Hydrolysis of cellobiose to monosaccharide catalyzed by functional Lanthanum(III) metallomicelle

Abstract

A novel surfactant, 3-(dodecylimino)butan-2-one-oxime (DMBO), was synthesized. The metallomicelle La(DMBO)₂ was prepared and used as a mimic of β-glucosidase to catalyze the hydrolysis of cellobiose in weakly alkaline aqueous solution at relative low temperature (80–110 °C). This study indicated that the functional metallomicelle displayed effective catalytic activity for hydrolysis of cellobiose to monosaccharide (glucose, fructose and 1,6-anhydroglucose) and glucosyl-erythrose. The conversion of cellobiose and selectivity of monosaccharide could reach 38.5% and 71.1%, respectively, for a reaction time of 10 h at pH 9.0 and 95 °C. The possible reaction pathways of cellobiose hydrolysis are proposed and the catalysis reaction rate constant k_cat and Michaelis constant K_m for the cellobiose hydrolysis were calculated. The apparent activation energy (E_a = 84.6 kJ mol⁻¹) of cellobiose to monosaccharide was evaluated.

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1. Introduction

Cellulose, a linear macromolecule connected by β-1,4-glycosidic bonds of D-glucose units, is the most abundant organic compound in nature.^1,2 Glucose is an important platform compound to produce biofuels and chemicals such as 5-(hydroxymethyl)furfural, lactic acid and 3-hydroxyacrylic acid.^3–6 Therefore hydrolysis of cellulose into glucose is one of the bottlenecks and challenging problems in the field of utilization of biomass.^7,8 Although some researchers have reported the hydrolysis of cellulose into glucose through acid catalysts,^9–12 subcritical and supercritical water^13–16 and ionic liquid,^17–19 the problems of low activity and/or selectivity, severe reaction conditions and potential environmental pollution have not been resolved. Cellulase-catalyzed hydrolysis is an ideal process for cellulose degradation owing to the high selectivity of glucose product and the benign conditions.^20,21 However, the high cost and instability of the enzyme limit its further application.²² There are three kinds of cellulase for cellulose hydrolysis by synergistic action: β-1,4-endoglucanase (EC3.2.1.4), β-1,4-exoglucanase (EC3.2.1.91) and β-glucosidase (EC3.2.1.21).^23,24 β-Glucosidase constitutes a major group of glycoside hydrolase and hydrolyzes cellobiose to glucose efficiently.^25,26 The catalytic mechanism of β-glucosidase was believed to consist of two reaction steps involving glycosylation and deglycosylation steps.^27,28

Functional micelles, a new kind of self-assembly supramolecular system, which could not only simulate the active center but also the hydrophobic microenvironment of enzymes, have attracted much attention of biologists and chemists.^29–33 Micelles, especially metallomicelles consisting of a metal and long-chain surfactant micelle, are widely applied to catalyze reactions^34–36 and to prepare new materials.^37–39 In this paper, a novel metallomicelle, La(DMBO)₂, as a mimic of β-glucosidase, was employed to catalyze the hydrolysis of cellobiose, which is the basic structural unit and a good model of cellulose, in weakly alkaline aqueous solution at relative low temperature (80–110 °C). This metallomicelle displayed excellent catalytic activity and selectivity of monosaccharide for cellobiose hydrolysis.

2. Experimental

2.1 Materials

β-D-(+)-Cellobiose was of biological grade and purchased from J&K Corp. Company. Diacetyl monoxime (Damx), dodecylamine, La(NO₃)₃·6H₂O and methanol were of analytical grade and purchased from Kelong Chemical Company and used after certain purification. Acetonitrile was of chromatographic pure grade and purchased from Adamas Company. Whatman 42 filter paper was purchased from GE Healthcare companies.

