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Nutritional perspectives of an ectomycorrhizal edible mushroom Amanita of the southwestern India

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The occurrence of ectomycorrhizal Amanita sp. is common in scrub jungles of southwest India and tender sporocarps serve as ethnic nutritional source for local dwellers during southwest monsoon season. Evaluation of the nutritional constituents of uncooked and cooked tender sporocarps revealed significantly higher quantity of total lipids and calorific value in uncooked than cooked samples, while it was opposite for the crude protein. There was no significant change in crude fibre and carbohydrates between uncooked and cooked samples. Uncooked as well as cooked samples were rich in potassium followed by iron. The Na-K ratio in uncooked as well as cooked samples (<1) was favourable, while the Ca-P ratio (<1) was not favourable. In cooked samples, most of the essential amino acids (histidine, isoleucine, methionine, cystine, phenylalanine, tyrosine, threonine and valine) were significantly increased. The in vitro protein digestibility was significantly higher in uncooked than cooked samples. The protein digestibility corrected to amino acid score was moderate to high (uncooked, 58-104; cooked, 54-91). The protein efficiency ratios in uncooked and cooked samples (>2) depicts the high quality of protein. Among the fatty acid methyl esters, oleic acid in uncooked samples, while palmitic and stearic acids in cooked samples were significantly higher. The tender sporocarps of Amanita sp. in scrub jungles of southwestern India provide valuable nutrients to the local dwellers during monsoon period. Key words  Amino acids  fatty acids  minerals  protein bioavailability  proximal qualities
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Submitted 6 September 2017, Accepted 18 January 2018, Published 30 January 2018
Corresponding Author: Kandikere R. Sridhar e-mail kandikere@gmail.com 54
Nutritional perspectives of an ectomycorrhizal edible mushroom
Amanita of the southwestern India
Greeshma AA, Sridhar KR and Pavithra M
Department of Biosciences, Mangalore University, Mangalagangotri, Mangalore 571 199, Karnataka, India
Greeshma AA, Sridhar KR, Pavithra M 2018 Nutritional perspectives of an ectomycorrhizal
edible mushroom Amanita of the southwestern India. Current Research in Environmental &
Applied Mycology 8(1), 5468, Doi 10.5943/Cream/8/1/4
Abstract
The occurrence of ectomycorrhizal Amanita sp. is common in scrub jungles of southwest
India and tender sporocarps serve as ethnic nutritional source for local dwellers during southwest
monsoon season. Evaluation of the nutritional constituents of uncooked and cooked tender
sporocarps revealed significantly higher quantity of total lipids and calorific value in uncooked than
cooked samples, while it was opposite for the crude protein. There was no significant change in
crude fibre and carbohydrates between uncooked and cooked samples. Uncooked as well as cooked
samples were rich in potassium followed by iron. The Na-K ratio in uncooked as well as cooked
samples (<1) was favourable, while the Ca-P ratio (<1) was not favourable. In cooked samples,
most of the essential amino acids (histidine, isoleucine, methionine, cystine, phenylalanine,
tyrosine, threonine and valine) were significantly increased. The in vitro protein digestibility was
significantly higher in uncooked than cooked samples. The protein digestibility corrected to amino
acid score was moderate to high (uncooked, 58-104; cooked, 54-91). The protein efficiency ratios
in uncooked and cooked samples (>2) depicts the high quality of protein. Among the fatty acid
methyl esters, oleic acid in uncooked samples, while palmitic and stearic acids in cooked samples
were significantly higher. The tender sporocarps of Amanita sp. in scrub jungles of southwestern
India provide valuable nutrients to the local dwellers during monsoon period.
Key words Amino acids fatty acids minerals protein bioavailability proximal qualities
Introduction
Similar to the plants and animals, fungi have an independent evolutionary line capable to
meet human requirements like nutrition, medicine and industrial applications. Hypogeous or
epigeous macrofungi possess distinct characteristic macroscopic fruit bodies (Chang & Miles
1989). They are the centre of attraction worldwide as they constitute important live material for
production of enzymes, metabolites, cosmetics and nanomaterials (Manzi & Pizzoferrato 2000, Wu
et al. 2004, Hyde et al. 2010, Vikineswary & Chang 2013, Arun et al. 2014, Taofiq et al. 2016).
