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J Appl Biol Chem (2016) 59(1), 57−62
http://dx.doi.org/10.3839/jabc.2016.011
Online ISSN 2234-7941
Print ISSN 1976-0442
Original Article: Food Science/Microbiology
Effect of Fermentation on the Antioxidant Activity of
Rice Bran by Monascus pilosus KCCM60084
Jinhua Cheng · Bong-Keun Choi · Seung Hwan Yang* · Joo-Won Suh*
Received: 13 November 2015 / Accepted: 21 December 2015 / Published Online: 31 March 2016
© The Korean Society for Applied Biological Chemistry 2016
Abstract In this study, we optimized fermentation conditions
for the solid state fermentation of rice bran with Monascus pilosus
KCCM60084, and the antioxidant activities were investigated.
Optimal fermentation conditions were determined by the production
of Monacolin K, a functional secondary metabolites with cholesterol
lowering activity. The highest Monacolin K production were 2.88
mg/g observed on day 10 with 45% moisture content in the
substrate when inoculated with 5% inoculum (w/w). Reducing
power, iron chelating activity and ABTS+ radical scavenging activity
were significantly enhanced after fermentation by 60, 80, and
38% respectively. Furthermore, the content of total flavonoid were
found to be increased by 4.58 fold. Based on these results,
Monascus-fermented rice bran showed strong possibility to be
used as a natural antioxidant agent due to its enhanced antioxidant
activity.
Keywords Antioxidant · Monacolin K · Monascus pilosus ·
Rice bran · Solid state fermentation
Introduction
Rice bran, which constitutes about 10% of the weight of whole
rice, is a byproduct in rice milling process. It is composed of
pericarp, aleurone, subaleurone, seed coat, and nucellus, along
with germ and a small portion of endosperm (Salunkhe et al.,
1992; Hargrove, 1994; Hu et al., 1996). Although varies in cultivars,
rice bran generally contains 12–22% oil, 11–17% protein, 6–14%
fiber, 10–15% moisture, and 8–17% ash, along with many
functional compounds including phenolic acids, flavonoids,
anthocyanins, tocopherols, -oryzanol and phytic acid etc. (Goufo
and Trindade, 2014; Sharif et al., 2014).
In spite of its high neutraceutical content, rice bran is being
used mostly in oil manufacturing, production of fertilizers, animal
feed and the cosmetic industry. The greatest restriction to the use
of rice bran as a food ingredient is its instability during storage.
Upon milling, the oil is exposed to lipases, causing rapid
breakdown to free fatty acids, at 5–7% of the weight of oil per
day. Hence, due to the naturally occurring enzymatic activity and
subsequent hydrolytic rancidity, it is necessary to stabilize the rice
bran by suitable techniques for controlling these undesirable
reactions. Moreover, phenolic acids, which are considered as the
major compounds for antioxidant activity in rice bran, are bound
through an ester linkage to the cell wall (Faulds et al., 1999), and
cannot be absorbed directly by humans.
The fungi of the genera Monascus, have been used for food
fermentation especially to make red yeast rice in Eastern Asia for
several centuries. Monascus-fermented products are developed as
popular functional foods for the prevention of cardiovascular
disease due to the production of Monacolin K, a cholesterol
lowering agent (Endo, 1979). Furthermore, Monascus species
were reported to produce diverse secondary metabolites with
biological functions, including a group of pigments (monascin and
ankaflavin), hypotensive agent (γ-aminobutyric acid), anti-
inflammatory compounds (Monasnicotinates), antioxidant compounds
including dimerumic acid and antibacterial compounds (Wong
and Bau, 1977; Aniya et al., 2000; Chuang et al., 2011; Wu et al.,
2011; Lee and Pan, 2012). In recent studies, other food materials
J. Cheng · J.-W. Suh
Division of Bioscience and Bioinformatics, College of Natural Science,
Myongji University, Cheoin-gu, Yongin, Gyeonggi, 449-728, Republic of
Korea
B.-K. Choi
NutraPham Tech, Giheung-gu, Yongin, Gyeonggi 446-916, Republic of
Korea
S. H. Yang · J.-W. Suh
Center for Nutraceutical and Pharmaceutical Materials, Myongji
University, Cheoin-gu, Yongin, Gyeonggi, 449-728, Republic of Korea
S. H. Yang
Interdisciplinary Program of Biomodulation, Myongji University, Yongin,
Gyeonggi, 449-728, Republic of Korea
*Corresponding authors (S. H. Yang: ymichigan@mju.ac.kr;
J.-W. Suh: jwsuh@mju.ac.kr)
This is an Open Access article distributed under the terms of the Creative
Commons Attribution Non-Commercial License (http://creativecommons.
org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use,
distribution, and reproduction in any medium, provided the original work is
properly cited.
