Open Access

β-Glycosidases: An alternative enzyme based method for synthesis of alkyl-glycosides

Sustainable Chemical Processes20131:7

DOI: 10.1186/2043-7129-1-7

Received: 3 March 2013

Accepted: 24 May 2013

Published: 13 June 2013

Abstract

Alkyl-glycosides and -polyglycosides are environment friendly, non-ionic surfactants with favourable properties like biodegradability and chemical stability. These are extensively used in personal care products, pharmaceutical preparations and membrane protein research.

Commercial production of these surfactants is carried out in multiple steps through Fischer glycosylation reactions under extreme conditions in the presence of toxic catalysts.

β-glycosidases provide an alternative enzymatic method for their synthesis as these are easily available from microbial systems and exhibit broad substrate specificity and high stereo-selectivity. This review highlights the recent progress in glycosidase catalyzed synthesis of alkyl-glycosides. Several reaction parameters that affect the overall reaction kinetics, such as, water activity, nature of the glycosyl donor, pH of the reaction medium, reaction time, temperature and source of enzyme are discussed. Strategies available to enhance the yield, including two-phase solvent systems and immobilization are described. Current challenges and future prospects in the biological routes of synthesis are also reviewed.

Keywords

Eco-friendly surfactants Transglycosylation Alkyl glycosides Alkyl polyglycosides Two-phase system

Alkyl -glycosides and -polyglycosides

Growing ecological concern and commercial demand has generated considerable interest in eco-friendly, biodegradable and non-ionic surfactants such as alkyl-glycosides (AGs) and alkyl-polyglycosides (APGs) [1]. These are better surfactants than Triton X-100, carbohydrate esters because of their superior protein extraction capability [2], chemical stability in water and alkali and non-reactivity towards oxygen [3]. AGs contain a carbohydrate head group (which could be glucose, galactose, maltose, xylose, α-cyclodextrin) and a hydrocarbon tail (usually a primary alcohol) of different chain length of saturated or unsaturated nature [36]. These find diverse and attractive applications in personal care products, cosmetics, extraction of organic dyes and membrane protein research [1, 7]. APGs contain more than one sugar group at the hydrophilic end and can be composed of a complex mixture of alkyl homologues, oligomers, anomers and isomers. These also find extensive use in preparation of micro emulsions, detergents, cosmetics and pesticide formulations because of their excellent behaviour at interfaces [8, 9]. Commercial grade APGs contain short carbohydrate head groups, primarily monoglycosides and diglycosides, and their properties depend on the structure and bonding between the oligomeric head groups [8]. Selective elongation of AGs, such as extension of dodecyl-β-D-maltoside to dodecyl-β-D-maltooctaside by addition of α-cyclodextrin to the head group has resulted in improving their water solubility and reducing cytotoxicity [3].

The commercial production of AGs is carried out by Fischer glycosylation through direct synthesis or transacetalization. In direct synthesis, which is a one step approach, a fatty alcohol is reacted with glucose producing a complex mixture of AGs due to condensation at equally reactive hydroxyl groups. In the transacetalization synthesis, a carbohydrate is first coupled to a short alcohol like methanol producing methyl glycoside which subsequently acts as a substrate in the transacetalization with a longer alcohol [10]. The chemical route involves extremes of temperature, pressure, use of toxic catalysts, and multiple steps of protection, deprotection and activation [11]. AGs can also be prepared enzymatically by Glycosidases (E.C.3.2.1.-). These are co-factor independent hydrolytic enzymes and cleave glycosidic linkages in vivo to form mono- or oligosaccharides from poly-sugars. They can be used to synthesize glycosides in-vitro with judicious selection of reaction conditions. Most glycosidases used for synthetic purposes are either retaining or inverting enzymes, classified on the basis of whether the stereo character of the donor’s anomeric bond is retained or inverted. They may exhibit broad specificity with respect to their natural substrates or engineered substrates which broaden their applications [12]. Availability of glycosidases from natural (microorganisms, plant) and commercial source (almond seeds), robust nature and easy handling make them more attractive for synthesis. Another advantage of using glycosidases is that they operate at near neutral pH, ambient temperature, atmospheric pressure and are highly enantio- and regio-specific [13, 14].

Several reaction parameters affect the yield of AGs using glycosidases. These are water activity, temperature, time of incubation, pH of the reaction system, nature of the substrate and source of enzyme [15, 16]. These operating conditions can be manipulated to give high yield of the end products. Some other strategies such as immobilization of glycosidases, presence of organic solvents and use of reverse micelle system [13, 1719] have been adopted to make the enzymatic route more economical than the chemical route by allowing reuse of enzymes and suppressing parasitic hydrolysis of the synthesized products to give high yield per unit of enzyme. Medium engineering has also been successfully used for improving yield and employs micro-aqueous, two-phase and ionic liquid systems [2022].

In recent years, synthesis has also been attempted, with good success, with whole cell systems. The microbial cells can be cultivated on inexpensive media, stored and often the associated enzyme activities are stable. These systems are also being investigated extensively [2326]. Our laboratory has successfully shown the use of whole yeast cells for synthesis of medium and long chain AGs, APGs and aryl-oligosaccharides [20, 24, 25]. The reaction specificity is decided by the cell bound glycosidases resulting in formation of regio- and stereo-specific products. Since side reactions are absent, purification of the products is relatively straight forward. This makes it a commercially viable option. A variation of this approach has been to display glycosidases on the cell surface by fusion with the cell wall anchored proteins. This, in a way, mimics the concept of immobilized enzyme reactions [2729]. A significant progress has been made in the past few years to improve the transglycosylation yields by suppressing the secondary hydrolysis of the synthesized products by using engineered enzymes. These are a novel class of glycosidases, called as glycosynthases, and are produced by replacement of the carboxylate nucleophile by non-nucleophilic amino acid residue [30]. Glycosynthases promote glycosidic bond formation by providing a suitable activated glycosyl donor, such as a sugar fluoride [31]. The glycosynthase technology is now well established and substantial improvements have been made in this area to make enzymatic synthesis a more attractive option.

