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Jackfruit Seed- A Novel Substrate for the Production of Monascus

Pigments through Solid-State Fermentation

Article  in  Food Technology and Biotechnology · October 2006

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S. BABITHA et al.: Jackfruit Seed for Production of Monascus Pigments, Food Technol. Biotechnol. 44 (4) 465–471 (2006) 465

ISSN 1330-9862 original scientific paper

(FTB-1569)

Jackfruit Seed – A Novel Substrate for the Production of

Monascus Pigments through Solid-State Fermentation

Sumathy Babitha1, Carlos R. Soccol2 and Ashok Pandey1*

1
Biotechnology Division, Regional Research Laboratory (CSIR), Trivandrum 695 019, India
2
Process Biotechnology Laboratory, Federal University of Parana, CEP 81530-970, Curitiba-PR, Brazil
Received: October 25, 2005
Accepted: January 19, 2006

Summary
Solid-state fermentation was carried out using jackfruit seed powder as substrate for
the production of pigments using a fungal culture of Monascus purpureus. Due to the buff-
ering nature of jackfruit seed powder, colour of pigments produced was stable over a wide
range of initial pH of the substrate. Jackfruit seed powder with a particle size between 0.4
and 0.6 mm without any additional carbon source was found to be the best for pigment
production. Water-soluble pigments were produced when jackfruit seed powder was sup-
plemented with monosodium glutamate, soybean meal, peptone or chitin powder. The ad-
dition of external nitrogenous compounds showed a positive impact on water-soluble pig-
ment production.

Key words: jackfruit seed powder, Monascus, pigment, solid-state fermentation

Introduction Many of the studies involving Monascus have dealt with

the general culture conditions to improve pigment pro-
Recent increasing concern regarding the use of edible duction. Monascus is probably a xerophilic fungus, which
colouring agents has banned various synthetic colouring grows in a wide variety of natural substrates (3). Some
agents, which have a potential of carcinogenicity and te- natural substrates that have already been tested, besides
ratogenicity. Nowadays there is an increasing tendency rice and other cereals, are cassava starch (4,5), wheat bran,
in food industry towards natural food colours. It has wheat meal, bread meal, corn meal (6) and dairy milk
long been known that microorganisms of the genus Mo- (7). Currently, several companies are selling dry, pulver-
nascus produce red pigments, which can be used for co- ized, fermented rice product as a food colour and as a
louring foods. Monascus pigments are a group of fungal nutrient supplement with ability to reduce cholesterol
secondary metabolites called azaphilones, which have levels, and others sell the dried product or purified ex-
similar molecular structures as well as similar chemical tracts as food colours.
properties. These pigments are produced mainly in the
cell-bound state. A few examples are the orange pig- Due to high cost of currently used technology of pig-
ments such as monascorubrin and rubropunctatin, which ment production on an industrial scale, there is a need
possess the oxolactone ring, the red pigments such as for developing low cost process for the production of
monascorubramine and rubropunctamine, which are the pigments that could replace the synthetic ones. Gene-
nitrogen analogues of the orange pigments and the yel- rally, pigment production in industrial scale has been
low pigments such as monascin and ankaflavin (1). The carried out using submerged fermentation (SmF). How-
pigments can easily react with amino group containing ever, solid-state fermentation (SSF) systems appear pro-
compounds in the medium such as proteins, amino ac- mising due to the natural potential and advantages they
ids or nucleic acids to form water-soluble pigments (2). offer (8). From the literature it is evident that utilization

