JOURNAL OF CULTURE COLLECTIONS
Volume 6, 2008-2009, pp. 97-105
COMPARATIVE STUDY OF ENVIRONMENTAL AND NUTRITIONAL
FACTORS ON THE MYCELIAL GROWTH OF EDIBLE MUSHROOMS
Ahmed Imtiaj, Chandana Jayasinghe, Geon Woo Lee and Tae-Soo Lee*
Department of Biology, University of Incheon, Incheon 402-749, Korea
*Corresponding author, e-mail: [email protected]
Summary
Mushrooms are usually fleshy fungi belonging to either basidiomycota or ascomycota. The optimal culture conditions for the mycelial growth of 371 strains belonging to 9 species of edible mushrooms were investigated. The temperature
suitable for the mycelial growth was found to be 25 ºC and optimal range of temperature was 20~30 ºC. Mushrooms have a broad pH range (5~9) for their mycelial
growth but mostly favorable pH was between pH 6 and 7. Hamada, Lilly, PDA and
YM were the most appropriate nutrient media whereas Czapek Dox, Hoppkins and
Hennerberg were the most unsuitable for radial mycelial growth of mushrooms.
Among 10 different carbon sources, dextrin, fructose and sucrose were the best
while lactose and galactose were the most unfavorable ones. In carbon sources,
mycelial density was found to vary from compact to somewhat compact. The most
suitable nitrogen sources for mycelial growth were glycine, ammonium acetate and
calcium nitrate whereas the most unsuitable were histidine and ammonium phosphate. In case of glycine, mycelial density was found to vary from nearly compact to
compact but in the rest of nitrogen sources the mycelial density was rather thin.
Key words: culture conditions, edible mushroom, media, mycelial growth, nutrition
Introduction
Mushrooms are fleshy fungi belonging to
either basidiomycota or ascomycota. Some
members of mushrooms are important and
delicious items of our food menu having both
nutritive and medicinal values [2, 6]. This item
is appreciated, not only for texture and flavor,
but also for their chemical and nutritional characteristics [14]. On a dry weight basis, they
are considered to be good sources of digestible proteins (10–40 %), carbohydrates (3–21 %)
and dietary fiber (3–35 %). Mushrooms contain
all the essential amino acids [5]. This group of
fungi is an excellent source of vitamin B1 (thiamine), B2 (riboflavin), B3 (nicotinic acid), C (ascorbic acid) and biotin. Edible mushrooms in
cooked or other processed forms are nutritio-
nally sound and good dietary components suitable for vegetarians, diabetic and heart patients [4]. Mushrooms have also been reported
as therapeutic foods, useful in preventing diseases such as hypertension, hypercholesterolemia and cancer [3]. Some recently isolated and
identified compounds, originating from mushrooms, show other significant medical properties, such as immunomodulatory, liver protecttive, antifibrotic, antiinflammatory, antidiabetic,
antiviral and antimicrobial activities [10, 17, 25,
26]. The world production of different cultivated mushrooms is about 1.3 billion pounds [19]
such as Agaricus bisporus 1956, Lentinula edodes 1564, Volvariella volvacea 181, Pleurotus
spp. 876, Auricullaria spp. 485 and Flammulina
97
velutipes 285 tons in 1997 [16] The production
was increased for A. bisporus 16.1, L. edodes
25.5, Volvariella sp. 16.3, Pleurotus spp. 537.9,
Auricullaria spp. 336.1 and F. velutipes with
43.0 % in 1990, compared to 1986 [18]. It is
generally recognized that growing mycelia in a
defined medium is a rapid and alternative method to obtain fungal biomass for further use
[27]. It is also well known that the mycelial
growth of mushrooms is enhanced by different
environmental and nutritional factors. Because
of that, our study has been conducted on the
mycelial growth of 371 strains belonging to
9 species of edible mushrooms. The different
environmental (pH, temperature) and nutritional factors (media, carbon and nitrogen sources) were used to assess the optimal culture
conditions for the mycelia of mushrooms.