58 J Appl Biol Chem (2016) 59(1), 57−62
(i.e. soybean and dioscorea) have also been fermented with
Monascus, and the level of monacolin K and the antioxidant
capacities were highly increased (Chiang et al., 2011; Pyo and
Seong, 2009). However, despite reports on the health benefits of
rice bran, the fermentation by Monascus on rice bran have not
been studied yet.
Fermentation is a simple technique for the long-term storage of
food, and production of bioactive compounds. Particularly, solid
state fermentation by yeast and fungus is traditionally used for
diary food preparation in East Asia. Recently, many studies have
been carried out to increase the utilization of rice bran for functional
use through solid state fermentation. Rice bran fermented with
Rizhopus oryzae enhanced the antioxidant activity and the content
of phenolic acid, especially ferulic acid (Schmidt et al., 2014).
Moreover, fermentation with Saccharomyces boulardii generates
novel metabolite profiles, and renders a novel bioactivity that can
reduce the growth of human B lymphomas (Ryan et al., 2011).
Here, we investigated and report the optimized conditions for
fermentation of rice bran with Monascus pilosus, the conversion
of polyphenol composition, and their antioxidant activity.
Materials and Methods
Solid state fermentation of rice bran with Monascus pilosus.
Rice bran was purchased at the local market in Yongin City,
Korea, and stored at −20oC before use. Monascus pilosus was
obtained from the Korean Culture Center of Microorganisms. The
moisture content of rice bran was adjusted to 35, 40, 45 and 50%
by adding water and mixed thoroughly; it was determined by a
moisture content meter. One hundred gram of rice bran was put in
a 1000 mL Erlenmeyer flask and autoclaved at 121oC for 20 min.
The fungus was cultivated on potato dextrose agar at 25oC for
72 h. An agar block (1×1 cm) with mycelium was cut and
inoculated into Mizutani medium (Kim et al., 2010) and cultivated
for 48 h. The mycelium was then homogenized in a Waring
blender and inoculated into rice bran at inoculation ratio of 1, 2,
5, and 10% (v/v) respectively. The fungus was cultivated at 25oC
for 10 days, harvested and dried at 50oC for 18 h.
Preparation of crude extract. Non-fermented rice bran (RB) and
Monascus-fermented rice bran (MRB) were dried at 50oC for
18 h, and ground to powder. Each 1 g of powder was extracted
with 10 mL of 70% ethanol at room temperature, with occasional
shaking for 24 h. The suspension was then centrifuged at 6,500
rpm for 15 min, and the supernatant was filtered through 0.2 µm
polytetrafluoroethylene filter before analysis.
Determination of monacolin K in fermentation products.
Standard Monacolin K was purchased from sigma (St. Louis, MO,
USA), and the acid form of Monacolin K was made according to
Friedrich et al. (1995). Content of monacolin K in fermented
products was determined by using high performance liquid
chromatography (HPLC). Analysis was performed using a YMC
ODS column (250 mm×4.0 mm; 5 µm) connected to binary
HPLC pump (Waters 1525) at a flow rate of 1.0 mL/min. The
mobile phase consisted of solvent A (0.5% trifluoroacetic acid in
water) and B (100% acetonitrile). The linear gradient solvent
system was programmed as follows: 0–15% B (45 min), 15–30%
B (15 min), 30–50% B (5 min), 50–100% B (5 min), and 100–0%
B (10 min). The photodiode array detector was set to 237 nm, and
the injection volume of sample was 10 µL. The content of
monacolin K was expressed as µg of monacolin K per g of dry
weight (dw).