In this review, we focus on the use of glycosidases as alternative tools for alkyl glycoside synthesis with emphasis on process parameters that affect the yield. Novel strategies employed for overproduction of AGs and current challenges are also discussed.

Routes of alkyl glycoside synthesis

Chemical routes

In the chemical route, preparation of an anomerically pure AG requires numerous protection, deprotection and activation steps. Typically, all hydroxyl groups of sugars are first protected by acetylation using acetic anhydride/sodium acetate, aldehydes, acetals or benzoyl halides at 140°C in organic solvents or by microwave irradiation under mild reaction conditions (i.e., without solvent or with reduced catalyst loading) followed by deprotection by sodium methoxide in methanol (Figure 1). Activation step involves exchange of anomeric hydroxyl group with a bromine or chlorine atom. Large amounts of catalyst, mostly FeCl3, SnCl4, phosphotungstic acid, phosphomolybdic acid (50-100% by weight compared to the amount of sugars) are used at high temperature (80°C) to promote synthesis of AGs with moderate yield. Under the chemical method, two routes are described, namely, the Fischer glycosylation method and the Koenigs-Knorr method. Fischer glycosylation is simpler and less expensive than the Koenigs-Knorr method but the main drawback here is the use of bulk alcohol and strong mineral acids, which complicate the purification of the final products [10, 32, 33]. Furthermore, an equilibrium mixture of α- and β- glycosidic products is formed in a ratio that is dependent on thermodynamic stability of the isomers [34]. Koenigs-Knorr method is also a widely used method for AG synthesis but the limiting factor for large scale synthesis is the requirement of heavy metal salts like cadmium carbonate which are used as promoters [35]. Microwave irradiation has been recently used by synthetic chemists and is simple to execute, decreases reaction times and increases the product yield and purity [34, 36]. However, this is not suitable for large scale preparation as most polar alcohols undergo quick degradation under microwave irradiation [33].
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Figure 1

General strategy of glycosylation for α/β-alkyl-glucoside synthesis via chemical routes. Global protection (GP) of all hydroxyl groups using acetic anhydride/sodium acetate, aldehydes, acetals or benzoyl halides at 140°C. Activation step involves exchange of anomeric group by bromine (Br), fluorine (F), Iodine (I), Thiophenol (SPh) or tricholoroacetamide. Deprotection of final product by sodium methoxide in methanol.

Biological routes

In contrast to multi-step and catalyst dependent chemical routes, glycosidases do the same job using either of the two pathways, namely, the thermodynamically controlled reverse hydrolysis path or the kinetically driven transglycosylation route. In the former, alkyl glycoside is synthesized by reacting a monosaccharide with an alcohol in which the equilibrium of the reaction is shifted towards synthesis by reducing water activity. This is done by addition of co-solvents or by increasing the substrate concentration [21, 37]. In the second approach, activated glycoside donors (mostly aryl-glycosides) and an alcohol (as nucleophilic acceptor) are used to generate a new glycosidic bond [15, 21, 38].

Reaction mechanism

Glycosidases fall in to two most commonly employed mechanistic classes; one with net retention and the second with inversion of configuration after hydrolyzing the glycosidic bond at the anomeric centre. Essential features have been recently described [39, 40] for these two types of reaction mechanisms. The active site of both classes of enzymes contains two carboxylic acid residues (Glu/Asp), designated as R2 and R3 in Figure 2, which play a key role in the catalytic process. In case of inverting glycosidases, these residues are positioned approximately 10Å apart: one residue acts as an acid catalyst and the other as a base (Figure 2) and catalyzes the reaction by single displacement mechanism. The positioning of the two residues at 10 Å distance presumably allows the water and the other substrate to bind simultaneously [41]. Inverting glycosidases do not catalyze transglycosylation reaction; they just work in reverse hydrolysis mode. Unlike inverting glycosidases, the reaction mechanism of the retaining glycosidases involves a nucleophile group and an acid/base catalyst located approximately 5.5 Å apart. The reaction proceeds by double displacement mechanism in which a glycosyl enzyme intermediate is formed (glycosylation step) that has an anomeric configuration opposite to that of the starting substrate (Figure 2). Aglucone departure is facilitated by the protonation of the glucosidic oxygen by the acid catalyst. The second step of this reaction (deglucosylation step) involves the hydrolytic breakdown of the glycosyl-enzyme intermediate with net retention of anomeric configuration (Figure 2) [41]. In this, a water molecule is activated by the catalytic base to serve as a nucleophile for the hydrolysis of the glucosidic bond [42]. Under suitable reaction conditions, covalently bond glucose of the glucosyl-enzyme intermediate is transferred to other nucleophile (NuH) designated as R4 in Figure 2, which can be an alcohol or a second sugar. Both inverting as well as the retaining glycosidases involve oxocarbenium-ion-like transition state.
https://static-content.springer.com/image/art%3A10.1186%2F2043-7129-1-7/MediaObjects/40508_2013_Article_7_Fig2_HTML.jpg
Figure 2

General reaction mechanism for glycosidases. (a) Inverting enzymes, (b) Retaining enzymes. The reaction cycle is explained in the text.

Advantages of β-glycosidase driven synthesis

The synthesis of well-defined sugars and sugar linked derivatives by β-glycosidases and other glycosyl hydrolases has resulted in a boom in the area of Green chemistry. Other enzymes, namely, transglycosidases, glycoside phosphorylases and ‘Leloir’ glycosyl transferases, each with specific characteristics, may also be used in glycosylation reactions [43]. Although ‘Leloir’ glycosyl transferases are highly efficient Nature’s catalyst for glycosylation reactions but they require very expensive nucleotide-activated sugars as donors like UDP-glucose, UDP-galactose which is the major bottleneck in their application for the commercial production of glycosides [43]. However, glycoside phosphorylases and transglycosidases are active with low cost donors that can be obtained in large quantities. Our discussion in the following paragraph focuses on β–glycosidases.