Materials and Methods
Collection of strains. The cultures of 371
strains belonging to 9 species of edible mushrooms such as A. bisporus, Agrocybe cylindracea, F. velutipes, Hypsizygus marmoreus,
L. еdodes, Lentinus lepideus, Pholiota adiposa, Pleurotus eryngii and Pleurotus ostreatus
were obtained from Culture Collection of Wild
Mush-room (CCWM) species, University of
Incheon, Korea. All strains obtained from CCWM
were recultured on potato dextrose agar (PDA)
medium and incubated for 10 days at 25 ºC for
further study (Table 1). Three replications were performed for each strain in different experiments.
Effect of temperature. To screen the suitable temperature for the mycelial growth the
9 species of edible mushrooms were incubated for 10 days at 5 different temperatures.
A 5 mm diameter agar plug removed from
10 days old cultures grown on PDA was placed in the centre of each plate filled with PDA.
The medium was adjusted to pH 6 and incubated for 10 days at 15 ºC, 20 ºC, 25 ºC, 30 ºC
and 35 ºC, separately. Radial growth of mycelia on each Petri dish was measured at 3 directions such as A to B, C to D and E to F
(Fig. 1). Average value of mycelial growth of
each Petri dish was calculated out of those 3
measurements. Similarly, mycelial growth was
measured of remaining 2 Petri dishes (since 3
replications were used for each strain). The
following formula was used to calculate the
mycelial growth of mushrooms.
Average mycelial growth on:
1st Petri dish (AB1+CD1+EF1) /3 = R1
2nd Petri dish (AB2+CD2+EF2) /3 = R2
3rd Petri dish (AB3+CD3+EF3) /3 = R3
Average mycelial growth of each strain is
(R1+ R2 + R3) /3 = F
Therefore, average mycelial growth of
each species is (F1+ F2+…+Fn) / n, where n is
number of strains used per species.
Fig. 1. Method of counting mycelial growth on Petri
plate.
Effect of pH. A 5 mm diameter agar plug
of an inoculum was removed with cork borer
from 10 days old cultures grown on PDA and
placed on the centre of each agar plate. The
medium was adjusted to pH 5, 6, 7, 8 and 9
with the addition of 1N NaOH or 1N HCl
before autoclaving and incubated for 10 days
at 25 ºC. The measurement of mycelial growth
was performed following the same technique
described earlier.
Screening of favorable culture media.
Ten different culture media namely Czapek
Dox, Hamada, Hennerberg, Hoppkins, Glucose peptone, Glucose tryptone, Lilly, Mushroom complete, PDA and YM were prepared
to investigate the mycelial growth of the studied mushrooms (Table 2). The media were
adjusted to pH 6 before autoclaving. After autoclaving for 15 minutes at 121 ºC, 20~25 ml
of each medium was aseptically poured into
plates. A 5 mm diameter plug of an inoculum
was removed from 10 days old culture grown
on PDA and placed in the centre of each plate
of 10 different culture media. After 10 days of
incubation at 25 ºC, measurement of mycelial
growth and density was performed as described above.
98
Table 1. List of strains used in this experiment.
