International Research Journal of Biochemistry and Biotechnology
IRJBB
Vol. 3(1), pp. 037-043, March, 2016. © www.premierpublishers.org. ISSN: 2167-0438x
Research Article
Flavoring and medicinal values of the yellow pigment
produced by Monascus ruber 4066 strain cultivated on
static malt agar medium
*Eman Mostafa Mohamed
*Department of Botany & Microbiology, Faculty of Science, Assiut University, PO Box 71516, Assiut, Egypt.
Fax: ++2 088 234 2708, E-mail: [email protected]
The Thin Layer Chromatographic analysis (TLC) of the crud red pigment extract of M. ruber
4066 cultivated on the malt static medium well developed into three separate bands includes
red, orange and yellow pigmented bands. Sixty four volatile metabolites are detected by GC/MS
analysis which gave yellow pigment high flavoring value. The detected metabolites are
classified, chemical and physical properties are characterized, and their uses are reported. The
detected metabolites including fourteen aliphatic metabolites, twenty nine aromatic metabolites
and terpenoids, thirteen nitrogenous metabolites and also five heterocyclic nitrogenous thiols
metabolites are detected. Also they are classified into thirteen volatile and aroma groups
includes one metabolite from the each "alcohol, acid, aldehyde, amine, furan and mercapto",
two phenols, three amides, four from each "indoles and ketones", twelve terpenoids, fourteen
alkanes & alkenes, sixteen esters and three metabolites are unknown for me.
Keyword: Malt medium, bioactive metabolites, Monascus ruber, yellow pigment, GC/MS analysis
INTRODUCTION
In food industry nowadays, yellow pigments production
has two main approaches: chemical synthesis and
natural plant and microbial extraction. The chemical
synthetic dyes unsafe products such as tartrazine, due to
its safety risk, has withered in use. Meanwhile the plant
dyes extracts such as gardenia yellow, safflower yellow,
are natural and low in toxicity, but are subject to the
season change, resulting in an unstable industrial
production. Comparing with these two approaches,
microbiological fermentation for yellow pigments
production, because its few safe hazards, low cost, and
wide variety of resource choices has received increasing
attention as a promising alternative. As far as industrial
production is concerned, Monascus is one of the
microbial good resources for pigment production.
Monascus pigments in fact are mixture of red, yellow and
orange pigment with different proportions but the red
pigment is the major component (Zhou et al., 2009;
Srianta et al., 2014).
Monascus yellow pigment have many advantages and
ideal characters referred to customer due to naturally
production, independent from weather conditions,
wonderful colors with different shades, produced by
simple and non expensive fermentation methods on
"grains, agricultural and agro-industrial wastes", through
few days (7-12 days), easily extracted, high safety, more
stability and high solubility in water and alcohol. It also
has high "nutritional, flavoring or aromatic, bioactive or
medicinal" values without any bad impact on human
health and environment (Yongsmith et al., 1993; 1994;
Zhou et al., 2008; 2009, Eman 2015; Yadav et al., 2015).
Monascus yellow pigment has many industrial
applications may be wider application range than red
Flavoring and medicinal values of the yellow pigment produced by Monascus ruber 4066 strain cultivated on static malt agar medium
Eman MM.
037
pigment such as a food additive and coloring agents in
foodstuffs (edible oil, biscuits, bread, cakes, beverages,
and dairy products specially yellow cheeses and
improves the processed fruits), tissue texture, leathers,
cosmetics, perfume and soups" for centuries, folk
medicine and recently it used in "pharmacology and
medicine" (Shih et al., 2004; Moharrum et al., 2012;
Srianta et al., 2014).
The Monascus anka mutant by UV light has high yield of
yellow pigment on the different media include corn syrup,
soaking rice in water and Malt Extract Agar medium.
Surface cultivation of M. anka mutant MYM yellow
pigment gives the maximum yield under optimizing the
nutrient conditions (Zhou et al., 2009).