2.2 Synthesis of 3-(dodecylimino)butan-2-one-oxime (DMBO)

Damx (2.525 g) was dissolved in 20 ml absolute methanol, and then the solution was added dropwise into 30 ml methanol solution of dodecylamine (3.70 g), then 0.4 g NaOH was added. The mixture was heated to 70 °C and refluxed for 20 h, then cooled to room temperature. The mixture solution was treated by silica gel column chromatography (2 : 3 v/v, ethyl acetate–chloroform) and a yellowish crystalline product was obtained. The yield of DMBO was 3.49 g (65%). The contents of C, H, N and O elements of DMBO were determined using an elemental analyzer (MOD 1106, Carlo Erba Company of Italy). Found: C, 71.62; H, 11.98; N, 10.39; O, 5.93%. Calc. for C₁₆H₃₂N₂O: C, 71.64; H, 11.94; N, 10.45; O, 5.97%. ¹H NMR (AM-400, Bruker of Switzerland): δ (400 MHz, CDCl₃): 11.8 (1H, s, –OH), 1.21–1.52 (22H, m, 11-CH₂); 3.15 (3H, s, –CH₃CNOH), 2.04 (3H, s, –CH₃CN–C₁₂H₂₅); 0.84 (3H, m, –CH₃C₁₁H₂₂).

2.3 Method

The initial reaction solution, containing 0.02 mol·L⁻¹ cellobiose and 0.002 mol·L⁻¹ catalyst, was heated and kept at desired temperature. Before heating, N₂ gas was passed into the solution for 30 min for the cases of reaction at temperature below 100 °C. For the cases of reaction above 100 °C, the N₂ was passed into reaction solution until the reaction was completed. Samples were extracted from the reactor periodically, and cellobiose and products in the reaction solution were analyzed and their concentrations were determined by HPLC equipped with a RI detector (Shodex 201R, Japan) and a Sugar-D chromatographic column. The pH of solution was adjusted by H₂SO₄ or NaOH. For the hydrolysis of cellulose (Whatman 42 filter paper), N₂ gas was passed into the flask continuously until the reaction was completed, and the total reducing sugar was detected by the DNS method^40,41 with a UV-5300 spectrophotometer (Yuanxi Company, China). On a carbon basis, the conversion of cellobiose X was calculated as X = (C₀ − C_t)/C₀, yield of monosaccharide Y was calculated as Y = C_1t/2C₀ and the selectivity of monosaccharide S was calculated as S = Y/X, where C₀, C_t are the concentrations of cellobiose at reaction time t = 0 and t, respectively, and C_1t is the total concentration of monosaccharide (glucose, fructose and 1,6-anhydroglucose) at time t.

3. Results and discussion

3.1 Critical micelle concentration of surfactant and Job plots

Surfactant molecules can aggregate to form micelles above the critical micelle concentration (cmc). Both the characteristics and the self-assembly supramolecular structure of a micelle are far different from its monomer.⁴² In this work the cmc of surfactant DMBO was measured with the electrical conductivity method using a conductivity meter (DDS-307, China). According to plots of electrical conductivity vs. concentrations of DMBO (Fig. S1 in the ESI†), the cmc of DMBO, which corresponds to the intersection of two straight lines, was evaluated as about 1.63 × 10⁻⁴ mol L⁻¹.

In order to determine the chelating stoichiometry of the reactive metal complex, the kinetic versions of Job plots were utilized, as shown in Fig. S2 in the ESI,† in which the conversion of cellobiose or yield of monosaccharide was plotted as a function of the mole fraction (r) of ligand or La³⁺ keeping their total concentration constant.^30,43 From Fig. S2 in the ESI† it can be seen that the r-values corresponding to the maximum conversion of cellobiose and yield of monosaccharide were all about 0.67, which suggests that the 1 : 2 complex (metal : ligand) should be the active species at pH 9.0.

3.2 Comparison of catalytic activity

Cellobiose is stable and difficult to hydrolyze in a near-neutral aqueous solution. However it can be rapidly degraded under strong acid (pH < 2) or alkali (pH > 10) conditions (Fig. S3 in the ESI†). The results of cellobiose hydrolysis catalyzed by different catalytic systems at pH 9.0, 90 °C and 10 h are listed in Table 1, from which we can see that in the absence of any catalyst only 3.7% of cellobiose could degrade under those conditions.