Scientific
name
A. bisporus
A. cylindracea
F. velutipes
H. marmoreus
L. edodes
L. lepideus
P. eryngii
P. ostreatus
P. adiposa
No. of
strains*
IUM strain (Incheon University Mushroom)
1946
1947
1948
1955
1956
2029
2097
2102
2107
2177
2178
0562
0736
0737
1389
1403
1424
1437
1459
1497
1571
1576
1590
1663
1664
1665
1803
1811
1901
2012
2028
0008
0149
0193
0200
0222
0223
0224
0225
0239
0786
0891
0892
1047
1048
1083
1090
1093
1209
1221
1241
1242
1243
1244
1245
1246
1247
1248
1249
1250
1251
1252
1253
1258
1266
1321
1322
1323
1324
1325
1326
1327
1328
1329
1330
1331
1332
1333
1334
1335
1336
1337
1338
1339
1399
1401
1421
1504
1512
1518
1519
1524
1530
1537
1539
1540
1559
1666
1667
1668
1672
1702
1776
1780
1950
2011
2115
2124
2125
2130
2162
2164
2186
2187
1397
1406
1408
1414
1417
1502
1515
1523
1534
1551
1562
1563
1588
1591
2120
2123
2127
2129
2138
2139
2140
2142
2145
2148
2151
2153
2154
2155
2157
2160
2185
0110
0429
1254
1390
1398
1404
1405
1412
1413
1418
1439
1456
1465
1500
1503
1506
1525
1535
1555
1567
1587
1646
1647
1748
1753
1778
1827
1851
1952
1952
1953
2062
2063
2065
2104
2116
2132
2135
2136
2141
2144
2146
2149
2150
2159
2165
2167
2168
2169
2170
2171
2172
2181
0010
0119
0296
0597
0747
0759
1086
1696
1723
1736
0112
0432
1255
1383
1384
1393
1410
1415
1416
1419
1420
1435
1444
1458
1461
1462
1463
1464
1480
1483
1484
1485
1513
1517
1550
1569
1577
1578
1589
1636
1637
1653
1659
1660
1661
1662
1708
1773
1777
1804
1824
1838
1949
1994
2027
2055
2100
2106
2111
2119
2126
2137
2143
2161
2166
2173
2175
2179
0165
0199
0655
0797
1257
1306
1311
1315
1317
1318
1319
1340
1341
1342
1343
1344
1345
1346
1347
1348
1350
1351
1352
1353
1357
1358
1359
1361
1362
1363
1364
1366
1367
1368
1369
1370
1371
1372
1376
1395
1491
1494
1496
1516
1520
1521
1526
1527
1532
1556
1586
1644
1645
1651
1656
1669
1670
1671
1676
1677
1710
1721
1746
1772
1774
1775
1779
1781
1783
1932
1951
1954
2013
2033
2040
2059
2066
2101
2103
2105
2110
2131
2134
2152
2158
2176
0132
0154
0155
0170
0235
0260
0437
0533
0613
0815
0819
0820
0909
1183
1198
1203
1229
1705
1809
99
20
83
31
53
10
Total strains
*Number of studied strains per species.
Three replications were used for each strain in every experiment.
11
58
86
19
371
Table 2. Different media and their compositions used in this study.
Media* (g/l)
Composition
Agar
Cza
Ham
Hen
Hop
GP
GT
Lil
MC
PDA
YM
20
20
20
20
20
20
20
20
20
20
20
10
Asparagine
2
Dextrose
10
Ebiose
5
Hyponex
3
Glucose
50
10
10
Malt extract
5
15
Maltose
20
3
2
5
10
Peptone
10
Potatoes
Sucrose
200
30
Triptone
10
Yeast extract
3
NaNO3
3
K2HPO4
1
MgSO4
0.5
KCl
0.5
FeSO4
0.01
CaCl2
10
3
2
3
2
1
0.5
0.5
0.5
0.5
1
0.5
0.1
KH2PO4
1
0.1
KNO3
2
2
*Media: Czapek Dox (Cza), Hamada (Ham), Hennerberg (Hen), Hoppkins (Hop), Glucose peptone (GP),
Glucose tryptone (GT), Lilly (Lil), Mushroom complete (MC), Potato dextrose agar (PDA), Yeast-malt extract
(YM).
Effect of carbon and nitrogen. To screen
carbon and nitrogen sources favorable for the
mycelial growth of selected mushrooms, the
tests were performed on the basal medium [23]
supplemented separately with each of 10 carbon and 10 nitrogen sources. The basal medium
was composed of: MgSO4 - 0.05 g, KH2PO4 0.46 g, K2HPO4 - 1.0 g, thiamine-HCl - 120 μg,
agar - 20 g and distilled water - 1000 ml. To
screen carbon sources favorable for the mycelial growth, each carbon source together with
5 g of peptone was added separately to the basal medium at the final concentration of 0.1 M
and mixed thoroughly [20]. The basal medium,
which was used for screening of favorable nitrogen sources, was made of the same additives as those described by Sung et al. [23].x Each
nitrogen source together with 20 g of glucose
was added to the basal medium at the final concentration of 0.02 M [20]. In both cases, the
basal medium was adjustted to pH 6 before
autoclaving for 15 minutes at 121 ºC and poured into plates. To measure colony diameter on
the media, all plates were incubated for 10 days
at 25 ºC.x Radial growth and density of mycelia
were measured as already described.