Monascus pigments act as the power of new
pharmaceutical products and possess numerous
bioactive
metabolites
used
as
anticancer,
immunomodulatory,
hepatoprotective,
antidiabetic,
antimicrobial,
anti-inflammatory,
anticholesterol,
anticardia vascular diseases, promote digestion,
eliminate dampness and phlegm muscle bruises,
dysentery, anthrax, and support human health agents,
also they possess an antioxidant metabolites which used
in prevention and treatments of warts, rheumatism,
female endocrine system and neuralgia from ancient
times and reported to exhibit stomachic, diuretic and
antispastic (Shih et al., 2004; Radu et al., 2011; Srianta
et al., 2014; Eman 2015).
When using toxigenic strains in pigment production the
monascidin A or citrinin are produced with the yellow
pigment under anaerobic condition. Pigment production
must occur under specific nutritional and environmental
condition for preventing the mycotoxins yield or occurs by
using the non toxigenic Monascus strains (Eman and
Abaddy 2014). The large international company must be
preparing their Monascus yellow pigment under national
standard with high safety without yellow citrinin
mycotoxins by selecting the non toxigenic strains or
improving the production conditions with citrinin level limit
of 0.2μg/g. For quality, food safety must be performed on
all supplements to ensure their identity, purity, strength,
non toxicity and composition (Zhou et al., 2008; 2009;
Srianta et al., 2014).
This investigation has been designed to study the
production, detection, separation of the yellow pigment
from M. ruber 4066 cultivated on the statically malt
medium and reported all the available information about
their metabolites found in it.
MATERIALS AND METHODS
Monascus strain
Monascus ruber was obtained from Assiut University
Mycological Centre, Assiut, Egypt. The strain of M. ruber,
AUMC 4066 (CBS 109.07), was tested for mixture of the
red and yellow pigments production and to identify their
metabolites. The tested strain was maintained on rice
medium containing rice powder 50, KH2PO4 2.5, NaNO3
3, MgSO4·7H2O 0.5 g/L distilled water 1 L and then
autoclaved at 121°C for 15 min. The fungus was then
inoculated and incubated at 30 °C and pH 6 for 10 days.
Preparation of inoculums, fermentation media and
cultivation
Monascus ruber strain is grown on PDA slants at 30°C.
To the fully sporulation (10-day-old) agar slope culture,
were cultivated in Petri dishes under strict aseptic
conditions and incubated at 28°C for 2 days.
Malt medium gave the best results for pigment
production and gave the highest number of detected
metabolites. Also the tested strain was recorded as non
toxigenic strain and completely safe, these results were
recorded by (Moharram et al., 2012). Malt medium
contained malt extract 5, yeast extract 3, glucose 5 g/ L
distilled water ( Lian et al., 2007).
Extraction of the Monascus pigment
Monascus ruber cultures were extracted with 95 %
ethanol (by volume), 50 mL/ flask, while agitating at 10
000 rpm for 24 h. The mixture was filtered through
Whatman filter paper No. 2 and dried over anhydrous
Na2SO4 (Lee et al., 2001; de Carvalho et al., 2007).
Spectrophotometric analysis
Monascus yellow pigment was determined by
spectrophotometer (Spectronic 2000 colourimeter,
Bausch and Lomb) at a visible spectrum with an apex at
370-395 nm. It separated from the mixture with red and
orange pigments by TLC analysis according to (Zhong et
al., 2015).
TLC analysis and separation of the yellow band
The crude red ethanolic extract was dried on water path
and diluted into one mL 500 μ mL were spotted on
activated TLC glass plate and run in chloroform 97%
and ethanol 3%. The developed plate gave two
separated red and yellow bands . Yellow pigments are
separated at Rf 0.73 with using ethanol aqueous solution
70% V/V. Yellow bands was crushed and dissolved
again in grade Sigma Aldrich ethanol for the GC/MS
analysis (Zhong et al., 2015).
Gas Chromatography/Mass Spectrometric (GC/MS)
analysis
Flavouring metabolites in ethanolic extracts of yellow
pigment are analyzed by GC/MS analysis. (Moharram et
Flavoring and medicinal values of the yellow pigment produced by Monascus ruber 4066 strain cultivated on static malt agar medium
Int. Res. J. Biochem. Biotechnol.
al., 2012; Zhong et al., 2015).