β-Glycosidases have gained wide acceptance in the area of biocatalysis. In the CAZy database (Carbohydrate Active Enzymes, http://www.cazy.org/) glycosidases are structurally divided in to 132 families [44]. Most of the well characterized β–glycosidases are from GH1, GH3 and GH30 families and are retaining enzymes, whereas those belonging to GH9 are inverting enzymes. GH1 includes the largest number of characterized β-glucosidases, which are of interest in biomass conversion [45]. Under unnatural conditions they are able to form the glycosidic linkages. The glycosidases used for the synthetic purposes are exo-glycosidases.

The two essential parameters for the use of glycosidases in industry are space-time yield (STY) and E factor (product/waste ratio) [46]. Under optimized conditions, the enzymatic glycosylation reactions have been reported to generate 5-fold less waste and 15-fold higher space-time yield [47]. One of the major problems in the fine chemical industry is generation of non-recyclable waste. In case of the classical Koenigs-Knorr procedure, nearly half of the waste consists of acetic acid. In the modified procedure of glycosylation [16] nearly 5g of mercuric salts are formed for each gram of the synthesized product. In the enzymatic methods, on the other hand, sugars are the only wastes formed. Although the cost of the substrate is high, the process is cleaner as enzymes operate naturally at ambient temperature and do not require toxic catalysts. A comparison between the chemical and the enzymatic method [13] indicates that while the yields are better in the former, it is accompanied by generation of a lot of waste (Table 1). In the different methods employed [4852], transglycosylation route resulted in the highest space-time yield [49].
Table 1

Comparison of enzymatic and chemical glycosylation in terms of Space-Time Yield and E-factor

Glycosylation method

Glycosyl donor

Product

Efactor (kg waste per kg product)

Space-time yield (g/l/d)

Reference

Direct glycosylation (by glycosidase)

Glucose

Glcβ-O(CH2)6OH

0.5

5.6

[48]

Transglycosylation

Lactose

Galβ-O(CH2)6OH

3

2380

[49]

(by β-galactosidase)

Koenigs-Knorr method

Galactose

Galβ-OPh-2-NO2

10

26

[50]

Direct glycosylation (by glycosidase)

Glucose

Glcβ-OCH(CH3)CHCH2

2

10

[51]

Koenigs-Knorr method

Glucose

Glcβ-OCH(CH3)CHCH2

20

36

[52]

Another fundamental parameter in glycosidase catalyzed synthesis is the cost and availability of reactants, especially the glycosyl donor. The most commonly used glycosyl donors in bulk are starch, sucrose, cellulose, glucose and fructose. Although there are other active glycosyl donors, which are more effective in transglycosylation reaction, the main drawback is the high cost of these compounds which restricts their use on large scale. Some commonly used donors in the glycosidase catalyzed reactions are listed in Figure 3.
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Figure 3

Glycosyl donors used for enzymatic synthesis of alkyl glycosides. (a) Commonly used substrates such as cellobiose, methyl-β-D-glucoside and aryl glucosides. (b) Novel substrates.

β-Glycosidase driven synthesis can be performed using either the reverse hydrolysis or the transglycosylation approach. As shown in Table 2, moderate yields (up to 62%) have been reported for lower chain length AGs, namely, methyl glucoside/xyloside and ethyl glucoside/xyloside, in the reverse hydrolysis approach over prolonged reaction times [5, 53, 54]. The yield of many of these compounds could be increased substantially (even up to ~90%) in the transglycosylation approach [5, 5358] (Table 3). A yield of over 90% has been reported for methyl-β-D-fucoside using the Paenibacillus enzyme [59].The yields (Table 2) for higher chain alkyl glucosides range from 1.9% (decyl glucoside) to 36% (for butyl glucoside) in the reverse hydrolysis approach [19, 21, 54, 55]. In the transglycosylation route (Table 3), the reported yield ranges from 4-97% [5, 16, 17, 19, 20, 24, 2629, 53, 5570]. As observed in Tables 2 and 3, majority of these synthesis reactions have been carried out using purified enzymes. A list of the microbial sources of these enzymes is provided in Figure 4. It can also be seen that much of the reported work has involved the use of bacterial or the almond enzyme (which is commercially available). Whole cell catalysis is a relatively newer area but given the high yields reported with some microbial cells [20, 24, 26], this approach requires an in-depth study.
Table 2

Synthesis of alkyl glycosides by β-glycosidases via reverse hydrolysis route

Source of enzyme

Glycosyl donor

Glycosyl acceptor

Product

Yield (%)

Time(h)

Ref

Almond β-glucosidase

Xylose

Methanol

Methyl-β-D-xylopyranoside

Poor Yields

6 Days

[5]

Ethanol

Ethyl-β-D-xylopyranoside

Propanol

Propyl-β-D-xylopyranoside

Butanol

Butyl-β-D-xylopyranoside

Pentanol

ND

Hexanol

ND

Heptanol

ND

Octanol

ND

Almond β-glucosidase

Glucose

Hexanol

Hexyl-β-D-glucopyranoside

11

144

[55]

Almond β-glucosidase

Glucose

Methanol

Methyl-β-D- glucopyranoside

58

54

[53]

Almond β-glucosidase

Glucose

Butanol

Butyl-β-D- glucopyranoside

30

Not Given

[21]

Almond β-glucosidase

Glucose

Octanol

Octyl-β-D-glucopyranoside

20

200

[19]

Almond meal

Glucose

Methanol

Methyl-β-D-glucopyranoside

27.6

168

[54]

Ethanol

Ethyl-β-D-glucopyranoside

62.5

Propanol

Propyl-β-D-glucopyranoside

58.7

Butanol

Butyl-β-D-glucopyranoside

36.1

Pentanol

Pentyl-β-D-glucopyranoside

13.7

Hexanol

Hexyl-β-D-glucopyranoside

9.17

Heptanol

Heptyl-β-D-glucopyranoside

4.57

Octanol

Octyl-β-D-glucopyranoside

4.05

Nonanol

Nonyl-β-D-glucopyranoside

2.92

Decanol

Decyl-β-D-glucopyranoside

1.93

ND: not detected.