*Corresponding author; Phone: ++91 471 24 95 949, ++91 471 25 15 279; Fax: ++91 471 24 91 712; E-mail: pandey@csrrltrd.ren.nic.in
466 S. BABITHA et al.: Jackfruit Seed for Production of Monascus Pigments, Food Technol. Biotechnol. 44 (4) 465–471 (2006)

of a cheaply available substrate through solid-state fer- out the experiment. Experiments were carried out to
mentation can attain the objective of pigment produc- evaluate the impact of particle size of the substrate and
tion in an economically feasible way. Various agroindus- initial pH of the substrate on pigment production. Initial
trial residues such as rice bran, wheat bran, cassava, etc. pH of the substrate was achieved by adjusting the pH of
have been exploited for pigment production. However, the salt solution. Studies were also performed to evalu-
no effort has been made so far to utilize jackfruit seed as ate the influence of the addition of different carbon
a substrate for pigment production. sources (dextrose, mannitol, lactose, cassava starch, xy-
Jackfruit (Atrocarpus heterophyllus Lam.) is a mono- lose, rice, sorbitol and sucrose, at 4 and 8 % by mass)
ecious evergreen tree that is popular in several tropical and organic nitrogen sources (chitin powder, monosodi-
countries. It is also called jak-fruit, jak, and jaca in Malay- um glutamate, corn steep solid, malt extract, tryptone,
sia; nangka in the Philippines; khanun in Thailand; khnor yeast extract, soybean meal and peptone, 1 % by mass)
in Cambodia; mak mi or may mi in Laos; and mit in Viet- on growth and pigment production.
nam. It is an excellent example of a food prized in some
areas of the world and allowed to go to waste in others.
Largest of all tree-borne fruits, the jackfruit can be 8 in Pigment extraction
to 3 ft (20–90 cm) long and 6 to 20 in (15–50 cm) wide, A known amount of fermented matter was taken in
and its mass ranges from 10 to 60 or even as much as 110 a 250-mL conical flask and mixed with 90 % ethanol
lbs (4.5–20 or 50 kg) (9). There may be 100 or up to 300 (adding 5 mL of ethanol per gram of fermented matter
seeds in a single fruit. Seeds make up around 10 to 15 % on dry mass basis). The content was mixed on a rotary
of the total fruit mass and have high carbohydrate and shaker at 200 rpm for 1 h, allowed to stand for 15 min
protein contents (10,11). Seeds are normally discarded or and filtered through Whatman No. 1 filter paper. Etha-
steamed and eaten as a snack or used in some local nol extract of unfermented substrate was kept as the
dishes. blank for pigment analysis so that any coloured substan-
Thus, the main objective of this study was to inves- ce from jackfruit seed powder was subtracted from the
tigate the potential of jackfruit seed powder as a sub- pigment produced by the fungus.
strate for Monascus pigment production by solid-state
fermentation process.
Pigment estimation

Materials and Methods The analysis of pigment production was done by

measuring absorbance maxima of pigment extract by
Culture spectral analysis using a double beam spectrophoto-
meter (Shimadzu, UV 1601), taking into consideration
A culture of Monascus purpureus LPB 97 obtained from the dilution factor of the sample (12,13). Only extracel-
Laboratory of Process Biotechnology, Brazil, was used in lular pigments were considered in this study. Pigment
the present study. It was maintained on yeast extract- yield was expressed as Amax at corresponding wave-
-peptone-glucose medium, preserved at 4 °C and sub- lenght (l) per gram of dry substrate (g) (14).
cultured once in every three weeks.

