Chemoenzymatic epoxidation of alkenes with Candida antarctica lipase B and hydrogen peroxide in deep eutectic solvents

Article abstract of DOI:10.1039/c7ra00805h

Epoxides are important synthetic intermediates for the synthesis of a broad range of industrial products. This study presents a promising solution to the current limitation of enzyme instability. By using simple deep eutectic solvents such as choline chloride/sorbitol, significant stabilization of the biocatalyst has been achieved leading to more robust reactions while using environmentally more acceptable solvents as compared to ionic liquids.

Full text of DOI:10.1039/c7ra00805h

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Chemoenzymatic epoxidation of alkenes with
Candida antarctica lipase B and hydrogen peroxide
in deep eutectic solvents†
Cite this: RSC Adv., 2017, 7, 12518
a
b
a
c
b
*
Pengfei Zhou, Xuping Wang, Bo Yang, Frank Hollmann and Yonghua Wang
Epoxides are important synthetic intermediates for the synthesis of a broad range of industrial products. This
study presents a promising solution to the current limitation of enzyme instability. By using simple deep
eutectic solvents such as choline chloride/sorbitol, significant stabilization of the biocatalyst has been
achieved leading to more robust reactions while using environmentally more acceptable solvents as
compared to ionic liquids.
Received 19th January 2017
Accepted 16th February 2017
DOI: 10.1039/c7ra00805h
rsc.li/rsc-advances
reported that ionic liquids (ILs) could substantially improve the
performance of chemoenzymatic Baeyer–Villiger and epoxida-
tion reactions.24 The authors suggested a two-fold effect of
hydrogen-bond-donor-ILs in the reaction: rst by stabilizing the
biocatalyst and second, by accelerating the reaction through
solvent-activation of the peracid.
Though frequently termed ‘green solvents’ (mostly due to
their non-volatility), ILs are actually questionable from an
environmental point-of-view.25 For example, toxicity issues can
impair the environmental friendliness as well as the sometimes
rather complex and resource-consuming synthesis (vide infra).
Therefore, it is not astonishing that current research efforts
focus on environmentally less demanding substitutes such as
(natural) deep eutectic solvents (DESs).
Introduction
Epoxides are important synthetic intermediates in the produc-
tion of many industrial products.1 Next to established chemical
syntheses such as the Prileshajev epoxidation using stoichio-
metric peracids2 or metal-catalyzed epoxidations,3,4 enzymatic5–9
and chemoenzymatic methods10–12 have also gained relevance.
Particularly, the latter methods are attractive due to the broad
availability of hydrolases. In essence, chemoenzymatic methods
rely on the in situ formation of a reactive peracid making use of
the ‘perhydrolase’ promiscuous activity of many lipases. The
peracids formed react with the alkene forming the product of
interest and re-forming the carboxylic acid, which enters a new
catalytic cycle (Scheme 1).13
The number of studies evaluating DESs as more environ-
mentally acceptable alternatives to ILs is steadily increasing.26
For example, benecial effects of DESs on lipase-catalysed
esterication reactions have been reported.27–29 Inspired by
these very promising reports, we set out to investigate the
possible benecial effects of DESs on the chemoenzymatic
epoxidation reaction.
A broad range of hydrolases has been investigated for the
perhydrolysis of carboxylic acids or their esters with hydrogen
peroxide to produce epoxides.14–18 Among them the lipase B
from Candida antarctica (CalB), immobilized onto an acrylic
resin (tradename Novozym 435), is probably the most-widely
used biocatalyst.19 Several studies dealing with lipase-
catalyzed in situ peracid formation to promote the Prileshajev
epoxidation underline the preparative potential of this
approach.20–23
In recent years, it has become clear that CalB suffers from
a pronounced instability against the harsh conditions of the
chemoenzymatic epoxidation reaction as compared to the
‘natural’ esterication reactions. Arends and coworkers
aSchool of Bioscience and Bioengineering, South China University of Technology,
Guangzhou 510006, P. R. China
bSchool of Food Science and Engineering, South China University of Technology,
Guangzhou 510640, P. R. China. E-mail: yonghw@scut.edu.cn; Fax: +86 (0)20 8711
3842; Tel: +86 (0)20 8711 3842
Scheme
1 Chemoenzymatic epoxidation reaction using in situ
cDepartment of Biotechnology, Del University of Technology, Van der Maasweg 9,
generated peracids. In the first step, lipase-catalyzed perhydrolysis of
a carboxylic acid with H2O2 forms the corresponding peracid, which
then, in a non-enzymatic Prileshajev reaction forms the epoxide and
the (catalytic) carboxylic acid.