Table 3

Synthesis of alkyl glycosides by βglycosidases via transglycosylation route

Source of enzyme

Glycosyl donor

Glycosyl acceptor

Product

Yield (%)

Time (h)

Reference

Trichoderma reesei β-xylosidase

Methyl-β-D-xyloside

Ethanol, Propanol

Ethyl-β-D-xyloside, Propyl-β-D-xyloside

52-55

12

[5]

Candida molischiana35M5N β- glucosidase

Cellobiose

1-decanol

Decyl-β-D-glucopyranoside

Lower yields

20

[60]

Almond β-glucosidase

Methyl-β-D-glucoside

Hexanol

Hexyl-β-D-glucopyranoside

25

24

[55]

Cellobiose

  

28

48

β-glucosidase II Aspergillus niger

Cellobiose

Methanol

Methyl-β-D-glucopyranoside

82

0.5

[56]

 

Ethanol

Ethyl-β-D- glucopyranoside

55

 

Almond β-glucosidase

Cellobiose

Methanol

Methyl-β-D-glucopyranoside

37

5

[53]

β-glucosidase from Fusarium oxysporum

Cellobiose

Methanol

Methyl-β-D-glucopyranoside

54.4

 

[57]

Gentiobiose

  

51.3

Amygdalin

  

63.4

Arbutin

  

72.2

Salicin

  

58

pNPG

  

74.2

Aspergillus niger β-glucosidase II

Cellobiose

Methanol

Methyl-β-D-glucopyranoside

83

6

[58]

 

Ethanol

Ethyl-β-D- glucopyranoside

53

3

Hyperthermophilic β-glycosidase

Lactose

Heptanol

Heptyl-β-D-glucopyranoside

22.5

25

[61]

β-Glucosidase from Thai Rosewood

pNPG

C1-C4 1° alcohols

β-alkyl glucosides

C1 = 97

7

[62]

C2 = 93

C3 = 81

C4 = 89

β-Galactosidase Penicillium canescencs

Lactose

Heptanol

Heptyl-β-D- galactopyranoside

43

80

[19]

Octanol

Octyl-β-D- galactopyranoside

45

Nonanol

Nonyl-β-D- galactopyranoside

37

Almond β- glucosidase

pNPG

Octanol

Octyl-β-D- glucopyranoside

42

NA

[63]

β-glucosidase from C. Saccharolyticum

pNPG

Octanol

Octyl-β-D- glucopyranoside

45

β-glycosidase from bitter almond

Methyl-β- D-glucoside

Hexanol

Hexyl-β-D- glucopyranoside

21

155

[64]

β-galactosidase from Aspergillus oryzae

Lactose

 

Hexyl-β-D- galactopyranoside

4

 

β-glycosidases from Sulfolobus solfataricus (LacS)/ Pyrococcus furiosus (CelB).

Lactose

Hexanol

Hexyl-β-D- glucopyranoside/Hexyl-β-D- galactopyranoside

29/28

10

[16]

41/63

20

Almond β- glucosidase adsorbed on Celite R-640®

pNPG

Octanol

Octyl-β-D- glucopyranoside

37.2

650

[17]

Almond β- glucosidase

pNPG

Primary alcohols (C1-C6)

β-alkyl glucosides

C1 = 81

24

[65]

C2 = 64

C3 = 48

C4 = 25

C5 = 22

C6 = 18

Whole cells of Bacillus pseudofirmus

Lactose

Hexanol

Hexyl-β-D-galactopyranoside

50

3

[26]

Octanol

Octyl-β-D-galactopyranoside

26

20

Thermotoga neapolitana β-glucosidase B

pNPG

Hexanol

Hexyl-β-D- glucoside

80.3

3

[66]

β-galactosidase from Aspergillus aculeatus displayed on Yeast cells

pNPG

Hexanol

Hexyl-β-D- glucoside

27.3

12

[27]

β-glucosidase Sclerotinia sclerotium

Cellobiose

Primary alcohols (C4-C8)

β-alkyl- glucosides

Moderate yields

30

[38]

β-galactosidase displayed on Bacillus spores

Lactose

Octanol

Octyl-β-D- galactopyranoside

27.7

24

[29]

Pseudoaltermonas 22b β- galactosidase

Lactose

1° alcohols (C5-C9)

Pentyl-β-D- galactopyranoside

31

48

[68]

Hexyl-β-D- galactopyranoside

28

Heptyl- β-D- galactopyranoside

18

Octyl- β-D- glactopyranoside

9

Nonoyl- β-D- galactopyranoside

5

β-D-Galactosidase from Paenibacillus thiaminolyticus

pNP-β-D- Fucose

Methanol

Methyl-β-D-fucoside

94

2.5

[59]

Ethanol

Ethyl-β-D-fucoside

72

Propanol

Propyl-β-D-fucoside

56 4

Octanol

Octyl-β-D-fucoside

15 2

β-D-galactosidase from Aspergillus niger

Lactose

Hexanol

Hexyl-β-D-pyranoside

10

3

[69]