Reducing power. Reducing power was determined according to
the method of Oyaizu (1986). Each extract (2.5 mL) was mixed
with 2.5 mL of 200 mM sodium phosphate buffer (pH 6.6) and
2.5 mL of 1% potassium ferricyanide, and the mixture was
incubated at 50oC for 20 min. After cool down, 2.5 mL of 10%
trichloroacetic acid (w/v) was added, and the mixture was
centrifuged at 6,500 rpm for 10 min. The upper layer (5 mL) was
mixed with 5 mL of deionized water and 1mL of 0.1% ferric
chloride, and the absorbance was measured at 700 nm against a
blank. A higher absorbance indicates a higher reducing power.
Ascorbic acid was used as positive control.
Scavenging ability on DPPH• radicals. The scavenging activity
of DPPH• (1,1-diphenyl-2-picryl-hydrazyl) free radical was
determined by the method of Gyamfi et al. (1999). Each extract
(50 µL) was mixed with 200 µL of DPPH• methanolic solution
(100 µM). The mixture was shaken vigorously and left to stand
for 30 min in the dark, and the absorbance was then measured at
517 nm against a blank. Ascorbic acid was used as a positive
control. The scavenging activity was expressed by the following
formula:
DPPH• scavenging activity =(1−As/A0)×100%,
where As is the absorbance of sample, A0 is the absorbance for
blank.
ABTS+ radical cation scavenging assay. Determination of
ABTS+ radical scavenging activity was modified from Re et al.
(1999). Briefly, ABTS+ was generated by oxidation of 7 mM
ABTS+ with 2.45 mM potassium persulfate, and then stored in a
dark place at room temperature for 12−16 h. The ABTS+ stock
solution was then diluted with deionized water to OD734=0.7
before use. Each extract (20 µL) was mixed with 1mL of ABTS+
solution. The mixture was shaken vigorously and left to stand for
3 min in the dark, and the absorbance was then measured at 734
nm against a blank. Ascorbic acid was used as a positive control.
The scavenging activity was expressed by the following formula:
ABTS+ scavenging activity =(1−As/A0)×100%,
where As is the absorbance of sample, A0 is the absorbance for
blank.
Chelating ability on ferrous ions. Chelating ability was
determined according to the method of Dinis et al. (1994). Since
the antioxidant activity of rice bran was very high, the extract was
diluted 10 fold in 70% ethanol before analysis. Each diluted
extract (1 mL) was mixed with 3.7 mL methanol and 0.1 mL of
2 mM ferrous chloride. To initiate the reaction, 0.2 mL of 5 mM
ferrozine was added to the mixture. After 10 min at room
J Appl Biol Chem (2016) 59(1), 57−62 59
temperature, the absorbance of the mixture was determined at 562
nm against a blank.
Determination of total phenolic content. The total phenolic
content was determined using a modified Folin-Ciocalteu method
with slight modification (Lee and Pan, 2012). Folin-Ciocalteu
reagent was diluted 5 fold by adding deionized water. A 1 mL
aliquot of the extract was mixed with 1 mL of diluted Folin-
Ciocalteu reagent and 1 mL of 10% Na2CO3. The mixture was
allowed to stand at room temperature for 1 h, and the absorbance
was measured at 700 nm wavelength. The total phenolic content
was expressed as mg gallic acid equivalent (GAE)/100 g of MRB.
The data presented is the average of three independent experiments.
Determination of total flavonoid content. Total flavonoid
content was determined by the method of Cheng et al. (2015). A
1 mL aliquot of the extract was transferred into 10 mL test tube,
then 0.1 mL of 10% aluminum nitrate, 0.1 mL of 1 M potassium
acetate and 4.3 mL of ethanol were subsequently added (Cheng et
al., 2015). The mixture was allowed to stand at room temperature
for 40 min, and the absorbance was read at 415 nm. Catechin was
used as a standard, and the total flavonoid content is expressed as
mg of catechin equivalent (CE)/100 g of MRB.
Statistical analysis of data. All the experiments were performed
at least three times. Significant differences in treatments were
analyzed by SPSS ver. 22 (IBM SPSS statistics, New York, NY,
USA) by one-way analysis of variance (ANOVA) for data comparison.
The Tukey’s test was used to compare means.