One of the interesting features of wild macrofungi is that their benefits (nutritional and therapeutic
value) are still recognized based on traditional knowledge of tribes or native people of a specific
geographic region. Asian countries are known for utilization of macrofungi for human nutrition and
therapy based on ethnic knowledge (Aly et al. 2011, Xu et al. 2011, De Silva et al. 2013). The
Western Ghats of India being one of major hotspots of biodiversity, known for a variety of
macrofungi grow in a wide range of forest ecosystems at different altitudinal ranges (Mohanan
Current Research in Environmental & Applied Mycology 8(1): 5468 (2018) ISSN 2229-2225
www.creamjournal.org Article
Doi 10.5943/cream/8/1/4
Copyright © Beijing Academy of Agriculture and Forestry Sciences
55
2011, Farook et al. 2013, Senthilarasu 2014, Pavithra et al. 2015, Senthilarasu & Kumaresan 2016).
Systematic inventories and discussion with tribals and native people resulted in recognizing many
edible mushrooms in the Western Ghats and west coast of India (Ghate et al. 2014, Senthilarasu
2014, Karun & Sridhar 2014, 2016, Pavithra et al. 2015). Amanita sp., Astraeus spp., Auricularia
spp., Lentinus spp., Russula spp. and Termitomyces spp. are some of the commonly traditionally
consumed macrofungi in the Western Ghats and west coast of India (Senthilarasu 2014, Karun &
Sridhar 2014, 2016, Pavithra et al. 2015).
The range of Amanita spp. worldwide represented from 900-1000 species (Tulloss 2005).
This genus consists of over 500 ectomycorrhizal species associated with diverse tree species (e.g.
Abies, Cedrus, Picea and Pinus) (Itoo et al. 2016). Although several members of Amanitaceae are
poisonous, many are edible (e.g. Amanita caesarea, A. chepangiana, A. citrina, A. crocea, A.
flammeola, A. franchetii, A. fulva, A. hemibapha, A. jacksonii, A. manginiana, A. loosii, A.
pseudoporphyria, A. princeps, A. rubescens, A. tuza, A. sinensis, A. vaginata and A. zambiana
(Pegler & Piearce 1980, Bhatt & Lakhanpal 1988, León-Guzmán et al. 1997, Ouzouni 2007, Pérez-
Moreno et al. 2008, Sanmee et al. 2008, Semwal et al. 2014, Tripathy et al. 2014). Recent
inventories in the lateritic soils of scrub jungles in southwestern India revealed occurrence of
Amanita sp. which is traditionally considered edible in tender stage (Karun & Sridhar 2014). This
mushroom has association with many tree species in scrub jungles (e.g. Acacia auriculiformis,
Anacardium occidentale, Hopea ponga and Terminalia paniculata). It is a traditional practice to
collect tender sporocarps in different shapes (spherical, oval, dumble and partly ruptured volva) for
consumption. The fruit bodies show up for a short period during southwest monsoon season (June-
July). Being edible in young stage, such fruit bodies of Amanita sp. were collected from the scrub
jungles in lateritic belt of southwestern India and evaluated its nutritional potential in uncooked and
cooked form.
Materials & Methods
Mushroom
Edible stages of Amanita sp. (young sporocarp stages) were collected from the lateritic soils
of the southwestern India (Konaje Village, Dakshina Kannada, Mangalore, India: 12°48’N,
74°55’E; 115 m asl) with support of local dwellers who regularly consume during monsoon season
(June-August). Its fruit bodies are very common underneath the tree species of Acacia
auriculiformis, Anacardium occidentale, Hopea ponga and Terminalia paniculata. Based on
macro- and micro-morphological features, although the Amanita sp. roughly matches with Amanita
marmorata reported from Hawaii (Miller et al. 1996), several glaring differences support to
consider it as a new species. The tender sporocarps collected and consumed by the villagers include
spherical, oval, dumble shapes and just partially ruptured volva stage (Fig. 1a-k). Sampling was
carried out in five locations with about 50 m apart in lateritic scrub jungles. The young stages of
mushroom in each sample were separately rinsed in distilled water to eliminate soil, roots and other
debris. They were wiped with clean cloth to eliminate moisture on the surface. Each replicate was
divided into two groups, the first group was oven dried at 50-55°C, while the second group was
separately cooked in a household pressure-cooker with distilled water (1:1 v/v) followed by oven
drying. The dried samples were milled in Wiley Mill (mesh #30) and powder was refrigerated in
air-tight containers for analysis.