2629HZ, Del, The Netherlands
† Electronic supplementary information (ESI) available. See DOI:
10.1039/c7ra00805h
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Results and discussion
In a rst set of experiments, we evaluated the inuence of
various DESs of the efficiency of the chemoenzymatic epoxida-
tion of 1-octadecene as a model reaction (Table 1).
From the nine DESs chosen for this experiment, the amine-
based DES gave the poorest results. Essentially product forma-
tion ceased already aer approx. 6 h. Possibly, inactivation of
the enzyme (maybe due to deprotonation of structurally essen-
tial amino acid residues) accounted for this behavior. Polyol-
based DESs gave signicantly higher robustness and conse-
quently also higher product titers. Hence, ChCl/sorbitol as
solvent resulted in more than 70% conversion of the starting
material. This effect has also been observed by Arends and co-
workers who have pointed out the importance on hydrogen-
bond-donating cosolvents (ILs) on the stabilization of the
protein structure.24 Similarly, Diego et al. have emphasized the
importance of polyols such as sorbitol on protein structure.30
Encouraged by these results, we became interested in shed-
ding some more light on the benecial and detrimental effect of
amine-based or polyol-based DESs on the stability of the bio-
catalyst. Therefore, the apparent half-life times of CalB in the
presence of different solvents were determined (Fig. 1). In
accordance to our previous observation,31 the amine-based
DESs signicantly reduced (as compared to buffer as incuba-
tion solvent) the stability of CalB over the entire temperature
range investigated whereas the polyol-based DESs signicantly
increased the stability of the biocatalyst.
Fig. 1 CalB stability (displayed as half life time) at different tempera-
tures in the presence of buffer, ChCl/urea and ChCl/sorbitol.
elements disappeared at the benet of random coil. On the
contrary, secondary structure elements were almost entirely
preserved (as compared to the freshly dissolved enzyme) upon
incubation of the enzyme in ChCl/sorbitol. This result is also in
agreement with our previous study.31 Hence, we conclude that
the increased stability of the enzyme was due to the preserva-
tion of its structural integrity in ChCl/sorbitol.
Next, the key parameters effecting the chemoenzymatic
epoxidation reaction; particularly the inuence of the reaction
temperature, the octanoic acid concentration and the hydrogen
peroxide concentration were investigated (Fig. 2).
Quite expectedly, initial this reaction rate increased linearly
with temperature (Fig. 2A). Hence, the rate-limiting step may be
diffusion of either the enzyme substrates (octanoic acid and/or
The effect of the single solvents on the structural integrity of
CalB was investigated in some more detail using circular
dichroism spectroscopy (CD). As shown in Table 2, the relative
amount of secondary structure elements within the enzyme
decreased to some extent aer incubation in phosphate buffer
for 24 h, while in ChCl/urea almost all secondary structural
H2O2) or products (peroctanoic acid). It is worth pointing out
32
¨
here that in similar studies Tornvall et al. reported a sharp
decrease of the enzyme activity at 60 ꢀC. This underlines the
stabilizing effect of ChCl/sorbitol on the enzyme.
The initial rate of the overall reaction showed a saturation-
type behavior with respect to the concentration of octanoic
acid used (Fig. 2B). Above 1.6 mmol of octanoic acid, no
signicant increase of the initial rate was observed. This may be
due to the Michaelis–Menten-type kinetics of the lipase-
catalyzed perhydrolysis reaction with octanoic acid. However,
it should be pointed out that in these experiments we could
Table 1 Epoxidation of 1-octadecene in different DESsa
Conversion
(%)
Table 2 Secondary structure percentages of CalB after incubation in
different media
Entry
Solvents (molar ratio)
1
2
3
4
5
6
7
8
9
10
ChCl/urea (1 : 2)
30.2
13.9
37.7
56.7
65.1
72.4
58.4
65.3
56.2
62.5
a-
helix
[%]
b-
strand
[%]
ChCl/acetamide (1 : 2)
ChCl/ethylene glycol (1 : 2)
ChCl/glycerol (1 : 1)
ChCl/xylitol (1 : 1)
ChCl/sorbitol (1 : 1)
ChCl/xylose/water (5 : 2:5)
ChCl/glucose/water (5 : 2:5)
ChCl/sucrose/water (5 : 2:5)
Phosphate buffer (pH6.0, 50 mM)
Turn
[%]
Random coil
[%]
Medium
Initial CalBa
KPi bufferb
ChCl/ureac
ChCl/
19.8
12.3
2.2
13.4
17.5
1.3
31
35.8
36.7
62.2
32
33.5
34.3
32.5
16.6
19.1
sorbitold
a
Determined directly aer complete dissolution of the enzyme.