Heptanol

Heptyl-β-D-galacto pyranoside

8

Cell bound β-glucosidase of pyranoside Pichia etchellsii

pNPG

Octanol

Octyl-β-D-glucopyranoside

70

4

[20]

β-Galactosidase on cell surface of Bacillus subtilis

Lactose

Octanol

Octyl-β-D-galactopyranoside

33.7

24

[28]

Xylanase from Thermobacillus xylanilyticus

Birchwood xylan

Pentanol

Pentyl-β-D-xylobioside

85

1

[70]

Octanol

Octyl-β-D-xyloside

8

 

Octyl-β-D-xylobioside

14

 

Octyl-β-D-xylotrioside

21

Cell bound β-glucosidase of Pichia etchellsii

Methyl-β- D-glucoside

Hexanol

Hexyl-β-D-glucopyranoside

48

6

[24]

Octanol

Octyl-β-D-glucopyranoside

53

Decanol

Decyl-β-D-glucopyranoside

27

Dodecanol

Dodecyl-β-D-glucopyranoside

13

https://static-content.springer.com/image/art%3A10.1186%2F2043-7129-1-7/MediaObjects/40508_2013_Article_7_Fig4_HTML.jpg
Figure 4

Publications on use of β-glycosidase from different sources for synthesis of various alkyl-glycosides in the period of 2000 2012. Source: Web of Science database (http://www.scopus.com/home.url).

Process parameters affecting enzymatic synthesis

Water activity

A key process parameter which affects the glycosidase-catalyzed synthesis is the water activity of the reaction medium; a sufficiently high water activity (aw = 0.6) is required by glycosidases to retain activity. This is unlike lipases which can be active at water activity close to zero [71]. However, a high water content promotes hydrolysis thus decreasing the overall product concentration. The yield in kinetically controlled reactions depends on the concentration of water and other competing nucleophiles like alcohols and the selectivity of the enzyme. Large alcohols need higher water activity to be active as glycosyl acceptors compared to the small ones as this increases the flexibility of the active site for accommodating the large nucleophiles. The optimal water activity has been determined for different chain length alcohols and indicated water activity (aw) of 0.43, 0.71 and 0.81 for propanol, hexanol and octanol respectively [16]. An optimal water activity of 0.67 was also reported for XAD-4 immobilized β-glucosidase for octyl-β-D-glucoside synthesis [71]. An elaborate study on five different glycosidase-catalyzed transglycosylation reactions in hexanol showed that the best conditions for transglycosylation were higher water activity but without a separate aqueous phase and for all the enzymes the selectivity for alcohol increased with an increase in water activity [16]. In the reverse hydrolysis mode, a decrease in water activity resulted in an increase in equilibrium yield of hexyl glucoside but this was not the case in the kinetically controlled reaction wherein the ratio between transglucosylation and hydrolysis increased with an increase in water activity [72]. Since water activity and water content show close correlation, studies on the effect of water content in the organic reaction are of crucial significance. Effect of water content (5-30%, v/v) on the ratio of transglycosylation rate to hydrolysis rate (rT/rH) has been studied during the synthesis of hexyl glucoside and octyl glucoside using p-nitrophenyl-β-D-glucopyranoside (pNPG) and methyl glucoside as donors respectively. For hexyl glucoside synthesis, a ratio of rT/rH of 5.1 at 16% water content was found to be optimum and a maximum ratio of rT/rH 2.28 at 8% water content was optimum for octyl glucoside synthesis. Above this optimum water content, a drastic decrease in rT/rH was observed possibly because of mass transfer limitation of pNPG or methyl glucoside from organic to aqueous phase [24, 66]. Thus, for every enzyme/cell system, the conditions need to be optimized.

Nature of the substrate

As mentioned in the previous sections, the yield of alkyl glycoside is generally lower in the reverse hydrolysis mode (Table 2) as the equilibrium constant of the reaction lies strongly in favour of hydrolysis. Thus, higher concentration of both the monosaccharide and other nucleophile is required in this route of synthesis. Since the transglycosylation route is directly under kinetic control and utilizes a pre- formed activated glycoside donor; the glycosyl donor must be cleaved more rapidly than the product formed. Several compounds have been used as glycosyl donors, the predominant ones being the aryl glycosides and disaccharides (Figure 3a).The transglycosylation approach gives higher yields (Table 3), especially, when aryl donors are used in the reaction. The use of nitro-phenyl glycoside donors may have many drawbacks like limited solubility, auto-condensation of the donor substrate and difficulty in removal of nitrophenol from the reaction mixture [12]. Glycosyl donors with other leaving groups (Figure 3b) have been proposed as a solution to this problem [12]. Besides these, glycosyl fluoride donors, which have poor stability in water, have also been used with glycosynthases. For β-glucosidases and β-galactosidases, glycosyl azides are considered to be good alternative substrates [73].

Different chain length alcohols, mostly primary alcohols, have been used as acceptors for the synthesis of AGs (Tables 2 and 3). These are also found to be better acceptors compared to the secondary or tertiary alcohols. This is attributed to their increased reactivity on account of favorable steric factors during nucleophilic attack. The inability of β-glycosidases to use secondary or tertiary alcohols as acceptors appears to be a general phenomenon with almost all glycosidases [13]. However, an exception is reported and this is the β-glucosidase from cassava [74].

Effect of pH, temperature and shaking

To carry out enzymatic reactions in aqueous solutions, it is a common practice to add buffering agents to influence the state of ionization of important functional groups at the active site of the enzyme. Likewise, ionization of functional groups at active site is also important while carrying out reactions in presence of organic solvents. Addition or removal of proton at the active site can turn the enzyme on or off. Enzymes in organic solvents retain the ionization state of active site residues of its natural environment (water) even after lyophilizing the enzyme, this is called as the ‘pH memory’ of enzymes [75]. Most of the glycosidases are active in the entire pH range of 4–7 and have highest hydrolytic activity at pH 6. Therefore, most of the synthesis work has been carried out in this pH range leading to maximum yield of the final product.