Proximal analysis
Moisture. Moisture content of uncooked and cooked mushroom powder of Amanita sp. was
assessed gravimetrically (AOAC 1995). Replicate flour samples were dried at 80°C for 24 hr and
difference between initial and final weight were considered to estimate moisture content in per cent
to express proximate composition on dry weight basis.
56
(where I, weight of sample before drying in g; F, weight of sample after drying in g; W, weight of
mushroom flour taken in g).
Fig. 1 Various stages of immature sporocarps a-b maturing sporocarps. c-e and mature fruit
bodies. f-g of Amanita sp.: spherical, beak-like protuberance, extended protrusion and dumble
shaped tender sporocarps a cut-open tender sporocarps. b extended stipe prior to opening of pileus.
c-e (note roots surrounding volva, arrows); mature fruit bodies. f gills, partial veil with intact volva
of a mature fruit body (g).
57
Crude protein. The crude protein content was evaluated by micro-Kjeldahl method
(Humphries 1956). Mushroom flour (100 mg) was extracted with pinch of catalytic mixture (copper
sulphate, selenium, potassium sulphate: 1:1:20 w/w), concentrated sulphuric acid (10 ml). The
mixture was digested in Kjeldahl flasks until it turns colourless and the volume was made up with
distilled water (100 ml). The digested sample (10 ml) was transferred to Kjeldahl apparatus, sodium
hydroxide (40%, 10 ml) was added and distilled until accumulation of 25 ml in receiver flask
containing boric acid (2%, 10 ml) and mixed indicator (0.2 % of methyl red and methylene blue in
ethanol, 2:1 v/v). After cooling to room temperature, the solution was titrated against hydrochloric
acid (0.01N) till the colour changes from green to pink and nitrogen content was calculated to
determine crude protein content.
(where A, volume of 0.01N HCl titrated minus volume of blank; N, normality of HCl; 0.0014, g
nitrogen in 0.1N HCl; W, weight of sample in g).
Total lipids. The total lipid was determined based on the method of AOAC (1995).
Mushroom flour (1 g) was extracted with petroleum ether (6 hr) in Soxhlet apparatus. The solvent
was evaporated to dryness. The initial and final weight of the sample was recorded to calculate the
percentage of total lipid.
(where I, weight of empty flask in g; F, weight of flask with lipid in g; W, weight of mushroom
flour taken in g).
Crude fibre. The crude fibre content was determined gravimetrically according to AOAC
(1995). Defatted mushroom sample (500 mg) was treated with sulphuric acid (0.025N, 200 ml) and
boiled (30 min). On cooling the contents were filtered, the residue was washed repeatedly in
boiling distilled water to eliminate acid traces. The residue was boiled in sodium hydroxide
(0.313N) (30 min). The contents were filtered and washed repeatedly in boiling water to remove
traces of alkali. The residue was transferred to pre-weighed crucible, heated in muffle furnace
(550°C, 3 hr) and the final weight was recorded on cooling.
(where I, weight of empty crucible in g; F, weight of crucible with fibre in g; W, weight of
mushroom flour taken in g)
Ash. The percentage of ash was determined based on AOAC (1995). The homogenised
mushroom flour (~1 g) was taken in pre-weighed porcelain crucible and dried in the oven at 100°C
for 68 hr. The crucible was then transferred to furnace (550°C, 8 hr) until attaining constant
weight to calculate the ash content.
(where I, weight of crucible in g; F, weight of crucible with ash in g; W, weight of mushroom flour
taken in g)
Carbohydrates. To evaluate carbohydrate content, the phenol sulphuric acid method proposed
by Dubois et al. (1956) was followed. Mushroom sample (100 mg) was treated with hydrochloric
58
acid (2.5N, 5 ml) and heated in boiling water bath (3 hr). The reaction was neutralized by the
addition of sodium carbonate until the effervescence ceases and the volume was made up to 100 ml
with distilled water. Sample (0.2 ml) was further diluted with distilled water (0.8 ml), phenol (5%,
1 ml) followed by sulphuric acid (96%, 5 ml) was added and kept in water bath (30°C, 20 min).