Conditions: CalB incubated in 50 mM pH 6.0 phosphate buffer.
a
b
c
Conditions: octadecene (1.6 mmol), octanoic acid (1.6 mmol) and
H2O2 (1.6 mmol added as 30% w/w solution) were reacted in different
DESs at 40 ꢀC using Novozym 435 (100 mg) as catalyst for 24 h with
magnetic stirring (300 rpm).
d
Conditions: CalB incubated in ChCl/urea and. Conditions: CalB
incubated in ChCl/sorbitol at 30 ꢀC for 24 h.
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the nominal concentration. Further experiments clarifying this
issue are currently underway.
We also evaluated the substrate scope of this partially opti-
mized reaction system. As shown in Table 3, a range of (ali)
cyclic alkenes as well as styrene derivates were converted in
good to excellent conversions in high selectivity as conrmed by
NMR analysis of the isolated products (see ESI† for details).
Only trace amounts (is any) of possible degradation (isomeri-
zation or hydrolysis) products were detectable.
The performance of the proposed chemoenzymatic reaction
system using ChCl/sorbitol as ‘performance additive’ compares
well with similar reactions reported in the literature.31 For
example, the conversion of 1-octadecene in aqueous reaction
media was 68% or 30% using the lipase from Penicillium cam-
emberti33 or the lipase from Malassezia globosa,34 respectively. In
a three-phase system of water/methyl dichloride/ionic liquid,
the conversion of cyclohexene was 41%.18 Therefore, the new
oxidation system proposed here represents
approach for preparative epoxidation reactions.
a promising
To further understand the molecular basis of the perhy-
drolysis reaction we modelled octanoic acid and H2O2 into the
active site of CalB (Fig. 3). Carbonyl atom of the octanoic acid is
bound in the oxyanion hole of the enzyme by two hydrogen
bonds to the amide nitrogens of Gln106 and Thr40. The
distance between carbonyl atom of octanoic acid and Og of
˚
Ser105 is 2.9 A, which is facilitate to nucleophilic attack
carbonyl group by Ser105 in active site to form an acetyl-enzyme
intermediate. Simultaneously, H2O2 is stabilized in the active
site by Gln157, Asp134 and His224. Then, hydrogen peroxide
attacked acetyl-enzyme intermediate to achieve perhydrolysis
reaction. This mechanism is similar to previous reports.33–35
Table 3 Substrate scope of the optimized chemoenzymatic epoxi-
dation systema
Fig. 2 Effects of temperature (A), molar ratio of octanoic acid to 1-
octadecene (B) and molar ratio of hydrogen peroxide to 1-octadecene
molar ratio (C) on the epoxidation of 1-octadecene.
demonstrate that octanoic acid performs as catalyst (TN ¼ 3),
pointing towards a truly catalytic system. Nevertheless, for all
further experiments we used a molar ratio of 1 : 1 (acid : alkene)
in order not to impair the overall reaction rate. Again, the
maximal conversion reached in these experiments was
approx. 70%.
Reaction time
[h]
Conversion
[%]
Product
24
11
82b
85
24
11
24
97
72
90
Interestingly, the amount of hydrogen peroxide applied to
the reaction system had almost no inuence on the initial rate
of the reaction (which may be explained by a comparably low KM
value for H2O2) (Fig. 2C). But it had a very signicant inuence
on the overall conversion reached. At a nominal molar ration of
1 : 1 (H2O2 to alkene) the maximal conversion observed in all
experiments so far was approx. 70%. However, already at
a molar ratio of 2 : 1 (H2O2 to alkene) full conversion was ach-
ieved. We believe that the most likely explanation for this
observation may be that the active H2O2 content of the stock
solution may have been signicantly lower (approx. 70%) than
11
90
a
General conditions: 0.4 g ChCl/sorbitol, 100 mg Novozym 435,
1.6 mmol octanoic acid, 1.6 mmol alkene and 3.2 mmol 30 wt% H2O2
at 40 ꢀC with magnetic stirring 300 rpm. b T ¼ 30 ꢀC.
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compared to [BMIM][BF4] (30 steps) the synthesis of ChCl/
sorbitol with only 10 steps is signicantly less complex.
Furthermore, most of the solvent (55% w/w) of ChCl/sorbitol
originates from renewable resources. Of course, only a full life
cycle assessment (LCA) will be suitable to holistically compare
the environmental impact of the solvent syntheses and the
chemoenzymatic reactions, but we hold the results from this
preliminary analysis to be very encouraging.