Effect of temperature on direct alkylation of glucose or in transglycosylation reactions has also been investigated and indicates no significant improvement in final yields with an increase in temperature [15, 20]. Although higher temperature is favourable for increasing the solubility of the substrates, it can inactivate the enzymes. Thus, thermostable enzymes would be desirable in synthesis. Generally, β-glycosidase have temperature optima between 40-50°C [76] and most of the synthesis work has been carried out in this temperature range. With some thermophilic β-glucosidases, such as those from Thermotoga neapolitana and Pyroccocus furiosus, synthesis of hexyl and octyl glucoside using pNPG and pentyl glucoside respectively as glucosyl donor has been reported. T. neapolitana β-glucosidases catalyzed 100% conversion of pNPG in hexanol/water mixture with increase in temperature up to 90°C with a yield of 80.3% [66]. Mutants from P. furiosus showed higher selectivity and resulted in increased hexyl glucoside yield from 56 to 69% over a temperature range of 50-95°C compared to the wild type [16]. These differences may be explained by two factors, namely enzyme denaturation and variation in media composition [77]. Thus, higher temperature can lead to better conversion efficiencies.

For the synthesis of long chain AGs, an important limitation is the poor water solubility of the glycosyl acceptor thus preventing an efficient contact with the glycosyl enzyme intermediate. For minimizing this physical effect, strategies such as vigorous shaking, use of co-solvents and use of different chain length glycosyl acceptors (like methanol, butanol, pentanol, hexanol, heptanol, octanol, decanol and dodecanol) in bulk can be employed [70]. Not much work has been done to study the effect of shaking but it is expected to enhance the conversion efficiencies by removing the products from the enzyme active site. An increase from 200 to 1000 rpm has been reported to enhance the yield from 80 mg/g to 362 mg/g [70] in the transglycosylation route.

Available strategies for improving the yield of alkyl glycosides

A number of strategies have been developed to increase the yield in enzyme driven synthesis of AGs and these are summarized below.

Immobilization, whole cell biocatalysis and cell surface display of enzymes

The use of immobilized enzymes is justified if the biocatalyst can be reused efficiently. For improving the yield of the glycosidase catalyzed reactions, hydration level of the media has to be carefully maintained because the presence of water is necessary for enzyme activity but at the same time water causes parasitic hydrolysis of the substrate and product [17]. Celite R-640® is a chemically inert silica-based matrix and has shown promising potential for maintaining hydration level of media during enzyme catalyzed peptide and amide synthesis [78]. The application of Celite R-640® as a support for immobilization of β-glucosidase for synthesis of AGs has been demonstrated [17]. This preparation exhibited good stability of the enzyme even in co-solvents like dimethyl formamide compared to enzymes immobilized on Amberlite XAD-4. Other materials such as DEAE-sepharose and polyacrylamide have also been used to immobilize β-glucosidases for synthesis of AGs. More than increased yield, this lead to improved stability of the enzyme when compared to the free enzyme [18]. Another support, namely, XAD-4/16 Celite has also been used and was shown to increase β-glucosidase activity. No effect on yield was reported with these preparations [16]. There is only one report on whole cell immobilization and that is of Bacillus pseudofirmus AR 199 cells on polyvinyl alcohol cryogel beads and on Celite for synthesis of alkyl galactosides. A decrease in reaction rate was observed with final yield of 26% for octyl galactoside in both cases after 72 h of reaction in comparison to 20 h with free cells [26].

Microencapsulation of β-glucosidase in permeable matrices prepared from polyallylamine hydrochloride/1-6, hexanediamine and dodecanedioyl chloride has been attempted to overcome mass transfer limitations in aqueous organic two phase system; the aqueous phase containing the enzyme and the substrate being contained in the hydrophobic phase [65]. The enzyme in the micro capsules prepared from polyallylamine hydrochloride performed significantly better presumably due to enhanced permeability emphasizing the importance of optimizing the polymer composition. At the same enzyme loading, the formation of hexyl glucoside was 2.5 times faster in microencapsulated system than with the enzyme immobilized on XAD-4 polymeric adsorbent. The potential for improved productivity using microencapsulated β-glucosidase has been further explored by operating a batch reactor at 50 ml scale with similar reaction kinetics over a period of two weeks by recharging microcapsules with glucose [65].

Whole cell biocatalysis approach has also been attempted, albeit, by only a few laboratories, for synthesis of AGs. The principal advantage of using whole cells is that the process can be economical and exhibit less sensitivity to denaturation as the cells can act as natural immobilized systems [20, 24, 26]. Cell permeabilization using membrane disrupting agents was suggested as a means to overcome mass transfer limitations but no effect was observed on the final yield of the desired products [24, 26]. Another advantage of using whole cell biocatalysts is that cells can be lyophilized without the aid of lyoprotectants unlike purified enzymes. Lyophilization presumably locks the enzyme molecules on the cell surface in their right conformation so that activity is not lost. On the other hand, with purified enzymes it can lead to significant denaturation of activity. Using a bacterial system, 26% yield was reported using lactose as glycosyl donor [26]. Promising yields of 53% and 70% were reported for a medium chain length alkyl glycoside (octyl glucoside) using methyl glucoside and pNPG as donors respectively [20, 24]. Interestingly, no side reactions were observed with this conversion. The whole cell system was also operated at 50 ml scale using methyl glucoside as donor for octyl glucoside synthesis. The reactor performance was tested in three reaction cycles run semi continuously over a period of 18 h with 100% substrate conversion and improvement in yield [24]. Given the economic viability of using whole cells, such transformations need to be studied with other systems as well. Another recent methodology attempted to make whole cell biocatalysis more attractive is to display recombinant enzymes on the cell surface. This can serve as an immobilized enzyme preparation with cell-wall-anchored proteins [27]. A yield of 27.3% of hexyl glucoside was obtained with this system using pNPG as donor. Recently, β-galactosidase was expressed on Bacillus subtilis spores by fusion with the spore coat proteins. This immobilized enzyme showed better solvent stability, enhanced thermal stability and transgalactosylation efficiency in non-aqueous media resulting in overall yield of 27.7 to 33.7% of octyl galactoside [28, 29].