Control was prepared based on the following method without addition of sample. The absorbance
was measured (490 nm). The D-glucose served as standard and the mean value was expressed in
gram of carbohydrate in 100 gram of mushroom sample.
Calorific value. The calorific value of the mushroom powder was calculated according to the
formula proposed by Ekanayake et al. (1999).
Mineral analysis
The scanning electron microscope-energy dispersive X-ray spectrometer (SEM-EDX) was
employed to evaluate minerals (Lui et al. 2015). Homogenised mushroom flour (particle size, ~40
μm) was dusted on the brass stub with the carbon tape. The mounted powder samples were coated
with gold by sputter coat (20 mA, 10 min). The samples were analysed by SEM (Carl Zeiss Sigma,
Germany) and EDX (Oxford instruments, Germany) at 3.5 mm working distance. The beam energy
used was 15KeV and maps of 98X pixel were obtained in the selected area. The generated mineral
maps were assessed for distribution of elemental concentration. The ratios of Na-K and Ca-P were
calculated.
Amino acid analysis
The amino acids content in the mushroom flour was assessed based on Hofmann et al. (1997,
2003).
Hydrolysis. Known quantity of mushroom sample was treated with hydrochloric acid (6N, 15
ml, 145°C, 4 hr). Alkaline hydrolysis was followed for tryptophan as they are stable in basic
condition and for sulphur amino acids oxidized samples were used. The contents were evaporated
to dryness to remove hydrochloric acid on a rotary evaporator (Büchi Laboratoriumstechnik
AGRE121; Switzerland) connected to diaphragm vacuum pump (MC2C; Vacuubrand GmbH,
Germany).
Derivatization. For derivatization, the hydrolysate was treated with trans-4-(aminomethyl)-
cyclohexanecarboxylic acid (purity, 97%; Sigma Aldrich) as internal standard.
Standards. The weighed standards in reaction vial were treated with dichloromethane and
dried to remove moisture by flushing inert helium with passive heating in an oil bath (60°C).
Acidified isopropanol (12 ml) (acetyl chloride + 2-propanol) (1:4 v/v) was added following by
heating (100°C, 1 hr). The contents were evaporated to dryness in the oil bath (60°C) by gently
flushing helium. The dry residue was treated with dichloromethane and evaporated; this process
was repeated to remove traces of water and propanol. The residues were treated with trifluroacetic
anhydride (200 ml) for overnight at room temperature. The fraction of the solution was injected in
gas chromatography-combustion-isotope ratio mass spectrometry (GC-C-IRMS/MS).
Analytical parameters. Isotope with GC-C-IRMS/MS (GC: Hewlett-Packard 58590 series II,
Germany; combustion series II-interface, IRMS MAT 252, Finnigan MAT, Germany; MS: GCQ,
Finnigan MAT, Germany) was carried out. The capillary column of dimension 50 m 0.32 mm
i.d. 0.5 µm BPX5 (SGE) was connected to gas chromatography. The flow of carrier gas was 1.5
ml/min with the head pressure 13 psi. The details of temperature programme are given in Table 1.
Essential amino acids. The ratio of total essential amino acids (TEAA) to total amino acids
(TAA) was calculated.
59
Table 1 Temperature programme for GC-C-IRMS/MS.
Time (min)
Temperature (°C)
1
50
10
50-100
10
100-175
10
175-250
10
250
The essential amino acid score (EAAS) was calculated by dividing individual EAA content
by FAO-WHO (1991) EAA reference pattern.