Table 1 Comparison of catalytic activity for various systems^a

System	Conversion of cellobiose/%	Yield of monosaccharide/%	Selectivity of monosaccharide/%
a [Cellobiose]0 = 0.02 mol L^−1, [catalyst] = 0.002 mol L^−1, pH 9.0, 90 °C, 10 h.
Bulk solution	3.7	1.9	48.6
Damx	8.9	4.6	51.7
DMBO	11.1	5.8	52.2
La(Damx)2	17.7	9.7	54.8
La(DMBO)2	29.5	17.8	60.3

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Damx containing the N–OH functional group in relatively low concentration displayed certain catalytic activity for cellobiose hydrolysis. Metal complex La(Damx)₂ clearly enhanced the reaction rate. Interestingly, when a long hydrocarbon chain was grafted onto Damx, micelles formed and showed excellent catalytic activity – probably owing to the enzyme-like microenvironmental effects.^30,31 Further, it was also found that the metallomicelle La(DMBO)₂ showed the best catalytic activity under the same conditions.

To understand the effect of the structure of the metal complex on reaction activity, several metal complexes (Fig. S4 in the ESI†) were employed as catalysts to catalyze cellobiose hydrolysis under the same conditions. These catalysts showed far lower catalytic activity than La(Damx)₂ (Table S1 in the ESI†). This indicated that the strong nucleophilic functional group N–O⁻ may play an important role in the catalysis process under weakly alkaline conditions.

3.3 Effect of pH

From Fig. 1 it can be seen that for the metallomicelle La(DMBO)₂-catalyzed system, pH has great influence on conversion of cellobiose and yield of monosaccharide. The conversion of cellobiose increased with increasing pH and reached about 100% for reaction of 10 h at pH 12 and 90 °C. However the variation of the yield of monosaccharide was complex. Initially the yield of monosaccharide increased with increasing pH and reached a maximum at pH 11.5. From Table 2 it can be seen that the main component is glucose. According to our experimental data, glucose and fructose can be rapidly degraded to smaller-molecule substances, including 5-(hydroxymethyl)furfural, laevulinic acid and methanoic acid, under strong alkali conditions (pH > 11.5).

Fig. 1 Plots of conversion of cellobiose () and yield of monosaccharide () versus pH at 90 °C for 10 h.

Table 2 Conversion of cellobiose, distribution of products and selectivity of monosaccharide at pH 9.0, 10 h

T/°C	Conversion of cellobiose/%	Yield of monosaccharide			Yield of monosaccharide/%	Yield of GE/%	Selectivity of monosaccharide/%
		Glucose/%	Fructose/%	1,6-Anhydroglucose/%
80	13.5	5.2	1.1	1.2	7.5	5.7	55.6
85	20.8	7.7	1.6	2.6	11.9	7.8	57.2
90	29.5	11.4	2.5	3.9	17.8	10.5	60.3
95	38.5	18.5	3.4	5.5	27.4	10.1	71.1
100	48.6	21.5	3.9	6.1	31.5	15.3	64.8
110	70.4	26.0	4.7	7.7	38.4	30.3	54.5

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3.4 Effect of temperature

Cellulose is stable and difficult to hydrolyze under mild conditions owing to the large activation energy of its hydrolysis reaction, so the hydrolysis reaction is usually carried out at high temperatures. However glucose can be easily decomposed to smaller-molecule substances, and therefore the selectivity of monosaccharide is generally very low at high temperatures.^15,44 In this work, cellobiose hydrolysis reaction was carried out at relatively low temperature (80–110 °C). Fig. 2 shows the effect of temperature on both conversion of cellobiose and yield of monosaccharide. Apparently, higher temperature accelerated the reaction rate of cellobiose hydrolysis. However, it can be further seen that the selectivity of monosaccharide increased gradually with increasing temperature from 80 to 95 °C, and then decreased from 95 to 110 °C.

Fig. 2 Conversion of cellobiose (A) and yield of monosaccharide (B) catalyzed by La(DMBO)₂ with time at different temperatures at pH 9.0: () 80 °C, () 85 °C, () 90 °C, () 95 °C, () 100 °C, () 110 °C.