Inoculum preparation Biomass estimation

M. purpureus LPB 97 was grown on YPG slants 30 The growth of fungal culture was estimated by de-
°C under static conditions. To fully sporulated (6-day- termining the N-acetyl glucosamine released by the acid
-old) agar slope culture, 10 mL of sterile distilled water hydrolysis of the chitin, present in the cell wall of the
was added and the spores were scraped under strict fungi (15). Acid hydrolysed sample (1 mL) was mixed
aseptic conditions. The spore suspension obtained was with 1 mL of acetyl acetone reagent and incubated in a
used as the inoculum (1.5·105 spores per mL). boiling water bath for 20 min. After cooling, ethanol (6
mL) was added, followed by the addition of 1 mL of
Solid-state fermentation (SSF) Ehrlich reagent and incubated at 65 °C for 10 min. After
Jackfruit seeds obtained from a local market in Tri- cooling, the absorbance was read at 530 nm against the
vandrum were used as substrate. After peeling off the reagent blank. N-acetyl glucosamine (Sigma) was used
white arils of seeds (seed coats), the seeds were sliced as the standard. When the media contained a chitin sup-
into thin chips, dried at 60 °C for 12 h and then ground. plement as nitrogen source, unfermented substrate with
A mass of 5 g of seed powder was taken into 250-mL chitin supplementation was kept as a control and this
Erlenmeyer flask and a salt solution (2 mL) containing was deduced from the estimated biomass.
(in g/L): KH2PO4 2, NH4NO3 5, NaCl 1, and MgSO4 ·7H2O
1 was added. Initial moisture was set at 65 % by adding TLC of the pigment extract
the requisite amount of distilled water. The contents of
the flasks were mixed thoroughly, autoclaved at 121 °C Crude extract was analysed by thin layer chromato-
for 20 min and cooled to room temperature. It was ino- graphy (TLC). Concentrated ethanol extracts were applied
culated with the spore suspension containing 1.5·105 to Silica Gel 60 plates (Merck, Darmstadt, Germany) and
spores per mL of M. purpureus LPB 97 and incubated at developed with a solution of chloroform/methanol/wa-
30 °C with 50 % humidity for 7 days. Unless otherwise ter (volume ratio of 90:25:4) to compare the Rf values of
mentioned, these conditions were maintained through- the pigments.
 S. BABITHA et al.: Jackfruit Seed for Production of Monascus Pigments, Food Technol. Biotechnol. 44 (4) 465–471 (2006) 467

Results and Discussion was obtained at l=469 nm, which corresponded to

orange pigments. For pH=3.5 and 4.0, the Amax shifted
The obtained results show that jackfruit seed pow- towards lower wavelength, giving the peak values at
der served as a good substrate for the growth of Mo- 445 and 394 nm, respectively. Over a wide range of pH,
nascus purpureus, which resulted in a considerable amount i.e. from 4.5 to 7.5, pigment yield showed similar ab-
of pigment production. The results reported are the av- sorption peaks around 390 and 500 nm, although with
erage of three sets of experiment values and standard varied pigment production. These results were con-
deviation <±5 %. firmed by separating the pigment extracts by TLC (Fig.
2). Spots I, II and III indicate the respective Rf values of
Effect of initial pH of the substrate
Irrespective of the set value of initial pH of the me-
dium using salt solution of varied pH, a change was no-
ticed after autoclaving the solid medium. This clearly
showed the buffering nature of the substrate (jackfruit
seed powder), which itself had a pH of 6.5 (Table 1).

Table 1. Optimization of pH of the salt solution in order to get

the desired pH after autoclaving
Fig. 2. TLC of pigment extracted from fermented substrate of
pH of the salt pH of the substrate after different initial pH
autoclaving
0.3 2
0.5 2.5
yellow, orange and red for the pigment extracts. Rf val-
ues of spots I, II and III were essentially the same for all
0.6 3 extracts, ranging from pH=4.5 to 7.5. These results indi-
0.7 3.5 cated that the same yellow, orange and red components
0.9 4 were produced during fermentation, regardless of the
1.5 4.5
initial pH of the substrate. Contaminants were not identi-
fied on TLC plates, since the spots obtained were in
1.7 5 agreement with the results of spectral analysis. This
8.4 5.5 could be attributed to the buffering capacity of jackfruit
11.5 6 seed powder. Since jackfruit seeds are a popular ingredi-
12.3 6.5
ent in many culinary preparations, the dried, pulverized
and fermented seed powder itself could be used as a
12.9 7 food colorant. Furthermore, the process involved in the
13.2 7.5 fermentation was simple and cheap. These results could
be quite significant as they open the scope of jackfruit
seed powder (which is otherwise discarded as waste) as
a potent food colorant by bringing down the production
There are reports in the literature describing the buffer-
cost of these food grade pigments.
ing nature of different agroindustrial residues (16). Set
initial pH values of the substrates were between 2.0–11.0.
At very low initial pH substrate (2.0 and 2.5), there was Effect of particle size
no fungal growth (Fig. 1). From the spectral analysis it Among the several factors in SSF processes which
was observed that for pH=3.0, the absorbance maximum are important for microbial growth and activity, the sub-
strate particle size is one of the most critical parameters
35 30
(17,18). Generally, smaller substrate particles provide a
larger surface area for microbial attack, and thus it should
30 25 be considered as a desirable factor. However, too small
w(glucosamine)/(mg/g)