GC/MS Conditions
GC-MS apparatus (7890 A - 5975 B). Column:-DB-5ms
(30m X 0.250 mm X 0.250µm). Oven Program: 40°C for 3
min, then 10°C/min to 150°C for 3 min, then 10°C/min to
220°C for 6 min and then 15 °C/min to 260 °C for 15 min
Run time, 47.667 min. 2 min (Post Run) 260 °C. Pressure
7.0699 psi. Flow program on 1 mL/min for 0 min
RESULT AND DISCUSSION
Sixty four volatile metabolites are detected by GC/MS
analysis. The detected metabolites including fourteen
aliphatic metabolites, twenty nine aromatic metabolites
and terpenoids, thirteen nitrogenous metabolites and also
five heterocyclic nitrogenous thiols metabolites are
detected. They are classified into thirteen chemical
groups and includes one metabolite from the each
"alcohol, acid, aldehyde, amine, furan and mercapto", two
phenols, three amides, four from each "indoles and
ketones", twelve terpenoids, 14 alkanes & alkenes and
16 esters. Also the detected metabolites are unknown
(Table 1 and Figure 1, 2). All the recorded metabolites
are volatile and give the Monascus yellow pigment high
flavouring value according to (Moharram et al., 2012;
Eman and Abbady 2014; Zhong et al., 2015).
Sixty four detected metabolites including: Fourteen
aliphatic metabolites, twenty nine aromatic metabolites
and terpenoids, thirteen nitrogenous metabolites and five
nitrogenous thiols metabolites.
Fourteen aliphatic metabolites including one aldehyde,
two alcohols, three esters and ten alkane & alkenes
(Table 1 and Figure 1,2). Nonanal-dimethyl-acetal is
pelargonaldehyde-dimethyl-acetal. It is a clear liquid with
a crisp, citrus odor, taste and floral smell that is soluble in
water and alcohol. It is used as a flavoring and fragrance
agent in foods, precursor for production of other
chemicals such as emollients and plasticizers. Alkanes
are playing a role in fungi as a source of carbon and
energy. GC/MS analysis of fungi are recorded that
seventeen volatile compounds included alkenes, alkanes,
alcohol, aldehyde, ketone, and other organic compounds.
C8 volatiles consisted of the major volatile compositions
of the fungus includes. 1-Octen-3-ol and 3-octanone are
the main volatile compounds. 1-octen-3-ol and 3octanone could be considered as biologically active
compounds, which are not only an important factor in the
fungal flavor but also contain crucial bio-information
related to antioxidant activity (Zhang et al., 2008).
Twenty nine aromatic metabolites including one ketone,
two phenols, three alkane, eleven esters and twelve
terpenoids contains or includes six mono-cyclic
terpenoids fenchol, eucalyptol or cineole, borneol,
038
endoborneol,
camphor
and
farnesane;
five
sesquiterpene
cedrol,
chrysorrhedial,
artemisinin,
chromolaena and
seychellane and one steroid
androstenolone or prasterone. One ketone, two phenols,
three and eleven esters (Table 1 and Figure 1, 2). 2,6diisopropylnaphthalene acts as plant growth regulator
and is used in the manufacturing of pesticide. It has clear
yellowish brown colour with a faint sweet odor.