Two-phase, micro-aqueous and mono-phasic system

The success of glycosidic bond formation depends on whether the glycosyl-enzyme intermediate is trapped by glycosyl acceptors other than water. Alcohols are better bound at enzyme active site than water, but at the same time water acts as a competing nucleophile thereby decreasing the overall transglycosylation yield [71]. The yields can be improved if these reactions are carried out predominantly in organic solvents but glycosidase lose activity in such media. Unlike lipase, glycosidase require a minimum amount of water to catalyze transglycosylation reactions. A water activity (aw) of 0.4-0.5 is required by almond β-glucosidase for lower alcohols (C3-alcohols) while for higher chain alcohols (C8) a water activity in the range of 0.67-0.8 was required [13, 71]. While using whole cells of Pichia etchellsii, again a high water activity was required for synthesis of octyl glucoside [20]. While it is desirable to shift the reactions to lower water activity environment to shift the reaction equilibrium towards synthesis, this will result in lowered activity of the enzyme and also poor solubility of long chain alcohols affecting the overall yield. To address these problems, aqueous organic two phase system has been suggested and used for synthesis of AGs [15]. The problems associated with the two phase system were the instability of glycosidases and competitive hydrolysis of substrate and products [13]. Organic one phase liquid system has also been used to address the problems associated with the two phase system, but some amount of water is always found to be necessary for catalytic activity of glycosidases and they fail to catalyze reactions in completely anhydrous organic media [21, 24]. It has been suggested that adding co-solvents increases the solubility of sugar substrates and decreases the water activity [15]. The co-solvents generally used should be biocompatible, water miscible, of low boiling point and must maintain high enzyme activity and low water activity. The most suitable co-solvents for β–glycosidases were found to be monoglyme, diglyme, 1,4-dioxane, methanol, acetonitrile, dimethyl sulfoxide, tetrahydrofuran, dimethyl formamide, tert-butanol. These can be used up to a concentration of 10 to 20% (v/v) of the total reaction volume [79]. The yields obtained under such conditions were 52, 26, 21 and 17% for hexyl-, octyl-, decyl and dodecyl glucoside respectively [79]. It is also important to note that low aqueous systems are feasible only with hydrophobic glycosyl donors like methyl-β-D-glucopyranoside, phenyl-β-D-glucopyranoside, and 4-nitrophenyl-β-D-glucopyranoside [20, 24].

Reverse micelles

Reverse micelles or micro emulsions can be considered as individual nano bioreactors and these have added new properties to biocatalysts in a variety of biotransformations [19]. Reverse micelles in organic medium are formed by association of surfactant molecules with outer layer formed of hydrocarbon tails and inner layer by polar heads. The most remarkable property of reverse micelles is their capacity to solubilize water and hydrophilic substrates with retention of catalytic activity. As observed in the preceding paragraph, much of the synthesis work on AGs has been reported in two-phase systems, with the aqueous phase containing the enzyme and the substrate. A major bottleneck in two-phase system is the poor solubility of long chain alcohols in the aqueous phase thereby displaying limited accessibility to the glycosyl enzyme intermediate. This leads to reduced rate of transglycosylation. Elevated temperatures can be used to improve yields but it leads to denaturation of enzyme [20, 21]. Due to these disadvantages in the two phase system, reverse micelles have been used and shown to enhance the yield significantly [19]. Reverse micelle system has also been used to catalyze synthesis of octyl-β-D-glucopyranoside and octyl-β-D-galactopyranoside with maximum yields of 40 and 45% using glucose and lactose as donors respectively exceeding the yields of enzymatic synthesis in two phase system where synthesis proceeds in extremely low yields (6-9%) [19]. The major concern in this reaction system remains the recovery of the final product from the surfactant in the reaction system [80].