100
Results and Discussion
Effect of temperature. The highest mycelial growth of tested mushrooms was obtained
at 25 ºC while the lowest mycelial growth was
recorded at 35 ºC. The fungi L. lepideus and
P. ostreatus like high temperature (30 ºC). The
lowest mycelial growth of these fungi appeared at 15 ºC (Fig. 2). Lee et al., 1999, and Shim
et al., 2003, reported that the mycelial growth
of Paecilomyces fumosoroseus had been expedited gradually in proportion to the rise of
temperature and the most suitable temperature was 25 ºC [12, 21]. Even though the myce-
Mycelial growth (mm)
15 ºC
lial growth of P. fumosoroseus was favored in
the range of 20 to 25 ºC and had been expedited in proportion to the rise of temperature, the
mycelial growth appeared to be suppressed at
temperatures higher than 30 ºC. Imtiaj et al.,
2007, reported that the temperature of 25 ºC
was the most suitable for the majority of mushrooms for their spontaneous mycelial growth
[11]. Sung et al., 1999, and Shim et al., 2005,
stated that the mycelial growth of Macrolepiota
procera and P. ostreatus was favored at 30 ºC,
which is in accordance with our results [22, 24].
20 ºC
25 ºC
30 ºC
35 ºC
80
60
40
20
0
Ab
Ac
Fv
Hm
Le
Ll
Pa
Pe
Po
Mushrooms
Fig. 2. Effect of temperature on the mycelial growth of different edible mushrooms. Standard deviation was
calculated for each strain and data are presented as mean values for studied strains per species:
A. bisporus (Ab), A. cylindracea (Ac), F. velutipes (Fv), H. marmoreus (Hm), L. edodes (Le), L.
lepideus (Ll), P. adiposa (Pa), P. eryngii (Pe)and P. ostreatus (Po).
Effect of pH. To screen pH values favoring growth of mushrooms, the pH range of
5~9 was observed and the best pH was found
to be 6~7. In case of L. lepideus and P. adiposa, the highest growth appeared at pH 5.
The rest of the mushrooms chose pH 6~7 for
their best mycelial growth (Fig 3). Shim et al.
(2005) revealed that pH 7 was the most suitable for the optimal growth of M. procera [22].
Chi et al. (1996) and Choi et al. (1999) reported that mycelial growth of Phellinus japonica
and P. linteus was optimal at pH 7 and 6~7,
respectively [7, 8]. Shim et al. (2003) showed
that optimal pH of Paecilomyces sinclairii was
8 [21]. Shim et al. (1997) also reported that the
most favorable and most unfavorable pH of
Grifola umbellata was 4 and 9, respectively
[20]. This result suggested that mushrooms
may have a broad pH range for their optimal
mycelial growth.
Screening of favorable culture media.
Ten different culture media were used to
screen the optimal mycelial growth of different
mush-rooms. According to mycelial growth
and density, Hamada, Lilly, PDA and YM
were the most suitable while Czapek Dox,
Hoppkins and Hennerberg were the most
unfavorable media for the mycelial growth of
mushrooms (Fig 4). Besides of slow growth,
mycelial density was also somewhat thin to
thin on Czapek Dox and Hoppkins media.
This result corresponded to that obtained with
P. sinclairii and P. fumosoroseus, which had
been reported by Shim et al. (2003), where
mycelial growth was optimal on Hamada
medium [21]. Shim et al. (2005) also reported
that PDA, YM, Mushroom complete and Hamada were the most suitable media, whereas
Czapex Dox and Glucose peptone were unfavorable to mycelial growth of M. procera [22].