Protein bioavailability
Digestibility. The in vitro protein digestibility was determined based on multi-enzyme
technique (Akeson & Stahmann 1964). Protein digest were prepared by treating 100 mg of
mushroom flour with 2.5 ml of 1.5 mg pepsin (3165 units/mg protein, Sigma Aldrich) in 0.1N
hydrochloric acid and was neutralized by the addition of 2.5 ml of 1N sodium hydroxide. The
reaction mixture was treated with enzyme solution i.e. trypsin (16100 units/mg protein, Sigma
Aldrich) and chymotrypsin (76 units/mg protein, Sigma Aldrich) (2 mg each in 2.5 ml of 0.1M
phosphate buffer, pH 8), incubated at 37°C for 24 hr. The reaction was halted by the addition of 0.7
ml trichloroacetic acid (100 %). Enzyme blank was prepared as described above but without
addition of sample. The contents were centrifuged and supernatant was recovered. The residue was
repeatedly washed with 10% Trichloroacetic acid and the supernatant was pooled. The supernatant
was treated with twice the volume of diethyl ether and ether layer was gently removed by
aspiration. The aqueous layer was maintained in water bath to eliminate the traces of ether. After
cooling, the volume was made to 25 ml by distilled water. The nitrogen content in the sample was
estimated by micro-Kjeldahl method (Humphries 1956). IVPD was calculated as follows:
PDCAAS. Protein digestibility-corrected amino acid score (PDCAAS) has been calculated
based on FAO-WHO (2007) for the measurement of the protein value in the human nutrition.
Protein efficiency ratio. The protein efficiency ratio (PER) determines the effectiveness of a
protein present in the sample. It was calculated based on Alsmeyer et al. (1974).
Fatty acid analysis
The total lipids content obtained by hot extraction of uncooked and cooked mushroom flour
was used to determine fatty acids methyl esters (FAMEs). The analysis was performed by the
method outlined by Padua-Resurreccion & Benzon (1979).
Methylation. Methylation was performed by acid-catalysed method. The lipid sample in the
screw cap glass tube (2557 mm) was treated with acidified methanol (0.2 ml) (5% hydrochloric
acid + 8.3 ml of acetyl chloride were added to 100 ml of absolute methanol in ice jacket). The
60
contents were vortexed and incubated (70°C, 10 hr). After cooling, distilled water (500 µl) and n-
hexane (HPLC grade, 100 µl) were added, vortexed and allowed to separate. The n-hexane layer
was aspirated into air-tight micro-centrifuge tubes and stored in refrigerator at 4°C for assay. The
trans-esterified samples (100 µl) were made up to 1 ml by n-hexane and the fraction of samples (1
µl) was injected into the gas chromatograph.
Analytical parameters. The FAMEs were quantified by gas chromatography (GC-2010,
Shimadzu, Japan) equipped with the fused silica column (BPX-70) and flame ionization detector
(FID). The column was conditioned (10 hr) prior to use. The signal detected by FID was amplified
and were processed in GC-solution software:
http://www.shimadzu.eu/products/software//labsolutions/gcgcms/default.aspx. The analytical
conditions were followed based on Nareshkumar (2007) (Table 2). The identification of peaks
obtained from the lipid profiling was determined by comparing retention time, molecular weight
and mass spectra with those available in NIST 11 (National Institute of Standards and Technology)
library (NIST 11 mass spectrometry library; NIST/EPA/NIH; version # 2011).
Table 2 Analytical conditions for gas chromatography.
Auto-sampler settings
Injection sample volume 1 µl; terminal air gap, nil; number of rinses with solvent during per-run, 4; number
of rinses with solvent during post-run, 6; number of rinses with sample, 5; washing volume, 8 µl; plunger
suction and injection speed, high; syringe injection speed, low; injection port dwell time, 1 sec
Injection port settings
Injection mode, split; temperature, 225ºC; carrier gas, N2/air; pressure, 114.9 kPa; column flow, 1.29 ml/min;
linear velocity, 34 cm/sec; purge flow, 3ml/min; split ratio, 50
Column oven settings
Initial temperature, 100ºC
Column oven temperature program
Equilibrium time, 3 min; total program time, 30 min
Temperatures hold time
100ºC, 1 min; 220ºC, 5 min; rate, 5ºC/min
Column information
Column, BPX-70; film thickness, 0.25 µm; inner diameter, 0.25 mm; column length, 30 m; column maximum
temperature, 260ºC
Detector settings
Detector, FID, temperature, 280ºC; makeup gas, N2/air; makeup flow, 30 ml/min; H2 flow, 47 ml/min;
airflow, 400 ml/min; sampling rate, 40 ms; stop time, 30 min; delay time, nil)
Data analysis
The t-test was followed to find out variation between uncooked cooked mushroom samples
for different nutritional components based on Statistica Version # 8.0 (StatSoft 2008).