3.5 Products analysis and possible reaction pathway

In order to analyze the reaction products, HPLC and pulsed amperometric detection and mass spectrometry (PAD-MS) (LCMS-IT-TOF, Shimadzu of Japan) were employed. These studies indicated that there were four products – namely glucose, fructose, 1,6-anhydroglucose and glucosyl-erythrose (GE) – in the reaction solution, which is illustrated in Fig. 3. For the monosaccharides (glucose, fructose and 1,6-anhydroglucose), their content in the reaction solution was determined by HPLC with the external standard method. An unknown substance, whose mass spectrometry peaks at 283.1 ([GE + H]⁺) and 304.3 ([GE + Na]⁺) by PAD-MS(E+) as shown in Fig. S5 in the ESI,† was believed to be GE, which has been widely reported as one of main products of cellobiose decomposition,^13,15 although it cannot be accurately identified. The conversion of cellobiose and distribution of products at various temperatures for reaction of 10 h at pH 9.0 are listed in Table 2. Based on these studies, possible reaction pathways of cellobiose hydrolysis were suggested, as illustrated in Scheme 1.

Fig. 3 HPLC chromatograph of reaction solution of cellobiose hydrolysis.

Scheme 1 Possible reaction pathways of cellobiose hydrolysis.

3.6 Reaction kinetics

In many previous reports, kinetic behaviors of cellulose and cellobiose degradation were generally described as pseudo-first-order reactions.^1,10,13 However, when the association of catalyst (or enzyme) with substrate before further reacting is not ignored, the catalysis reaction involves a more complex kinetic process than simple first-order kinetics. In this work we found the hydrolysis of cellobiose showed complex kinetic characteristics. It seemed that two apparent first-order kinetic processes occurred, as illustrated in Fig. S6 in the ESI;† there were two straight lines in plots of −ln(1 − c_t/c₀) versus t. It is possible that the reaction product would inhibit the reaction, which resulted in a much slower reaction rate in the later stage than in the early stage of the hydrolysis reaction. Thus, according to our experimental results, a more detailed reaction pathway for cellobiose hydrolysis is proposed as shown in Scheme 2: first, cellobiose S combined with surfactant E to form an intermediate compound ES, and then ES further reacted to monosaccharide M and glucosyl-erythrose GE. In the first step, the surfactant E combined with substrate S reversibly with rate constants k₁ and k₋₁. Then followed the rate-determining steps with rate constants k₂ and k₃. k₄ and k₅ are the rate constants of cellobiose hydrolysis to M and GE in bulk solution, respectively. Based on reaction kinetic theory, kinetic eqn (1) and (2) were deduced, and the detailed deduced process can be found in the ESI.†where is the Michaelis constant, k_cat = k₂ + k₃, k₀ = k₄ + k₅, and E_T is the total concentration of surfactant. To avoid the interference of reaction products with reaction rate, the data of initial reaction time of 10 h were used to calculate k_cat, K_m and k₂ in this work. Variables K_m and k_cat were obtained by nonlinear fitting according to eqn S(9) in the ESI.† Variable k₂ was calculated according to eqn S(16) in the ESI.† The calculated results are listed in Table 3. From Fig. S7 and S8 in the ESI† it can be seen that the experimental data were in good agreement with the theoretical curves, and both the nonlinear correlation coefficients of eqn S(9) and the linear correlation coefficients of eqn S(16) were all above 0.97. This indicated that the reaction pathways (Scheme 2, eqn (1) and (2)) were reasonable.

Scheme 2 The reaction pathway proposed for catalysis reaction.

Table 3 K_m, k_cat and k₂ of cellobiose hydrolysis catalyzed by La(DMBO)₂ at pH 9.0

T/°C	80	85	90	95	100	110
10^2 Km/mol^−1 L^−1	2.48	2.55	2.89	3.03	3.47	3.53
10^4 kcat/s^−1	0.879	1.29	1.94	2.90	4.53	11.5
10^4 k2/s^−1	0.57	0.77	1.21	2.04	2.89	4.91