101
Mycelial growth (mm)
pH 5
pH 6
pH 7
pH 8
pH 9
80
60
40
20
0
Ab
Ac
Fv
Hm
Le
Ll
Pa
Pe
Po
Mushrooms
Mycelial growth (mm)
Fig. 3. Effect of pH on the mycelial growth of different edible mushrooms. Standard deviation was calculated for
each strain and data are presented as mean values for studied strains per species: A. bisporus (Ab),
A. cylindracea (Ac), F. velutipes (Fv), H. marmoreus (Hm), L. edodes (Le), L. lepideus (Ll), P.
adiposa (Pa), P. eryngii (Pe)and P. ostreatus (Po).
A. bisporus
A. cylindracea
F. velutipes
H. marmoreus
L. edodes
L. lepideus
P. adiposa
P. eryngii
P. ostreatus
80
60
40
20
Mycelial growth (mm)
0
Cza
Ham
Hen
Hop
GP
GT
Lil
MC
PDA
YM
80
60
40
20
0
Media
Fig. 4. Effect of media on the mycelial growth of different edible mushrooms. Standard deviation was
calculated for each strain and data are presented as mean values for studied strains per species.
Media: Czapek Dox (Cza), Hamada (Ham), Hennerberg (Hen), Hoppkins (Hop), Glucose peptone
(GP),: Glucose tryptone (GT), Lilly (Lil), Mushroom complete (MC), Potato dextrose agar (PDA),
Yeast-malt extract (YM).
102
Mycelial growth (mm)
Adejoye et al. (2006) also reported that the
Yeast and Malt extract medium enhanced the
mycelial growth of Pleurotus florida [1]. The
mycelial growth in Hennerberg was slightly
slo-wer growth than that in PDA and Hamada.
It may be due to the ineffective utilization of
microelements such as Mg+2, SO4-2, NO3-1 and
PO4-3 by the mushrooms.
Effect of carbon sources. Ten different
carbon sources were used to screen the optimal culture conditions. Among them, dextrin,
fructose and sucrose were the best carbon
sources for the mycelial growth. Lactose and
galactose were the most unfavorable carbon
sources. Maltose and mannose were also effective for the mycelial growth of studied mushrooms. In carbon sources, mycelial density (data
not shown) varied from compact to somewhat
compact (Fig. 5). This result is completely simi-
lar to [22] and [20] but partially similar to [21].
Shim et al. (2005) proved that maltose, dextrin,
sucrose and mannose were effective where
lactose was highly ineffective [22]. Shim et al.
(1997) reported that growth of G. umbellata was
favored by the most of carbon sources except
salicin, cellobiose and lactose.[20]. Shim et al.
(2003) revealed that dextrin was suitable for mycelial growth of P. fumosoroseus, which is similar to our findings, but they showed that mycelial density is thin in all carbon sources wher-as
our result is opposite [21]. Morrison and Boyd
(1992) studied the utilization of carbon sources
and explained that dextrin, which is a polymer
of glucose, can be transformed to glucose during metabolic processes [15]. Garraway and
Evans (1984) also found that glucose is the
second best carbohydrate, which may be metabolized easily to produce cellular energy [9].
A. bisporus
A. cylindracea
F. velutipes
H. marmoreus
L. lepideus
P. adiposa
P. eryngii
P. ostreatus
L. edodes
80
60
40
20
Mycelial growth (mm)
0
Dex
Fr
Ga
Gl
Lac
Mal
Man
Sor
Suc
Xy
80
60
40
20
0
Carbon sources
Fig. 5. Effect of carbon sources on the mycelial growth of different edible mushrooms. Standard deviation
was calculated for each strain and data are presented as mean values for studied strains per species.
Carbon sources: Dextrin (Dex), Fructose (Fr), Galactose (Ga), Glucose (Gl), Lactose (Lac),
Maltose (Mal), Mannose (Man), Sorbitol (Sor), Sucrose (Suc):and Xylose (Xy).