Results & Discussion
Analysis of proximal properties of food stuff is one of the basic steps which grossly reflect
the nutritional value. The moisture content of Amanita powder was significantly higher in
uncooked than cooked samples (p<0.05) (Table 3). Crude protein was significantly higher in
cooked than uncooked samples (p<0.05). Total lipids content, ash content and calorific value were
significantly higher in uncooked than cooked samples (p<0.05). There was no significant change in
crude fibre and carbohydrate content between uncooked and cooked samples.
The increase of crude protein may be due to increased free amino acids owing to pressure
cooking of Amanita sp., which has also reflected in increased amino acids. This view has been
supported by Reid et al. (2016) based on studies carried out on Amanita zambiana, where crude
protein significantly increased on microwave treatment and predicted that such change was due to
increase in protein availability as a result of enzyme hydrolysis of insoluble protein. The crude
protein content in Amanita sp. is higher than many edible Amanita spp. (Amanita citrina, A, fluva,
61
A. loosii and A. rubescens) (León-Guzmán et al. 1997, Tripathy et al. 2014, Sharma & Gautham
2015), while lower than A. caesarea and A. zambiana (Sharma & Gautham 2015, Reid et al. 2016).
Table 3 Proximal properties of uncooked and cooked Amanita sp. on dry weight basis (n=5;
mean±SD; t-test: *p<0.05).
Uncooked
Cooked
Moisture (%)
5.6±0.2*
4.8±0.4
Crude protein (%)
16.3±0.49
20±0.97*
Total lipids (%)
4.7±0.58*
1.9±0.65
Crude fibre (%)
7.4±0.37
6.7±0.43
Ash (%)
13.5±2.4*
8.2±2
Carbohydrates (%)
22.5±1.22
18.5±1.6
Calorific value (kJ/100 g)
827.4±25.8*
717.2±20.9
Usually the total lipid contents in edible mushrooms will be low and advantageous for human
health. The total lipids in Amanita sp. is comparable to dried, but lower than fresh and frozen A.
zambiana (Reid et al. 2016). The total lipids, crude fibre and ash contents of Amanita sp. is higher
than A. caesarea, A. citrina, A, fluva and A. rubescens (León-Guzmán et al. 1997, Sharma &
Gautham 2015). As seen in Amanita sp., the ash content decreases in mushrooms on conventional
cooking as minerals drain away in water, thus alternative thermal processing helps retaining many
essential minerals. The carbohydrates in uncooked Amanita sp. is higher than fresh and frozen A.
zambiana, while lower than dried A. zambiana (Reid et al. 2016). The percentage of carbohydrate
of Amanita sp. is lower than A. caesarea, A. citrina and A. fluva (Sharma & Gautham 2015).
Although crude protein of Amanita sp. increased on cooking, total lipids as well as carbohydrates
decreased, which has reflected in significantly low calorific value (p<0.05). The present study
projects moderate quantities of protein as well as carbohydrates with low fat content in Amanita sp.
thus this diet is helpful to maintain homeostasis in humans.
Table 4 Mineral composition of uncooked and cooked Amanita sp. (mg/100 g) (n=5; meanSD; t-
test: *p<0.01, **p<0.001; aNRC-NAS 1989 recommended pattern; BDL, below detectable level).
Uncooked
Cooked
Infants/
Childrena
Adultsa
Sodium
855.3±10.1*
621.6±7.6
120-400
500
Potassium
4823±5.7**
3385±6.6
500-1600
1600-2000
Calcium
150±10*
94.3±4
600-800
800
Phosphorus
728±7.5*
618±15.7
500-800
800
Magnesium
127±2**
55.3±1.5
60-170
280-350
Manganese
134.3±4.5
BDL
Iron
1306±5.56**
488.3±6.6
10
10-15
Sulphur
716.6±20.8**
248.3±4.7
Copper
238.3±34
BDL
0.6-2
1.5-3
Aluminium
1231±10.2**
917.3±8.7
Na-K ratio
0.17
0.20
Ca-P ratio
0.18
0.15
The uncooked and cooked samples of Amanita sp. were rich in potassium followed by iron
and aluminium (Table 4). Sodium (p<0.01), potassium (p<0.001), calcium (p<0.01), magnesium
(p<0.001), phosphorus (p<0.01), iron (p<0.001), sulphur (p<0.001) and aluminium (p<0.001)
contents were significantly higher in uncooked than cooked samples. The rest of the minerals
(copper and manganese) although detected in uncooked samples, they were below detectable limit
62
in cooked samples. Sodium, phosphorous and iron in uncooked Amanita sp. is higher, while
calcium and magnesium contents are lower than A. caesarea and A. loosii (Tripathy et al. 2014).