Results and Discussion
Optimization of fermentation condition by moisture content
and inoculum size. The most important secondary metabolites
produced by Monascus pilosus is Monacolin, a cholesterol-
lowering agent, which acts as a potent competitive inhibitor of 3-
hydroxy-3-methylglutaryl coenzyme A reductase (HMG-CoA
reductase). To optimize the solid fermentation condition, rice bran
was adjusted to different moisture contents, and the production of
monacolin K was monitored during the fermentation time. It has
been reported that suitable moisture content is important for the
culture of Monascus species and the production of secondary
metabolites. Excessively dry or wet conditions will inhibit the
growth of Monascus species (Lee et al., 2006). Production of
monacolin K started from day 3 of fermentation, and increased
dramatically from day 5 (Fig. 1). After 10 days of fermentation,
the content of monacolin K reached 1574, 2347, 2881 and 2579 µg/
g dry weight for the moisture content of 35, 40, 45, and 50%
respectively. After that, the content of Monacolin K didn’t change
too much, this may be due to the shortage of moisture in the
substrate. Until now, rice is traditionally used as fermentation
substrate, however the content of monacolin K is relatively low.
Recently, yam is concluded to be the best substrate for Monascus
species to produce Monacolin K, the content of Monacolin K is
2.584 mg/g (Lee et al., 2006). Compared with yam, rice bran is
much cheaper that make it more promising for industrial production.
Since the inoculum size plays a key role for production of
secondary metabolites in solid fermentation, the effect of different
inoculum sizes were investigated. Fermentation of rice bran by
Monascus pilosus lead to the production of two forms of
monacolin K: mevinolin and mevinolinic acid. After fermentation
for 10 days, the 5% inoculum showed highest monacolin K
production, reaching up to 2.881 mg/g of dry weight (Fig. 2).
Radical scavenging activity of fermented rice bran. Antioxidant
activity is related with compounds capable of protecting a biological
system against the potentially harmful effects of processes or
reactions that cause excessive oxidation, involving reactive oxygen
(and nitrogen) species (RONS). The most commonly used method
for measuring the antioxidant activity are those involving chromogen
compounds of a radical nature to simulate RONS. In this study,
DPPH• and ABTS+ were used for the detection of hydrophobic
and hydrophilic antioxidants respectively. DPPH• is a widely used
stable organic radical that can be acquired directly by dissolving
Fig. 1 Production of Monacolin K in different moisture content. Erro
r
b
ars indicate the standard deviation among the replications.
Fig. 2 Production of Monacolin K with different inoculation size after 10
days fermentation with M. pilosus. Error bars indicate the standar
d
deviation among the replications. Data points indicated with differen
t
letters are significantly different from each other at p<0.05. MK:
mevinolin; MKA: mevinolinic acid.
60 J Appl Biol Chem (2016) 59(1), 57−62
in organic solvents. The antioxidants react with it and convert it
from a violet coloured, stable-free radical, into a yellow coloured
α,α-diphenil-β-picrylhydrazine. The discolouration of the reaction
mixture can be quantified by measuring the absorbance at 517 nm,
which indicates the radical-scavenging ability of the antioxidant.
ABTS+ was generated by chemical reactions in aqueous solution
(Arnao, 2000).
The DPPH• scavenging activity of MRB did not change significantly
Fig. 3 Antioxidant activity of rice bran (RB) and Monascus-fermented rice bran (MRB). A: DPPH• radical scavenging activity, B: reducing power, C:
ABTS+ radical scavenging activity, D: Iron chelating activity. Error bar indicate the standard deviation (±SD) among the replicates. Data points
indicated with different letters are significantly different from each other at p <0.05.
J Appl Biol Chem (2016) 59(1), 57−62 61
compared with unfermented RB (p>0.05) at all the concentrations
(Fig. 3A), while the ABTS+ radical scavenging activity increased
20% after fermentation, at concentrations of 0.25, 0.5, and 1 mg/
mL (Fig. 3B). This result demonstrated that many water soluble
antioxidant compounds were produced through fermentation.
Iron chelating ability of fermented rice bran. Another strategy
to avoid ROS generation that is associated with redox active metal
catalysis, involves chelating of the metal ions. Antioxidants inhibit
the interaction between metal and lipids through formation of
insoluble metal complexes with ferrous ion (Hsu et al., 2003).