Effect of nitrogen sources. It was observed that for mycelial growth of mushrooms on
the culture media the most suitable nitrogen
sources were glycine, ammonium acetate and
calcium nitrate while the most unsuitable were
histidine and ammonium phosphate. Nitrogen
sources stimulate the growth of mycelia where no mycelial growth was found on the culture
103
media. In glycine supplemented medium, mycelial density was compact to somewhat compact while in the rest of nitrogen sources somewhat thin to thin mycelial density was observed
(Fig. 6). Imtiaj et al. (2007) studied the growth
conditions of mushrooms and found that ammonium acetate and glycine strongly enhanced
the growth of mushroom mycelia whereas ammonium phosphate and histidine discouraged
the growth of mycelia [11]. Shim et al. (2005)
clarified that glycine was the most favorable
Mycelial growth (mm)
A. bisporus
L. lepideus
A. cylindracea
P. adiposa
and histidine, arginine and ammonium oxalate
were the most unfavorable for the mycelial
growth of M. procera on the culture media [22].
Lee and Han (2005) showed that soytone,
malt extract, yeast extract and bacto-peptone
were the most favorable while NaNO3 and
urea were the most unfavorable for the mycelial growth of Ramaria botrytis [13]. Moreover,
organic nitrogen is more effective than inorganic nitrogen. The result of the present study is
similar to the findings of Lee and Han [13].
F. velutipes
P. eryngii
H. marmoreus
P. ostreatus
L. edodes
80
60
40
20
Mycelial growth (mm)
0
Ala
AA
AP
Arg
CN
Gly
His
Met
PN
Ur
80
60
40
20
0
Nitrogen sources
Fig. 6. Effect of nitrogen sources on the mycelial growth of different edible mushrooms. Standard deviation
was calculated for each strain and data are presented as mean values for studied strains per species.
Nitrogen sources: Alanine (Ala), Ammonium acetate (AA), Ammonium phosphate (AP), Arginine (Arg),
Calcium nitrate (CN), Glycine (Gly), Histidine (His), Methionine (Met), Potassium nitrate (PN) and
Urea (Ur).
Conclusion
This is the first study investigating the optimal conditions for mycelial growth of 371 strains
belonging to 9 species of mushrooms. To obtain accurate growth conditions, a large number of mushroom strains of a given species
were studied and it was found that the nutriational requirements for the mycelial growth of
taxonomically identical strains were about similar. Thus, the basic information obtained from
this study can be used for the mass production of mycelia of tested mushroom species.
Acknowledgement. This work was jointly
supported by research grant from Korean Science and Engineering Foundation (KOSEF)
and Agricultural R & D Promotion Center
(ARPC) through Culture Collection of Wild
Mushroom (CCWM) species in the University
of Incheon, Korea.
104
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СРАВНИТЕЛНИ ПРОУЧВАНИЯ НА ВЛИЯНИЕТО НА
УСЛОВИЯТА НА КУЛТИВИРАНЕ И ХРАНИТЕЛНИТЕ ФАКТОРИ ВЪРХУ
МИЦЕЛНИЯ РАСТЕЖ НА ЯДЛИВИ ГЪБИ
Ахмед Имтиай, Чандана Явасингхе, Геон Уо Лии, Тае-Соо Лии*
Резюме
Ядливите гъби обикновено са плътни гъби, принадлежащи към Basidiomycota или Ascomycota. Изследвани са оптималните културални условия за мицеларен растеж на 371 щама, принадлежащи към 9 вида ядливи гъби. Установено е, че подходящата температура за растеж е 25оС, а оптималните температурни граници са от 20 до 30оС. Гъбите имат широк рН диапазон за мицелен растеж (5-9), но най – благоприятното рН е между 6 и 7. Най-подходящи
хранителни среди са Hamada, Lilly, PDA и YM, докато Czapek Dox, Hoppkins u
Hennerberg са неподходящи за радиален мицелен растеж. От изпитаните 10
различни въглеродни източници, декстрин, фруктоза и захароза са най-добре
усвояеми, докато лактоза и галактоза са най-неблагоприятни. При използването на различни въглеродни източници бе установено, че мицеларната
плътност варира от компактна до малко компактна. Най-подходящи азотни
източници за развитие на мицела са глицин, амониев ацетет и калциев нитрат, докато най-неблагоприятни са хистидин и амониев фосфат. В случаите
с глицин е установено, че мицелната плътност варира от почти компактна
до компактна, а при останалите азотни източници мицелът е по-скоро тънък.
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