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From Table 3 it can be seen that values of K_m were all relatively small, which indicated the association of catalyst with cellobiose was clearly present in the kinetic reaction process. Although the reaction rate constants k_cat and k₂ were 100–300-fold smaller than those of catalysis by natural β-glucosidases,^20,45 the metallomicelle La(DMBO)₂ displayed considerable catalytic activity under these conditions. The hydrolysis mechanism for β-glucosidase was believed to be a two-step displacement process involving glycosylation and deglycosylation steps. In the catalytic active domain, two carboxylic acid groups –COOH and COO⁻ of glutamate residues play an essential role for the catalysis reaction.^27,28 In previous reports, organic acid catalysts such as oxalic acid, fumaric acid and maleic acid showed good catalytic activity only for the pretreatment of cellulose.^46–48 In our recent studies, we found that micelles containing the carboxylic acid group –COOH showed certain catalytic activity for the hydrolysis of methyl-β-D-cellobioside; however, the micelles displayed catalytic activity only for the glycosylation step rather than for the deglycosylation step.⁴⁹ In the present work it is found that metallomicelles containing oximido group N–OH displayed excellent catalytic activity for both hydrolysis of cellobiose and selectivity of monosaccharide, although the oximido functional group does not appear in the catalytic active domain of natural cellulase.

The activation energy and pre-exponential factor of the reactions were determined from the Arrhenius plots of ln k_cat vs. 1/T and ln k₂ vs. 1/T, as shown in Fig. 4. The activation energy E_a1 and pre-exponential factor A₁ of cellobiose conversion were evaluated as 96.13 kJ mol⁻¹ and 1.36 × 10¹⁰ s⁻¹ respectively. The activation energy E_a2 and the pre-exponential factor A₂ for generation of monosaccharide were evaluated as 84.6 kJ mol⁻¹ and 1.88 × 10⁸ s⁻¹ respectively, which were obtained easily through the slope and intercept of the linear plots respectively and the correlation coefficients of linear plots were above 0.98. It has been reported that the activation energy E_a of cellobiose hydrolysis catalyzed by enzyme was about 3–50 kJ mol⁻¹,^20,50,51 the activation energy of cellobiose hydrolysis catalyzed by non-enzyme was in the range of 110–200 kJ mol⁻¹,^1,13,52–55 and the activation energy for generation of monosaccharide was in the range 100–130 kJ mol⁻¹.^52,53 The activation energies for the hydrolysis of cellobiose and the generation of monosaccharide in this work are all relatively small, which indicates that the metallomicelle system displayed good catalytic efficiency for the breakage of β-glycoside bonds under mild conditions.

Fig. 4 Plots of ln k_cat vs. 1/T for the cellobiose hydrolysis and ln k₂ vs. 1/T for the generation of monosaccharide.

Further, the metallomicelle La(DMBO)₂ was used to catalyze the hydrolysis of cellulose (Whatman 42 filter paper). The experimental results showed that for a reaction time of 20 h at pH 9.0 and 95 °C, the residual mass of insoluble filter paper was about 91.7%, and the yield and selectivity of total reducing sugar were 5.7% and 70%, respectively. This indicated that the metallomicelle La(DMBO)₂ could catalyze the hydrolytic breakage of β-1,4-glucoside bond inside the cellulose molecule as does β-glucosidase.

4. Conclusions

This work investigated the catalytic hydrolysis of cellobiose to monosaccharide under mild conditions. The novel metallomicelle La(DMBO)₂ displayed excellent catalytic activity for both the conversion of cellobiose and yield of monosaccharide (glucose, fructose and 1,6-anhydroglucose) in weakly alkaline aqueous solutions at relative low temperature (80–110 °C). This catalytic activity could be attributed to the special enzyme-like micelle microenvironment and the strong nucleophilicity of the N–OH functional group. The relatively low activation energy E_a1 = 96.13 kJ mol⁻¹ for the conversion of cellobiose and E_a2 = 84.6 kJ mol⁻¹ for the generation of monosaccharide was calculated. This work may provide a new technology and method for the hydrolysis of cellulose to monosaccharide under mild conditions.

Acknowledgements

This work has been supported by the National Natural Science Foundation of China (no. 21273156).

Notes and references

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Footnote

† Electronic supplementary information (ESI) available. See DOI: 10.1039/c4ra14521f

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