Conclusions
In the present study, it has been demonstrated that DESs
represent a true alternative to the commonly used ILs to facili-
tate the chemoenzymatic epoxidation of alkenes. The system
excels particularly by the lower environmental impact of the
cosolvents (DESs) used as compared to ILs. This advantage,
however, does not come with an impaired performance
compared to classical ILs. The practical applicability and effi-
ciency of the current system is at least as good as the one of the
systems of the state-of-the-art. Therefore, we are convinced that
exciting future developments will arise from the application of
DESs to chemoenzymatic epoxidation reactions.
Fig. 3 The mode of CalB (PDB ID: ILBT) catalyzed epoxidation
mechanism. The atom of hydrogen, oxygen and nitrogen are shown in
white, red and blue, respectively. Hydrogen bonds are shown in yellow
dash with distances in angstroms.
Finally, we performed a preliminary evaluation of the envi-
ronmental impact of the chemoenzymatic epoxidation reaction.
For this, the Sheldon's E-factor (environmental factor) analysis
was used (eqn (1))36,37 and compared our chemoenzymatic
epoxidation of styrene with a similar reaction reported by
Experimental sections
Materials
Arends and coworkers.24
X
Candida antarctica lipase B (CalB, Novozym 435-immobilized on
a polyacrylate resin) was obtained from Novo Nordisk (Den-
mark). The 30% (w/w) hydrogen peroxide, choline chloride
(98%), urea (99%), acetamide (99%), ethylene glycol (98%),
glycerol (99%), xylitol (98%), D-sorbitol (98%), D-xylose (98%), D-
(+)-glucose (99.5%), sucrose (ACS grade), 1-hexene (99%),
cyclohexene (99%), 1-decene (99.5%), 1-octadecene (95%),
styrene (99%), a-methylstyrene (99%), cyclohexene oxide (98%)
and styrene oxide (98%) were bought from Aladdin Chemistry
Co., Ltd (Shanghai, China). 1,2-Hexylene oxide (98%), decene
oxide (98%), octadecene oxide (99%) and a-methylstyrene oxide
(97%) were obtained from TCI (Japan). All other reagents were
of analytical grade.
mðwaste productsÞ ½kgꢁ
mðproductÞ ½kgꢁ
E-factor ¼
(1)
Eqn (1) calculation of Sheldon's E-factor.
It becomes clear from Table 4, that the solvent (either ChCl/
sorbitol or [BMIM][BF4]) has a very signicant impact on the E-
factor of the reaction contributing 31% or even 75% to the total
value, respectively.
Given this importance of the solvents, also their upstream
processing should be considered. Following Jessop's approach
of evaluating the environmental impact of solvent synthesis
based on the synthesis trees38 we compared those for [BMIM]
[BF4] and ChCl/sorbitol (Fig. S1†). This comparison reveals that
Preparation DESs
Deep eutectic solvents were formulated in different molar ratios
of quaternary ammonium salt (choline chloride) to hydrogen
bond donors. The eutectic mixtures were prepared by rotary
evaporation of the two components at 80 ꢀC in water bath until
a homogeneous transparent liquid was formed.
Table 4 E-factor analysis
Entry
DESs systema,b
ILs systema24
0.08 g (1) 40%
Non-converted
(styrene) conversion (%)
CalB (biocatalyst)
Octanoic acid
0.016 g (0.09) 90%
0.1 g (0.58)
0.23 g (1.35)
0.4 g (ChCl/sorbitol)
(2.35)
0.56 g (3.29)
0.17 g
0.01 g (0.13)
0.029 g (0.2)
1 g ([BMIM][BF4])
(12.5)
0.14 g (1.75)
0.08 g
Stability of enzyme
Puried CalB enzyme was added into 50 mM phosphate buffer
pH 6.0, DESs ChCl/urea or ChCl/sorbitol incubated at temper-
ature from 25 ꢀC to 70 ꢀC for 12 h. The samples were extracted
from reaction mixture at periodically, and then the perhy-
drolysis activity was followed spectrophotometrically at 290 nm
as described by Peter Bernhardt.39 The tests were carried out in
96-well microtiter plates with a reaction of volume 100 mL (80 mL
assays solution to 10 mL samples and 10 mL hydrogen peroxide
Solvent
H2O/H2O2
Product
E-factor
7.7
16.7
a
Numbers in parentheses represent the individual E-factor
b
contributions (i.e. g component ꢂ g product ꢃ 1). Results taken
from Table 3.
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ꢀ
in 0.1 M pentanoic acid buffer pH 5.0) at 40 C for 5 minutes 2014AA093514, 2014AA093601) and Science and Technology
using microplate reader Cytation™ 5 (BioTek, USA). The blank Planning project of Guangdong province (2014B020204003,
experiments were carried out under the identical conditions 2015B020231006).
adding inactived enzymes. All tests were performed in triplicate.
Notes and references
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