The organic potassium salts in food have a broad range of health benefits for heart, kidney,
bone and other tissues (Weaver 2013). Dietary potassium also lowers the risk of stroke by
decreasing blood pressure (Weaver 2013). The food stuffs possessing Na-K ratio <1 are known to
alleviate the high blood pressure (Yusuf et al. 2007). Sodium as well as potassium in Amanita sp.
are higher than NRC-NAS (1989) stipulated standards for infants/children and adults. In addition,
the Na-K ratio in uncooked as well as cooked samples is in favourable range (0.17-0.2). Calcium as
the major component of bones confers hardness and rigidity. However, calcium content was higher
in uncooked samples than cooked samples of Amanita sp., it was lower than NRC-NAS (1989)
pattern. The phosphorus content was higher than NRC-NAS (1989) stipulated pattern, but the Ca-P
ratio ranged between 0.18-0.15, which is not a favourable ratio (Shills & Young 1988). The
magnesium content in uncooked Amanita sp. is comparable with NRC-NAS (1989) pattern for
infants/children, but not for adults. Iron is an essential component for production of haemoglobin,
which binds to oxygen. Iron content in uncooked and cooked Amanita sp. is higher than NRC-NAS
(1989) pattern. Aluminium content was significantly lowered on cooking (p<0.001), which is an
improvement sign to decrease its content by thermal treatments. According to Hill et al. (2000),
lateritic rock/soil type is rich in iron as well as aluminium contents, thus Amanita sp. may also have
these elements in high quantity.
Table 5 Amino acid composition of uncooked and cooked Amanita sp. in comparison with
soybean, wheat and FAO-WHO pattern (g/100 g protein) (n=5, meanSD; t-test: *p<0.05, **
p<0.01, ***p<0.001; aBau et al. 1994, bUSDA 1999, cFAO-WHO 1991 pattern, dMethionine +
Cystine, ePhenylalanine + Tyrosine, fRatio of total essential amino acids and total amino acids,
BDL, below detectable level).
Uncooked
Cooked
Soybeana
Wheatb
FAO-WHOc
Essential amino acid
Histidine
1.76±0.11
2.5±0.03***
2.50
1.9-2.6
1.9
Isoleucine
3.73±0.28
4.73±0.03*
4.62
3.4-4.1
2.8
Leucine
7.17±0.06**
6.63±0.03
7.72
6.5-7.2
6.6
Lysine
9.38±0.03
9.04±0.03
6.08
1.8-2.4
5.8
Methionine
2.17±0.05
2.56±0.02**
1.22
0.9-1.5
2.5d
Cystine
0.08±0.01
0.19±0.02**
1.70
1.6-2.6
Phenylalanine
3.32±0.04
4.74±0.05***
4.84
4.5-4.9
6.3e
Tyrosine
2.77±0.16
3.03±0.02**
1.24
1.8-3.2
Threonine
4.32±0.16
4.75±0.04*
3.76
2.2-3.0
3.4
Tryptophan
BDL
BDL
3.39
0.7-1.0
1.1
Valine
5.05±0.04
5.92±0.06***
3.7-4.5
3.5
Non-essential amino acid
Alanine
8.41±0.05
10.2±0.25**
Arginine
7.11±0.03***
4.9±0.07
Aspartic acid
7.21±0.05***
3.89±0.10
Glutamic Acid
9.80±0.03
BDL
Glycine
12.3±0.07 ***
9.83±0.05
Proline
6.17±0.04
7.14±0.03***
Serine
5.84±0.06
6.88±0.07***
TEAA-TAA ratiof
0.41
0.50
Among the EAA in Amanita sp., except for lysine (p>0.05) the rest were significantly
changed on cooking (Table 5). In cooked Amanita sp., isoleucine, threonine (p<0.05), methionine,
cystine, tyrosine (p<0.01), histidine, phenylalanine and valine (p<0.001) were significantly
increased, while it was reverse for leucine (p<0.01). Except for cystine and tryptophan, rest of the
63
amino acids in uncooked/cooked Amanita sp. are comparable or surpassed the quantities present in
soybean and wheat, so also the FAO-WHO (1991) stipulated pattern.
