A new technique for promoting cyclic utilization of cyclodextrins in biotransformation
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J Ind Microbiol Biotechnol (2017) 44:1–7
DOI 10.1007/s10295-016-1856-1
BIOCATALYSIS - ORIGINAL PAPER
A new technique for promoting cyclic utilization of cyclodextrins
in biotransformation
Yanbing Shen1 · Ziqi Yu1 · Xu Yang1 · Fang Wang1 · Jianmei Luo1 · Min Wang1
Downloaded from https://academic.oup.com/jimb/article/44/1/1/5995731 by guest on 10 February 2022
Received: 10 August 2016 / Accepted: 30 October 2016 / Published online: 15 November 2016
© Society for Industrial Microbiology and Biotechnology 2016
Abstract Cyclodextrins (CDs) can improve the productiv- and cell uptake are serious challenges that influence bio-
ity of steroid biotransformation by enhancing substrate solu- transformation efficiency [6]. Cyclodextrins (CDs) are
bility. CDs can be recycled by grafting them with appropri- water-soluble cyclic oligosaccharides containing six, seven,
ate carriers. Loofah fiber is an excellent grafting material for or eight α-1, 4-linked D-glucopyranose units (α-, β-, and
CDs, and can be applied to the biotransformation and recy- γ-cyclodextrins). These compounds can selectively carry a
cling of β-cyclodextrin (β-CD). In this work, a technique for wide range of guest molecules into their hydrophobic cavity
recycling β-CD in cortisone acetate (CA) biotransforma- by van der Waals interactions and hydrogen-bond formation
tion by Arthrobacter simplex CPCC 140451 was studied. [1]. At present, CDs are extensively used as stabilizers and
Loofah fiber-grafted β-CD (LF-β-CD) was prepared using solubilizers for several steroid drugs during biotransforma-
epichlorohydrin, which is a cross-linking agent. The graft- tion to increase the reaction rate and degree of conversion by
ing yield of β-CD was 74.8 mg g−1 dried fibers. LF-β-CD forming a host–guest complex [12, 16]. However, the exten-
could increase the solubility of CA and enhance biotrans- sive application of CDs is limited because of their high cost.
formation. The initial conversion rate of CA was 1.5-fold Grafting new specific groups on cellulose molecules
higher than that of the blank group. LF-β-CD was also used through functionalization can combine the advantageous
in biocatalytic reactions for eight cycles, and it maintained properties of cellulose to form synthetic polymers. In this
the conversion ratio of CA at approximately 90%. Given the way, cellulose can serve as a backbone for chemically
above positive results, LF-β-CD can be utilized in biotech- bonded groups, which can be functionalized permanently
nological recycling applications. This method can also be [7]. As environmentally friendly auxiliaries, CDs can
applied to CD derivatives and hydrophobic compounds. also be grafted onto macromolecules with cross-linkers
for modification. Numerous cross-linking agents, such as
Keywords Loofah fiber · β-cyclodcxtrin · Graft · epichlorohydrin [22], cyanuric chloride [8], N-methylol
Biotransformation · Recycle acrylamide [14, 15], and polycarboxylic acids [11, 28],
have been utilized to graft β-cyclodextrin (β-CD) onto
natural fibers. Functional agents can be introduced to CDs
Introduction using cellulose fibers as immobilized carriers, which can
readily form inclusion complexes with various small mol-
Microbial steroid transformation is a powerful tool for gen- ecules [9]. In addition, loofah fiber is a natural, biodegrada-
erating novel steroidal drugs, while low substrate solubility ble, low-cost, non-toxic, and useful lignocellulosic material
[2]. The fiber mainly consists of cellulose, hemicellulose,
* Min Wang and lignin [13]. Loofah fiber is also an excellent carrier for
minw@tust.edu.cn immobilizing microorganisms and plant and animal cells
1
[4, 19]. This lignocellulosic material has also been utilized
Key Laboratory of Industrial Fermentation Microbiology,
for practical applications in food and wastewater treatment
Ministry of Education, College of Biotechnology, Tianjin
University of Science and Technology, Tianjin 300457, industries. Furthermore, immobilization can be achieved
People’s Republic of China by simply inoculating the cells into the reactor containing
132 J Ind Microbiol Biotechnol (2017) 44:1–7
the loofa sponge bed [18]. This technique can produce Loofah fiber was obtained from the ripped dried vegetable
CD-grafted loofah fiber, fully utilize CDs in bioconversion of Luffa aegyptica purchased from a local shop in Tianjin,
reactions, and implement recycling of CDs. China. All reagents were chromatographically pure or of
The present work aims to use a low-cost loofah fiber as analytical grade.
