). The thicknesses were comparable to the molecular lengths of ethyl and butyl β-cellooctaoses (Figure S1a,b in the Supporting Information), thus suggesting the possibility that these molecules were aligned perpendicularly to the base plane of the nanoribbons. Furthermore, the XRD measurements revealed three diffraction peaks for a d spacing of 0.72, 0.45, and 0.40 nm (Figure 5a), which were assigned to 11̅0, 110, and 020 for the antiparallel cellulose II allomorph, respectively.23 Other detectable peaks were not observed in the spectra, thus suggesting that the alkyl chain moieties were in amorphous states. In addition, the ATR-FTIR absorption spectra revealed two sharp peaks at approximately 3440 and 3490 cm−1, which
Figure 6. TEM (top) and AFM (bottom) images of the products for (a) hexyl (m = 6) and (b) octyl (m = 8) β-cellulosides. The insets of TEM and AFM images are magnified and cross-sectional images, respectively.
Figure 5. (a) XRD patterns and (b) ATR-FTIR absorption spectra of the products for ethyl (m = 2) and butyl (m = 4) β-cellulosides. 10123
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that the micelle formation of the primers was not essential for the formation of the cellulose I allomorph. Even though the concentrations of αG1P monomers, the primers, and CDP were changed for the enzymatic reactions, the allomorphs of the products for hexyl (m = 6) and octyl (m = 8) β-cellulosides were not changed (Figure S4 in the Supporting Information). Therefore, the cellulose I allomorph tended to be produced on the basis of the total balance of intermolecular interactions among the products. In other words, the modulation of the intermolecular interactions between the cellulose oligomers through the substitution of alkyl groups at the reducing ends should be an attractive route to allow control of their allomorphs.
Figure 7. (a) XRD patterns and (b) ATR-FTIR absorption spectra of the products for hexyl (m = 6) and octyl (m = 8) β-cellulosides.
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CONCLUSIONS Multidimensional self-assembled structures of alkyl β-cellulosides synthesized via the CDP-catalyzed oligomerization of αG1P monomers against alkyl β-D-glucoside primers with different alkyl chain lengths were systematically investigated. The alkyl chain length drastically affected the assembled morphologies of the products and the crystal structures of the cellulose moieties. Hydrogels composed of extremely wellgrown nanoribbons with the cellulose II allomorph were obtained by using primers with relatively smaller alkyl chain lengths (m = 2 and 4), whereas dispersions composed of helical nanorods or distorted nanosheets with the cellulose I allomorph were obtained by using primers with greater lengths (m = 6 and 8). This fundamental study successfully demonstrated a new potential of crystalline oligosaccharides for structural components of molecular assemblies with controlled morphologies and crystal structures. This study also demonstrated that the CDP-catalyzed synthesis of cellulose oligomers using adequate primers could produce highly ordered molecular assemblies in a single step under aqueous mild conditions. The physicochemical and functional characterizations of these unique molecular assemblies are under investigation.
assigned to 110̅ , 110, and 200 for the parallel cellulose Iβ allomorph, respectively.33 The XRD measurements also suggested that the alkyl chain moieties were in amorphous states. The ATR-FTIR absorption spectra revealed a peak at approximately 3340 cm−1, which was representative of the stretching vibration bands of the OH groups in the cellulose I allomorph (Figure 7b). 32 These observations strongly suggested that the helical nanorods were composed of cellmembrane-like bilayer structures packed in a parallel manner, as illustrated in Figure 1b. The dispersion obtained by the primer with m = 8 was composed of 2D distorted nanosheets with a thickness of 9.7 ± 0.4 nm (Figure 6b). The thickness was comparable to twice the length of octyl β-celloheptaose (Figure S1d in the Supporting Information). Furthermore, spectroscopic analyses revealed the formation of the cellulose Iβ allomorph (Figure 7). These observations suggested that the distorted nanosheets were composed of bilayer structures packed in a parallel manner, as illustrated in Figure 1b. Accordingly, the slight difference in the alkyl chain lengths of the primers (m = 6 vs 8) resulted in different morphologies with the same crystal allomorph of the cellulose moieties. In biological systems, plural cellulose molecules are synthesized in the same direction from cellulose synthase assembled in cell membranes (forming structures called terminal complexes), and this is followed by parallel packing for the cellulose I allomorph.34 Most previous studies on the enzymatic synthesis of cellulose using homogeneously soluble enzymes have produced the cellulose II allomorph, which is thermodynamically more stable than the cellulose I allomorph.18 Only one study has succeeded in producing the cellulose I allomorph by using aggregated micelle-like cellulases; however, the cellulose I allomorph was observed as a part of the products.24 Therefore, to the best of our knowledge, this study is the first demonstration of the highly efficient formation of the cellulose I allomorph in molecular assemblies by using homogeneous soluble enzymes. To speculate on the mechanism for formation of the cellulose I allomorph, micelle formation of the primers with m = 6 and 8 was investigated on the basis of the fluorescence of pyrene molecules in the presence of the primers.29 The dependence of the fluorescent intensity on the primer concentrations revealed CMCs of 198 and 18 mM, respectively (Figure S3 in the Supporting Information). The former was greater, but the latter was smaller than the primer concentration for the enzymatic reactions, thus indicating that the primer with m = 6 did not form micelles in the reaction solution, whereas that with m = 8 formed micelles. These observations suggested
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ASSOCIATED CONTENT
* Supporting Information S
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.langmuir.6b02679. Estimated molecular lengths of alkyl β-cellulosides, the low-magnification TEM image of the product for hexyl βcelluloside, CMC measurements of hexyl, and octyl β-Dglucosides, and ATR-FTIR absorption spectra of the products for hexyl and octyl β-cellulosides prepared under different conditions. (PDF)
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AUTHOR INFORMATION
Corresponding Author
*Fax: +81-3-5734-2128. 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. 10124
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ACKNOWLEDGMENTS We thank the Division of Materials Analysis Ookayama (Tokyo Tech) for the SEM/TEM observations and the WAXD measurements. This study was partially supported by the Funding Program for Next Generation World-Leading Researchers (NEXT Program), Grants-in-Aids for Scientific Research (26288056, 26620174, and 16K14075) from the Japan Society for the Promotion of Science, and collaborative research with JX Nippon Oil & Energy.
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