Use of ionic liquids as a novel medium for yield improvement

An elegant new strategy to enhance yield in glycosidase catalyzed reactions has been the use of ionic liquids in place of organic solvents to suppress/lower the water activity of the system. These are salts that do not crystallize at room temperature. Because of the outstanding thermal stability (up to 300°C), near to zero vapor pressure and an excellent miscibility property, they are considered as green solvents for future [81, 82]. Typical ionic liquids are mixtures of dialkylimidazolium cations with weakly coordinating anions such as methyl sulfate or hexafluorophosphate. Over the past decade, ionic liquids have gained increased attention as reaction media for enzyme catalyzed reactions with promising results by replacing organic co-solvents. They can be used as a pure solvent, as a co-solvent in aqueous systems or in a biphasic system. To date use of ionic liquids (1-Butyl-3-methylimidazolium hexafluorophosphate, 1-Butyl-3-methylimidazolium tetrafluoroborate) has shown excellent results with lipase, esterases and protease enzymes by retaining activity and selectivity as in the original medium [83]. Very little research has been done on synthesis of alkyl glycosides and oligosaccharides in ionic liquids using glycosidases [84]. The yields are often disappointing as the formation of the glycosidic bond is considered to be thermodynamically less favourable than formation of an ester or an amide bond. In contrast to esterases and lipases, most glycosidases lose activity in ionic liquids, although solubility of their substrates (sugars) is reported to be increased [85]. Use of ionic liquid 1,3-dimethyl-imidazol methyl sulfate for the enzymatic synthesis of N-acetyllactosoamine from lactose and N-acetylglucosamine using β-galactosidase from Bacillus circulans has shown promising results by doubling the yield from 30% to 60% by suppressing secondary hydrolysis of the synthesized product [86]. Another glycosidase from P. furious has shown 10% increase in galactosyl transfer from lactose to glycerol using 45% (v/v) 1,3-di-methyl-imidazol methyl sulfate ionic liquid [84]. Recently, Yang and his co-workers have examined various ionic liquids for the enzymatic synthesis of aryl-, alkyl-β-D-glucopyranosides catalyzed by crude enzyme preparation (prune seed meal, Prunus domestica). Among the examined ionic liquids, the novel 1-butyl-3-methylimidazole iodide [BMIm]I at 10% concentration proved to be the best and was used first time for the synthesis of aryl-, alkyl-β-D-glucopyranosides with yields ranging from 15-28% [87]. Use of ionic liquid 1-butyl-3-methyl-imidazolium chloride has been reported by synthetic chemists in conversion of cellulose to isomers of alkyl glucosides with yields of 82-86% in presence of an acid catalyst [88]. This reaction can be replaced by an enzymatic route to make the process more attractive. From the initial investigation on use of ionic liquids, it is obvious that they offer a useful method in enzymatic transglycosylation and are effective in reducing water activity and increase solubility of the hydrophilic substrates. The polar nature of ionic liquids makes them suitable candidates for glycosidase catalyzed synthesis, if one has to use cheap polar substrates like glucose, lactose, cellobiose, maltose, cellulose hydrolysate as glycosyl donors. In order to make the ionic liquid system more competitive and better than the water co-solvent systems, recovery and reuse of ionic liquids will play a major role. The issues of cost, toxicity and biodegradability of these compounds also needs to be addressed.

Protein engineering

Recent technological and scientific achievements in DNA recombinant technology has broadened the scope of biocatalysis both in the laboratory as well as on industrial scale [89]. Major bottleneck for using biocatalyst is its poor stability and optimizing the biocatalyst for the non-natural substrates. Currently the molecular biology methods are used to rapidly modify enzymes via in vitro version of Darwinian evolution, commonly known as directed evolution. This involves creation of smarter libraries by random amino acid changes in protein with improvement in its stability and broad substrate specificity [89]. Since glycosidases are often limited by their tight donor specificities, several groups have developed glycosidases with altered and broad substrate specificity. Promiscuous glycosidases have been developed by site directed mutagenesis in Sulfolobus solfataricus by mutating two key residues which resulted in broad substrate specificity capable of processing many sugars namely lactose, xylose and glucose. The mutant enzymes from S. solfataricus showed good synthetic activity and produced methyl-β-galactoside, methyl-β-xyloside and methyl-β-glucoside in 100, 50 and 87% yield [90].

Conclusions

Alkyl glycosides are used in wide range of applications particularly in personal care products, membrane protein research, as boosters for antibacterial agents. They have several attractive properties like biodegradability, low toxicity and can be prepared from renewable sources. The chemical route of synthesis is followed currently for large scale production of these compounds. The enzymatic routes can be followed using glycosidases which use either the `reverse hydrolysis’ or the `transglycosylation’ approach. The major advantage of using β-glycosidases for alkyl glycoside synthesis is that these operate at neutral pH, ambient temperature, atmospheric pressure and catalyze enantio- and regio-specific reactions. While significant progress has been made in increasing the yield in enzyme catalyzed synthesis the cost of production still remains high. Further, the enzyme based synthesis works well for the synthesis of lower chain length alkyl glycosides. With higher chain length alcohols (above C8) low yields are obtained due to poor miscibility of long chain alcohols with water. Medium engineering has been used as a successful approach for increasing the yield. Although solubility can be improved by using higher temperature but that leads to denaturation of the enzymes. Development of thermophilic and organic solvent tolerant enzymes by protein engineering approach can address some of these issues.

Future prospects

Nearly 30% more people will occupy Earth in the year 2050, increasing the demand for day-to-day services. This is likely to result in ecosystem degradation, reduced bio-diversity and of course changing climate. One of the major concerns is to reduce use of chemical routes for synthesis of common products and shift towards enzyme based technologies. New strategies need to be developed as enzymatic methods provide an excellent eco-friendly alternative. Coupling the enzymatic routes to continuous product removal strategies (for instance, by use of special matrices that selectively bind products) can lead to efficient conversion efficiencies. While such systems can be operated at laboratory scale, a bioreactor for commercial scale production is in high demand. Thermophilic enzymes (or cell sources of these enzymes) could also be used in such conversions. Whole cell catalysis is a novel approach and requires an in-depth study. Development of genetically engineered enzymes with increased organic solvent tolerance and selectivity towards nucleophile other than water would be desirable. Ionic liquids offer many advantages over conventional organic solvents because of their excellent physico chemical properties like thermal stability, near-zero vapour pressure, tunable properties like polarity/hydrophobicity/solvent miscibility. Some success has been reported with these in alkyl glucoside synthesis. These also allow use of a large range of compounds which can be solubilized by adjusting the cation/anion ratio. Another important feature of using ionic liquids is their ability to enhance in some cases enantio-, stereo-, and regio selectivity. Very little work has been reported using this solvent for β–glycosidases and needs to be investigated extensively.

Authors’ information

MYR is currently a visiting scientist in the Dept. of biotechnology at Lund university, Sweden. SM is a Professor in the Dept. of biochemical engineering and biotechnology at IIT Delhi, New Delhi.

Declarations

Acknowledgements

The work in this area was supported by a grant from Defense Research Development Organization (Govt. of India).

Authors’ Affiliations

(1)
Department of Biotechnology, Lund University
(2)
Department of Biochemical Engineering and Biotechnology, Indian Institute of Technology Delhi

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