particles may result in substrate agglomeration, which

Pigment yield/(A/g)

25
20 may interfere with aeration (due to less interparticle
20
15
space) and may, thus, result in poor microbial growth.
15 At the same time, larger particles provide better aeration
10 efficiency (due to increased interparticle space), but pro-
10
vide limited surface for microbial attack. Therefore, it
5 5 may be necessary to provide compromised particle size
(19). In the present study, jackfruit seed powder of dif-
0 0
2 2.5 3 3.5 4 4.5 5 5.5 6 6.5 7 7.5 ferent particle sizes was used to prepare different media,
Initial pH viz. M1 (particles <0.09), M2 (particles between 0.09 and
0.1 mm), M3 (particles between 0.1 and 0.2 mm), M4
394 nm 400 nm 445 nm 469 nm 500 nm Biomass
(particles between 0.2 and 0.3 mm), M5 (particles be-
Fig. 1. Effect of initial pH of the substrate on growth and pig- tween 0.3 and 0.4) and M6 (particle between 0.4 and 0.6
ment yield mm). Substrate moisture was set at 65 %. Results indi-
 468 S. BABITHA et al.: Jackfruit Seed for Production of Monascus Pigments, Food Technol. Biotechnol. 44 (4) 465–471 (2006)

cated that particles between 0.4 and 0.6 mm were opti- observation from the spectral analysis (Fig. 5) was that
mal for pigment production (Fig. 3). In the subsequent there was a shift in absorbance maxima for xylose, giv-
experiments, therefore, particle size between 0.4 and 0.6 ing peak values at 498 and 409 nm. Even though it did
mm of jackfruit seed powder was used for the produc- not support growth as well as other supplements, the
tion of pigments. yield of pigment with an absorbance peak at 409 nm
was close to other best carbon sources. Utilization of
carbon sources for growth appears to be strain specific
35
since for other stains of Monascus glucose and its oligo-
30 and polysaccharides were better than other carbon sour-

w(glucosamine)/(mg/g)
25
ces both for growth and pigment production (20–22).
Pigment yield/(A/g)

20

15 25 60

50

w(glucosamine)/(mg/g)
10 20

Pigment yield/(A/g)
40
5 15
30
0
M1 M2 M3 M4 M5 M6 M7 M8 M9 10
20
Particle size
5 10
Pigment yield Biomass
0 0
Dextrose Mannitol Lactose Xylose Rice Sorbitol Sucrose Cassava Control
Fig. 3. Effect of particle size on growth and pigment yield starch
Carbon source