carrier-grafted β-CD to achieve the recycling of β-CD and to
reduce the cost of industrial applications. In this study, 1-dehy- Bacterial strain and cultivation
drogenation of cortisone acetate (CA) by Arthrobacter simplex
CPCC 140451 (ASP) [21] was selected as an experimental ASP was stored in the laboratory and prepared in two cul-
model. Loofah fiber-grafted β-CD (LF-β-CD) was prepared tivation steps in shake flasks, as previously described [17].
and used as a medium for CA biotransformation and recycling. The ASP cells were collected by centrifugation at 4 °C,
The LF-β-CD in biotransformation solutions was studied first, and the resultant was then rinsed and resuspended with
and optimum grafting conditions were then investigated. The 100 mmol KH2PO4–NaOH buffer (pH 7.2).
effect in solubility of CA, biotransformation yields, and effi-
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ciency of the grafted β-CD was evaluated. This method can be LF‑β‑CD preparation
used in recovering CD derivatives for hydrophobic compound
biotransformation and improving economic efficiency. The process for the preparation of LF-β-CD is illustrated
in Fig. 1. Loofah fiber was cut into discs with a diameter
of approximately 2.5 cm and thickness of 3–4 mm. The
Materials and methods discs were soaked in boiling water for 30 min, thoroughly
washed with tap water, and left for 24 h in distilled water.
Chemicals The water was replaced three to four times. The discs were
then oven dried at 70 °C [23].
CA standard with purity of ≥98% was kindly provided by Epoxidized loofah fiber was first obtained by reacting
Xianju Pharmaceutical Company Ltd. (Zhejiang, China). epichlorohydrin with loofah fiber and then grafted with
Fig. 1 Scheme of LF-β-CD composite preparation. (LF-β-CD was prepared using epichlorohydrin as a cross-linking agent.)
13J Ind Microbiol Biotechnol (2017) 44:1–7 3
β-CD. The pretreated loofah fiber with a certain weight was The content of β-CD grafted with loofah fiber was deter-
soaked in distilled water, and NaOH solution (0.1 mol L−1) mined using a UV–visible spectrophotometer at 552 nm.
was then added for 1 h to obtain sufficient swelling. The Phenolphthalein method was performed on the basis of the
fibers were placed in a flask filled with epichlorohydrin and decrease in the absorbance of phenolphthalein caused by
NaOH solution (10 mol L−1). The mixture was reacted at the presence of β-CD in the alkaline solution [5].
45 °C for 3 h and then washed with water until epichlo- The samples were withdrawn and extracted by ethyl
rohydrin was removed. The material was washed for two acetate and dried in vacuum. The solid extracts were then
times with acetone and dried at 50 °C. Epoxidized loofah redissolved in mobile phase (dichloromethane/ether/meth-
fiber and various β-CD concentrations were dissolved in anol at a ratio of 86:12:3.6, v/v/v) and filtered through a
10 mol L−1 NaOH solution. The mass ratio of the epoxi- 0.45 µm filter. The extracts were assayed by HPLC (Agi-
dized loofah fiber was 1:40. The mixture was shaken in a lent 1100, USA), and their absorbance was measured at
water bath for 3 h at a constant temperature of 40 °C. The 240 nm, as previously described [17].
obtained fibers were washed in distilled water until the fil-
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trate was neutral. The fibers were then dried at 50 °C.
Results and discussion
Effect of LF‑β‑CD on CA solubility
Characterization of LF‑β‑CD
Aqueous solution and a certain amount of grafted β-CD
were added to a final volume of 20 mL in 250 mL shake To recycle CD in CA biotransformation, the structure of
flasks. After the addition of CA, the shake flasks were incu- the cellulose after treatment was maintained and CD was
bated under the conditions identical to those employed in grafted with loofah fiber. The SEM images of original cel-
bioconversion (32 °C, 180 rpm). The flasks were tightly lulose fibers and alkaline solution-treated fibers are shown
sealed to avoid evaporation. After 24 h, 1 mL aliquot of the in Fig. 2. The SEM image in Fig. 2a reveals rough surface
slurry was withdrawn and filtered through a 0.2 µm filter. and an outer lignin rich layer around the fibers [3, 27]. In
The filtrate was dried in vacuum and redissolved in mobile Fig. 2b, NaOH-treated fibers contained an irregular surface;
phase (methanol/water, 80:20, v/v), and the total concentra- the inner layers of the fiber were exposed, because a large
tion of CA in the filtrate was analyzed by high-performance area of the surface material was removed. Therefore, inner
liquid chromatography (HPLC), as previously reported single fibers were exposed to some extent, because loo-
[29]. The concentration of CA was determined from the fah fiber was treated with alkali solution. This scenario is
calibration curves, which were obtained from the eluent beneficial for the β-CD grafted with loofah fiber. The SEM
solutions of standard CA. images reveal that the ordered structure of cellulose was
not disrupted. Therefore, the fiber can serve as a carrier for
Recovery of β‑CD and biotransformation grafting.