Six mono-cyclic terpenoids metabolites are detected in
yellow band including fenchol, eucalyptol is a
monoterpenoid cyclic ether, it is a colorless liquid with
flavorings, fragrances and taste which used as a flavoring
agent for baking, confectionery, meat products and
beverages, fragrances, cosmetics, medicinal products,
insecticide, insectrepellent, brands of mouthwash, cough
suppressant and body powder. Borneol and endo-borneol
are bicyclic monoterpens and used in traditional Chinese
medicine as moxa insect repellent. Camphor is a
terpenoid. It used in cooking; as a plasticizer for
nitrocellulose; ingredient for fireworks and explosive
munitions; antiinsects, used to make mothballs,
antisnakes and other reptiles; antimicrobial agent; antiitch gels and cooling gels cough suppressant and as a
decongestant. Camphor is used for minor heart
symptoms and fatigue. treat sprains, swellings, and
inflammation. antimania, anticholera. Farnesane; 2,6,10trimethyl-dodecane is responsible for the characteristic
green apple odor. Its oxidation by air gives compounds
that are harmful the fruit. The oxidation products injure
the cell membranes which eventually causes cell death in
the outermost cell layers of the fruit, resulting in a storage
disorder known as scald. α-Farnesene is also used as
insect repellent. Five sesquiterpenes which are as
antioxidant, aroma agent includes cedrol alcohol,
chrysorrhedial has pungent aldehyde, artemisinin has
lactone and acts as antimalaria, anticancer and antisweet
wormwood. Chromolaenin is used for treatment of skin
diseases such as wounds, rashes, antimicrobial, antiinflammatory, insect repellent, funcigicidal, nematicidal
and soil fertilizer agent. In general terpenes are large
class of bioactive 2ry fungal metabolites used as
fragrance and flavor industries. The terpenoids group
show significant pharmacological activities, such as antiviral, anti-bacterial, anti-malarial, anti-inflammatory,
inhibition of cholesterol synthesis and anti-cancer
activities. Antioxidant compounds are therapeutics agents
used for prevention and treatment of oxidative diseases
such as cancer, cardiovascular disease, atherosclerosis,
hypertension, ischemia/ reper fusion injury, diabetes
mellitus, neurodegenerative diseases "Alzheimer and
Parkinson diseases", rheumatoid arthritis, ageing, antiinflammatory, antitumor, antimutagenic, anticancer,
antimicrobial activities. Antioxidants agents such as
phenols, flavonoids and terpenes (Pimentel et al., 2011;
Smith 2014; Eman 2015; Yadav et al., 2015).
Fourteen nitrogenous
metabolites are
detected and
Flavoring and medicinal values of the yellow pigment produced by Monascus ruber 4066 strain cultivated on static malt agar medium
Eman MM.
039
Flavoring and medicinal values of the yellow pigment produced by Monascus ruber 4066 strain cultivated on static malt agar medium
Int. Res. J. Biochem. Biotechnol.
040
Legend: All the chemical structure and formula are collected from different internet sites includes NIST (Notional Institute of Standards and
Technology); Chem-Spider Search and share chemistry and Wikipedia, free encyclopedia https://en.wikipedia. org/wiki/DIPN.
Note: Three metabolites are detected by GC/MS and I can't to draw their chemical structure which includes [spiro(cyclopropane-1,3-tricyclo(3.2.(2,7)heptane) alka; 2-benzoyl-3-formyl-6-methyl-4,5-diphenyl-O-diacylbenzole K and dimethyl(1,1,2-trimethyl) –silanol-Alc].
Flavoring and medicinal values of the yellow pigment produced by Monascus ruber 4066 strain cultivated on static malt agar medium
Eman MM.
041
Groups
Alcohol
Aldehyde
Acid
Amine
Furan
Mercapto
Phenols
Amides
Ketones
Indoles
Terpenoids
Alkanes
Esters
Total
Table 1. Classification of the GC/MS detected metabolites into different flavouring groups in the
yellow M. ruber strain
No.
1
1
1
1
1
1
2
3
4
4
12
14
16
61
Figure 2. Flavouring and medicinal metabolites of Monascus ruber 4066 strain in yellow pigment analyzed by GC/MS
including one from each of acid, amine, ester and three
ketones. Levomethamphetamine is a sympathomimetic
vasoconstrictor which is the active ingredient used in
some over-the-counter nasal decongestants including the
formulation of Vicks Vapo Inhaler. It is useful for nasal
decongestion. Five heterocyclic nitrogenous thiols
metabolites are detected. Monascus ruber strains have
been found to be an important source of aroma
compounds, such as volatile fatty acids, esters, lactones,
aldehydes, alcohols and ketones, which play a significant
role in the production and improve the aroma flavor. Malt
extract medium has a high nutritional and aromatic
values; it contains enzymatic modifying complex
macromolecules specially starch malt grains and
proteins. The modifying starch includes glucose, maltose,
maltotriose, maltodextrines and small amounts of sucrose
and fructose; also proteins converted to amino acids,
vitamin B complex, minerals, fragnance and aroma
enhancer metabolites, enzymes and prevention of crystal
formation agents. Malt medium acts as an excellent
substrate for production of the deep red pigment of the M.
ruber and their bioactive metabolites. Esters are
responsible for the fruity fragrance. The ethanolic extract
of the red pigments have 27 esters including eight butyric
acid esters 2-ethylbutyric acid, hexadecyl ester. Different
fruity fragrance compound such as methyl butyrate "apple
fragrance", methyl butanoate pineapple, ethyl butyrate
orange, ethyl butanoate pineapple, pentyl butyrate pear
and pentyl butanoate apricot (Moharram et al., 2012).