503 nm 413 nm 498 nm 409 nm Biomass

Effect of supplementation of carbon source Fig. 5. Effect of supplementation of carbon source (4 % by mass)
Jackfruit seed powder medium was supplemented on growth and pigment yield
with additional carbon source at two different concen-
trations (4 and 8 % by mass). In our study, at 4 %, even
though dextrose supported the growth of the organism, At 8 % (Fig. 6), there was an inhibition in pigment
pigment yield was very negligible when compared to production for those samples supplemented with dex-
other carbon sources. Control itself gave the maximum trose, mannitol and lactose. Rice supplementation gave
yield for red pigment (19.5 A/g) as well as yellow pig- only a marginal increase in pigment yield (19.5 A/g for
ments (19 A/g), followed by rice supplementation with red pigment and 22.5 A/g for yellow pigment) when
a pigment yield of 18 A/g for red and 18.3 A/g for yel- compared to the control (17.9 A/g and 20.8 A/g for red
low. Even though there was an increase in the growth, and yellow pigments, respectively). Regarding yellow
pigment yield was poor when supplemented with sor- pigments, xylose gave the maximum yield (23.3 A/g)
bitol and mannitol. Lactose, cassava starch and sucrose and it should be noted that at 8 % xylose supplemen-
were found to be good supporters for pigment produc- tation resulted in the production of only yellow pig-
tion next to rice and control, except for sucrose where ments with a single absorbance peak at 413 nm (Fig. 7).
there was a reduction in growth (Fig. 4). A significant Therefore, considering both red and yellow pigments,

Fig. 4. Spectrum of pigment extracts showing the effect of additional carbon source (4 % by mass)
1 jackfruit seed powder without carbon source, 2 xylose, 3 rice, 4 lactose, 5 sucrose, 6 cassava starch, 7 sorbitol, 8 mannitol, 9 dextrose
 S. BABITHA et al.: Jackfruit Seed for Production of Monascus Pigments, Food Technol. Biotechnol. 44 (4) 465–471 (2006) 469

30.0 14

507 nm
25.0 12
40
Chitin powder

w(glucosamine)/(mg/g)
10 420 nm 509 nm
Pigment yield/(A/g)

20.0 30
MSG
8 20
15.0 Cornsteep solid
6 10
413 nm 500 nm
10.0 Malt extract
4 0
5.0 Yeast extract
2
Soybean meal
0.0 0 438 nm 502 nm
Dextrose Mannitol Lactose Xylose Rice Sorbitol Sucrose Cassava Control
starch Peptone
Carbon source
424 nm 505 nm Control
503 nm 413 nm Biomass

Fig. 6. Effect of supplementation of carbon source (8 % by mass) Fig. 8. Effect of supplementation of organic nitrogen source on
on growth and pigment yield pigment yield

Fig. 7. Spectrum of pigment extracts showing the effect of additional carbon source (8 % by mass)
1 jackfruit seed powder without carbon source, 2 xylose, 3 rice, 4 lactose, 5 sucrose, 6 cassava starch, 7 sorbitol, 8 mannitol, 9 dextrose

and since only marginal increase in pigment yield was optimal for growth, but unfavourable for pigment pro-
obtained for the best carbon source at higher concentra- duction. Spectral analysis of water extract showed that
tion, jackfruit seed powder without any supplementa- jackfruit seed powder without any addition of nitrogen
tion of carbon source can be utilized as a suitable sub- source was not able to produce any water-soluble pig-
strate for pigment production. ments. It has been reported that the addition of mono-
sodium glutamate could give rise to water-soluble red
pigments (25). In the present study, the addition of ni-
Effect of supplementation of nitrogen source
trogen sources such as monosodium glutamate, soybean
Utilization of different nitrogen sources has been meal, peptone and chitin powder gave water-soluble pig-
known to produce different pH patterns in fermentation, ments with maximum absorbance peaks at 484 and 413
which affects growth and pigment production (23,24). nm, 482 and 405 nm, 482 and 402 nm, 484 and 385 nm,
But in our study, difference in pigment yield cannot be respectively (Fig. 9), whereas only single absorbance peak
attributed to different pH pattern due to buffering na- corresponding to yellow pigment was obtained when
ture of jackfruit seed powder. From the spectral analysis, supplemented with corn steep solid, malt extract and
slight shift in absorbance maxima was observed for dif- yeast extract. Although the monascorubrin-rubropuncta-
ferent organic nitrogen sources. In our study monoso- tin mixture, which constitutes the orange pigment pro-
dium glutamate was found to be outstanding for both duced as the direct fermentation product of Monascus
red and yellow pigment production (30.8 and 25.5 A/g, species, is water-insoluble and therefore of limited util-
respectively), followed by peptone, soybean meal and ity as a food colorant, it has been reported that these
chitin powder (Fig. 8). This result was similar to the materials react with primary amines to afford red colo-
findings of Lin and Demain (21,22) who reported that rants, many of which are water-soluble (26). Therefore,
monosodium glutamate was most suitable for pigment jackfruit seed powder supplemented with required or-
production. They observed that organic nitrogen was ganic nitrogen sources could be considered as a poten-
470 S. BABITHA et al.: Jackfruit Seed for Production of Monascus Pigments, Food Technol. Biotechnol. 44 (4) 465–471 (2006)