FTIR was used to examine the functional groups of
CA (0.06 g), 1 g LF-β-CD, and 1 mL of ASP cells (10 g LF-β-CD (Fig. 3). The adsorption bands at 3403, 1418,
dry weight per liter) were added to 19 mL KH2PO4–NaOH 1081, 941, and 707 cm−1 in the spectrum corresponded to
buffer at 34 °C and 180 rpm for 8 h, as previously described β-CD [20]. The region between 1335 and 1165 cm−1 was
[24]. During incubation, the samples were withdrawn and related to the C–H and C–O bond stretching frequencies.
extracted using ethyl acetate. These samples were then A peak at 2925 cm−1 was assigned to C–H vibration. The
analyzed by HPLC (Agilent 1100, USA). The experiments band ranging from 3200 to 3400 cm−1 corresponded to the
were performed in triplicates. LF-β-CD was reused for sev- vibration stretching of intermolecular and intramolecular
eral cycles to investigate reusability. hydrogen bonds of β-CD. Compared with the spectra of the
untreated cellulose fibers, those of LF-β-CD reveal a new
Analytical methods vibration at 668 cm−1, which can be assigned to the pres-
ence of a new pyran ring. Thus, CD is successfully grafted
Scanning electron microscopy (SEM, SU-1510) operated at with cellulose.
2 keV was used to observe the changes in the loofah fiber
samples before and after treatment with alkaline solution. Effect of LF‑β‑CD on biotransformation
The infrared spectroscopy curves of loofah fiber, β-CD,
and grafted β-CD were measured by Fourier transform Biotransformation experiments were conducted using
infrared spectroscopy (FTIR, Tensor-27). The dried sam- LF-β-CD. The grafting conditions shown in Table 1 were
ple was mixed with KBr powder for tableting. The analysis optimized to maximize the use of LF-β-CD. These data
results ranged from 400 to 4000 cm−1. reveal the following optimal reaction conditions: 1:20
134 J Ind Microbiol Biotechnol (2017) 44:1–7
Fig. 2 SEM images of loofah fiber. a untreated loofah fiber; b loofah fiber treated by alkaline solution
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Fig. 3 FTIR spectra of β-CD,
loofah fiber, and LF-β-CD. a
β-CD; b loofah fiber; c β-CD
graft loofah fiber
weight ratio of loofah fiber and epichlorohydrin and 1:1.3 in content of cellulose and materials used. This study uses
weight ratio of the epoxidized loofah fiber and β-CD. The loofah fiber, whereas the previous studies use cellulose
grafting yield of the grafted CD was 74.8 mg/g of oven- fiber.
dried fibers (Table 1). These conditions produced high ini- The effect of LF-β-CD on the biotransformation of
tial and final conversion rates. The reason can be due to that CA was also evaluated (Fig. 4). The group with LF-β-CD
high amount of epichlorohydrin which could enhance the yielded a higher conversion ratio than that of the control
amount of grafting β-CD, thereby improving the conversion group. Unlike the latter, the former could shorten the dura-
of CA. Moreover, the amounts of β-CD and epichlorohy- tion of fermentation. The conversion observed in this exper-
drin influenced the grafting conditions. Prior studies have iment was slightly enhanced because of the dense network
shown that the final CA conversion ratio in hydroxypropyl- structure of loofah fiber. The efficiency of substrate utiliza-
β-CD free medium can reach more than 90% [29]. Similar tion and the productivities of various fermentation processes
result is observed in that of grafted β-CD. were improved by providing a protective microenvironment
Compared with the control, the solubility of CA system [25]. The β-CD rigid ring might open after graft-
increased by twofold to 0.0396 mg mL−1 (data not shown). ing with loofah fiber. As a result, the solubility of CA was
The grafting ratio of β-CD was 7.5%. This ratio is different improved, the initial conversion rate was increased, and the
from that in literature, which is 9.7% by covalently bonding final conversion rate was enhanced. Cell contraction was
β-CD with cellulose fiber using citric acid as cross-linking facilitated by loofah fiber with a substrate, and viability was
agent [10]. The dissimilarity may be due to the difference maintained by fixing the cells [26]. However, the complex
13J Ind Microbiol Biotechnol (2017) 44:1–7 5