Nemours endophytic fungi are produced many bioactive
metabolites with pharmacological activities which act as a
health-promoting benefits, antimicrobial, anticholesterols,
antiviral, immune suppressants and immune enhancer
agents These metabolites include vitamins, organic
acids, β-glucans, antibiotics, polyketides, terpenoid, and
trace elements "selenium". antioxidant metabolites such
as phenols, and terpenoids which are used as anticancer, anti-microbial, anti-inflammatory and cytotoxic
agents (Govindappa et al., 2013; Ruma et al., 2013;
Flavoring and medicinal values of the yellow pigment produced by Monascus ruber 4066 strain cultivated on static malt agar medium
Int. Res. J. Biochem. Biotechnol.
Sadrati et al., 2013; Kandasamy and Kandasamy 2014;
Smith 2014; Kumaresan et al., 2015).
Monascus bioactive metabolites are classified into eight
categories including anticancer agents "ergosterol,
ergothioneine, essential fatty acids, eicosanoids, βglucan, glycoproteins, lectins, monacolin K, pyran
derivative, phenols and triterpenoids; Anticardiovascular
disease; human health supporting agent's and health
care; terpenoids "ergosterol and flavonoids"; immune
enhancer; fragrances and flavor compounds "alcohols,
benzaldehydes, esters, lactones, phenols, terpenoids,
thiols and mercapto compounds"; antimicrobial;
antioxidant and hepatoprotective agents; anticholesterols.
Also the bioactive metabolites of the yellow mutant of the
M. pilosus strain on the fermented rice (Eman & Abaddy
2014).
Two Monascus ruber strains are cultivated on four kinds
of media and recorded 142 flavour and antioxidant
metabolites by GC/MS analysis including 48 phenolic
compounds, 39 esters, 23 alkanes and alkenes, 10
ketons, 5 from each of azole and indoles compounds, 4
terpenoids, 2 for each of amides and amines, one from
each of aldehyde, free fatty acids, pyran and cycloribitolalcohols (Eman 2015).
CONCLUSION
Yellow pigment has high flavoring and medicinal value
due to the presence of 64 volatile and flavors metabolites
which are classified into 13 aroma groups including acid,
alcohol, aldehyde, alkanes, amids, amine, furan, indoles,
ketones, mercapto, nitrothiol compounds, phenols,
terpenoids and esters. Fourteen metabolites related two
chemical groups (two phenols and twelve terpenoids)
have antioxidant activity and repotted by many Authors
and includes Two metabolites have floral odor including
nonanal-dimethyl-acetal "citrus odor" and farnesane
"green apple odor". Also three new yellow metabolites
are detected and include 2,6-diisopropyl naphthalene, 4phenylquinoline
and
2,4-dimethyl-benzo[1]quinoline
which reported as a food colouring agent.
ACKNOWLEDGEMENT
We thank (Prof MS Abaddy "Professor of organic
chemistry and Dr Iman Sayed Ahamed ES Kallaf "
lecturer Pharmacognosy dep. Fac. of Pharmacy" Assiut
University, Egypt) for the critical revision of the all
chemical structure and the chemical formula found in this
manuscript. We also thank Prof AH Moubasher and all
members of Assiut University Mycological Center for
supporting this work. I acknowledged the Analytical
Chemistry Unit, Assiut University, Egypt, for help in the
determination of metabolites found in the present study.
042
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International Research Journal of Biochemistry and
Biotechnology, 3(1): 037-043.
Copyright: © 2016 Eman MM. This is an open-access
article distributed under the terms of the Creative
Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium,
provided the original author and source are cited.
Accepted 03 December, 2015.
Citation: Eman MM (2016). Flavoring and medicinal
values of the yellow pigment produced by Monascus
ruber 4066 strain cultivated on static malt agar medium.
Flavoring and medicinal values of the yellow pigment produced by Monascus ruber 4066 strain cultivated on static malt agar medium