Ferrous ions are one of the most effective pro-oxidants; their
interaction with hydrogen peroxide in biological systems can lead
to the formation of highly reactive hydroxyl radicals. Ferrozine is
a ferroin compound that can quantitatively form stable magenta-
coloured complexes with ferrous ions (Fe2+). In the presence of
other chelating agents, the complex formation is disrupted and the
colour of the complex decreases. Measurement of the rate of
colour reduction therefore allows estimation of the chelating
activity of the coexisting chelator.
In this study, the iron chelating capacity assay was used to
evaluate the ability of MRB and RB to disrupt the formation of
the complexes, or to prevent the interaction between metals and
lipids. Ion chelating activity increased from 15 to 33% at the
concentration of 0.25 mg/mL, and increased from 32% to 55% at
the concentration 0.5 mg/mL (Fig. 3C). These results suggested
many lipid antioxidants are generated through fermentation by
Monascus species.
Reducing power of fermented rice bran. Reducing ability was
determined by using ferric reducing antioxidant power (FRAP).
The FRAP method is based on the reduction of a ferroin analogue:
the Fe3+ complex of tripyridyltriazine Fe(TPTZ)3+ to the intensely
blue-coloured Fe2+ complex Fe(TPTZ)2+ by antioxidants in acidic
solution.
The absorbance at OD700 for RB is 0.25, 0.30, 0.37, and 0.51 at
concentrations of 0.25, 0.5, 1, and 2 mg/mL respectively. However,
the value for MRB is 0.29, 0.38, 0.53, and 0.82 at the same
concentration. At the concentration of 2 mg/mL, the reducing
power increased about 1.6 fold (Fig. 3D). It has been reported that
Monascus fermented rice exhibits higher antioxidant activity
including reducing power, DPPH• radical scavenging ability, and
ferrous ions chelating ability (Yang et al., 2006). The enhanced
antioxidant activity was attributed to the enhanced content of
polyphenol and flavonoids. Furthermore, fermentation can produce
many small peptides and some other secondary metabolites which
are more sensitive in their reducing power and iron chelating
activity. This may be the reason that iron chelating activity is more
notable after fermentation, compared with radical scavenging
activity. It is reported that the composition of adzuki bean have
been changed after fermentation by Monascus pilosus; the content
of crude protein and crude lipid increased 26 and 5% respectively
(Cheng et al., 2015).
Content of total polyphenol and flavonoid. Total polyphenol
contents in rice bran and fermented products are 1,706 µg
GAE/g dry weight and 1,793 µg GAE/g dry weight respectively,
which shows no significant change after fermentation (p>0.05,
Fig. 4A). In contrast, the content of total flavonoid increased
remarkably from 123 µg QE/g dry weight to 518 µg QE/g dry
weight after fermentation (Fig. 4B). It has been recognized that
the total phenolic content of plant extracts is associated with their
antioxidant activities due to their redox properties, which allows
them to act as reducing agents, hydrogen donors and singlet
oxygen quenchers. The enhanced contents of flavonoids in the
MRB may contribute to the antioxidant activity in MRB. In
addition, the enhanced antioxidant activity may be due to some
metabolites produced by Monascus species during fermentation. It
is reported dimerumic acid was isolated from Moanscus anka, as
strong antioxidant compounds having scavenging and iron chelating
activity (Aniya et al., 2000). Furthermore, many secondary
metabolites, such as pigments and polysaccharides (Wang et al.,
2014), have also been reported to show antioxidant activity.
In conclusion, Monascus-fermented rice bran has strong potential
to be developed as functional food by showing binary functional
activities of cholesterol-lowering and enhanced antioxidant activity.
Fig. 4 The content of polyphenol and flavonoid of rice bran (RB) an
d
M
onascus-fermented rice bran (MRB). A: The contents of polyphenol
components B: The content of flavonoid components. Data points
indicated with different letters are significantly different from each othe
r
at p <0.05.
62 J Appl Biol Chem (2016) 59(1), 57−62
Acknowledgment This work was carried out with the support of
“Cooperative Research Program for Agriculture Science & Technology
Development (Project No. PJ01132402)” Rural Development Administration,
Republic of Korea.
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