Table 1 Amount of grafting β-CD, initial conversion rate and conversion ratio of CA at different graft conditions (20 mL cell suspension, corti-
sone acetate 0.06 g, adding a certain amount of grafted β-CD under different graft conditions)
The weight ratio of loofah The weight ratio of Amount of grafting β-CD The initial conversion rate Conversion ratio of
fiber and epichlorohydrin epoxidized loofah fiber (mg g−1-oven dried fibers) of CA CA (%)
and β-CD (×10−2 g L−1 min−1)
Control Control – 1.05 ± 0.03 86.9 ± 0.2
1:10 1:0 – 1.06 ± 0.02 91.2 ± 0.6
1:10 1:1.3 47.1 ± 0.03 1.24 ± 0.05 93.2 ± 0.3
1:10 1:1.5 40.9 ± 0.02 1.14 ± 0.08 92.6 ± 0.2
1:10 1:2.0 42.5 ± 0.02 1.13 ± 0.01 92.4 ± 0.3
1:15 1:0 – 1.07 ± 0.02 92.2 ± 0.5
1:15 1:1.3 61.0 ± 0.11 1.28 ± 0.04 93.4 ± 0.8
1:15 1:1.5 57.1 ± 0.01 1.09 ± 0.02 92.1 ± 0.2
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1:15 1:2.0 58.2 ± 0.01 1.03 ± 0.05 92.6 ± 0.3
1:20 1:0 – 1.09 ± 0.03 91.3 ± 0.7
1:20 1:1.3 74.8 ± 0.01 1.69 ± 0.04 93.7 ± 0.7
1:20 1:1.5 60.7 ± 0.02 1.62 ± 0.02 93.2 ± 0.8
1:20 1:2.0 67.9 ± 0.03 1.55 ± 0.01 91.3 ± 0.6
Fig. 4 Transformation curve of CA at the optimum graft conditions. Fig. 5 The recycle times and conversion ratio of CA using LF-β-CD
(20 mL cell suspension, cortisone acetate 0.06 g, adding a certain as reaction media (20 mL cell suspension, cortisone acetate 0.06 g,
amount of grafted β-CD under optimum graft conditions, without adding a certain amount of LF-β-CD under optimum graft conditions)
addition of grafted β-CD system was used as a control.)
mechanisms of the increase in biocatalytic reactions caused capacity of CD inclusion diminished. The effectiveness of
by loofah fiber grafted with β-CD must be further studied. loofah fiber-fixed bacteria also gradually weaken.
After increasing the circulation of LF-β-CD, the conver-
Cyclic utilization of LF‑β‑CD sion ratio of CA was nearly the same. Assuming that the
loofah fiber was linked with CD through chemical bond-
Biotransformation experiments were performed using the ing and that β-CD was barely lost during each circulation
same LF-β-CD for eight times. After each experiment, process is reasonable. In addition, the methods of grafting
LF-β-CD was separated, washed, and recycled. As shown β-CD on loofah fiber for recycling β-CD omitted the extrac-
in Fig. 5, the grafted CD maintained a good conversion tion steps of CD and did not replenish CD in the beginning
ratio even after eight cycles of reuse. The first conversion of each circulation, as reported in literature [24]. In indus-
ratio was high, possibly because grafted β-CD formed bet- trial applications, the desired products can be isolated from
ter inclusion complexes with CA, and the substrate/prod- the by-products and substrate when the conversion ratio of
uct mass transfer resistance was small during the first trial. CA is over 90% by the recrystallization method. Therefore,
With the increase in conversion number, the conversion this finding suggests that LF-β-CD exhibits excellent reuse
ratio of CA slightly decreased. After multiple cycles, the capability.
136 J Ind Microbiol Biotechnol (2017) 44:1–7
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AA (2009) Citric acid used as a cross-linking agent for grafting
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As a potential carrier, loofah fiber is natural, low-cost, and 710. doi:10.1080/03602550902824572
non-toxic. β-CD can be grafted successfully on loofah 12. Hesselink PGM, van Vliet S, de Vries H, Witholt B (1989) Opti-
fiber, and this fiber can be used as a solid support for bio- mization of steroid side chain cleavage by Mycobacterium sp. in
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transformation. The maximum graft quantity of 74.8 mg-β-
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ditions. LF-β-CD can promote CA biotransformation. This tion of loofa (Loofah fiber) sponge as immobilization carrier for
molecule provides several advantages, including easy sepa- bioprocesses involving cellulase. J Biosci Bioeng 103:311–317.
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ral Science Foundation of China (Grant Nos. 21276196, 21406167, 16. Manosroi A, Saowakhon S, Manosroi J (2008) Enhancement of
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