Fig. 9. Spectrum of water extract showing the effect of additional organic nitrogen
1 monosodium glutamate, 2 corn steep solid, 3 yeast extract, 4 peptone, 5 soybean meal, 6 chitin powder, 7 malt extract, 8 control

tial substrate for the production of water-soluble Monas- 5. Y.K. Lee, Production of Monascus pigments by a solid-liq-
cus pigments. uid state culture method, J. Ferment. Bioeng. 79 (1995) 516–
518.
6. C.F. Lin, H. Iizuka, Production of extracellular pigment by
Conclusions a mutant of M. kaoling sp. nov., Appl. Environ. Microbiol. 43
(1982) 671–676.
From the results it could be concluded that jackfruit
7. A.V. Kujumdzieva, J.N. Hallet, V.A. Savov, T.V. Rasheva,
seed could be an effective substrate for the production Monascus purpureus strain producer of pigments and by-
of pigments by fungal culture of Monascus sp. The fun- -products, US patent 5627068 (1997).
gal culture did not require any additional carbon source, 8. A. Pandey, Recent developments in solid-state fermenta-
but supplementation of external nitrogen sources was tion, Process Biochem. 27 (1992) 109–117.
useful in enhancing the pigment production, especially 9. J. Morton: Jackfruit. In: Fruits of Warm Climates, J.F. Morton
water-soluble pigments. It could also be established that (Ed.), Miami, Florida, USA (1987) pp. 58–64.
by varying the fermentation conditions, the fungal me- 10. F.O. Bobbio, A.A. El-Dash, P.A. Bobbio, L.R. Rodrigues, Iso-
tabolism changed to produce yellow or red pigments in lation and characterization of the physicochemical proper-
varying concentrations, which could be significant for ties of the starch of Jackfruit seeds (Atrocarpus heterophyl-
industrial application. lus), Cereal Chem. 55 (1978) 505–511.
11. S. Kumar, A.B. Singh, A.B. Abidi, R.G. Upadhyay, A. Singh,
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nol. 25 (1988) 141–152.
SB acknowledges the award of a fellowship by the
Council of Scientific and Industrial Research, Govern- 12. S.W. Chiu, K. Poon, Submerged production of Monascus
pigments, Mycologia, 85 (1993) 214–218.
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 FTB 44 (4) 465-471.
Sjeme biljke Artocarpus heterophyllus (Jackfruit) – novi čvrsti supstrat za
proizvodnju pigmenata uzgojem gljive Monascus

Sažetak
Pigmenti iz gljive Monascus purpureus dobiveni su uzgojem kulture na čvrstoj
podlozi od praha dobivenog mljevenjem sušenog sjemena biljke Artocarpus heterophyllus
(Jackfruit). Boja dobivenih pigmenata bila je stabilna bez obzira na početnu pH-vrijednost
supstrata zahvaljujući puferskom svojstvu praha. Najbolji supstrat za proizvodnju pigmenata
bio je prah veličine čestica od 0,4 do 0,6 mm, bez dodanog izvora ugljika. Kad se prahu doda
natrijev glutamat, sojina sačma, pepton ili hitinski prah, dobiju se pigmenti topljivi u vodi.
Dodatak dušikovih spojeva pozitivno utječe na proizvodnju pigmenata topljivih u vodi.

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