Among the non-essential amino acids, glycine was the highest followed by glutamic acid and
alanine. Alanine (p<0.01), proline and serine (p<0.001) were significantly higher in cooked
Amanita sp., while it was opposite for arginine, aspartic acid and glycine (p<0.001). The amino
acid composition in Amanita sp. is higher than A. caesarea, A. citrina, A. fluva and A. rubescens
(León-Guzmán et al. 1997, Sharma & Gautham 2015). Sudheep & Sridhar (2014) also reported
significant increase in many amino acids on cooking the wild edible mushroom Termitomyces
globulus of the Western Ghats. Lysine plays a key role in calcium absorption by reducing the
amount of calcium excretion in urine. Its deficiency in chicks limits the synthesis of proteins
(including cytokines) as well as proliferation of lymphocytes impairing immune responses leading
to increased morbidity and mortality (Kidd et al. 1997, Konashi et al. 2000). Threonine is a major
component of intestinal mucin and plasma -globulin in animals (Kim et al. 2007). Leucine has the
capacity to dissolve visceral fat and helps in reduction of weight owing to activation of mTOR
signalling pathway, which regulates protein synthesis and degradation in cells (Meijer &
Dubbelhuis 2004). Increase in TEAA-TAA ratio on cooking Amanita sp. is favourable indication of
the improved quality.
The IVPD was significantly higher in uncooked than cooked of Amanita sp. (p<0.05)
indicates its nutritional value in uncooked stage (Table 6). According to the nutrition labelling
regulations of the food and drug administration (FDA 1993), EAAS and PDCAAS determine the
overall protein quality (Cuptapun et al. 2010). The EAAS of histidine, isoleucine, methionine +
cystine, phenylalanine + tyrosine, threonine and valine were increased in cooked Amanita sp. The
PDCAAS depicts protein quality of food stuffs, its range in Amanita sp. was from 57.9-103.6 and
53.7-90.7 in uncooked and cooked samples, respectively. The maximum PDCAAS value is
Table 6 In vitro protein digestibility (IVPD; t-test: *p<0.05), essential amino acid score (EAAS),
protein digestibility corrected amino acid score (PDCAAS) and protein efficiency ratio (PER) of
uncooked and cooked Amanita sp.
Uncooked
Cooked
IVPD (%)
64.4±2.9*
53.7±3
EAAS
Histidine
0.92
1.31
Isoleucine
1.33
1.68
Leucine
1.08
1.00
Lysine
1.61
1.55
Methionine + Cystine
0.90
1.10
Phenylalanine + Tyrosine
0.96
1.23
Threonine
1.27
1.39
Valine
1.44
1.69
PDCAAS
Histidine
59.24
70.34
Isoleucine
85.65
90.21
Leucine
69.55
53.70
Lysine
103.68
83.23
Methionine + Cystine
57.96
59.07
Phenylalanine + Tyrosine
61.82
66.05
Threonine
81.78
74.64
Valine
92.73
90.75
PER
PER1
2.29
2.00
PER2
2.49
2.22
PER3
2.47
2.13
64
100% for milk, eggs, and soy protein, while those proteins devoid of EAA have a PDCAAS as 0.
According to Friedman (1996), the PER of food stuffs greater than 2 are high quality, from 1.5-2
are moderate quality and less than 1.5 are poor quality. The PER of uncooked samples were greater
than cooked Amanita sp. (2.29-2.49 vs. 2-2.22) indicates its high quality in uncooked as well as
cooked stage.
Uncooked and cooked Amanita sp. showed highest quantity of palmitic acid, which
significantly increased on cooking (p<0.01) (Table 7). Stearic acid was also significantly increased
in cooked samples (p<0.01), while it was reverse for oleic acid (p<0.001). The TSFA were higher
in cooked samples, while it was opposite for TUFA. Uncooked samples showed higher and
favourable TUFA-TSFA ratio than cooked samples. In Amanita sp. total saturated fatty acids were
higher but unsaturated fatty acids were lower than A. rubescens (León-Guzmán et al. 1997).
Dietary stearic acid is well known for dramatic reduction of visceral adipose tissue (VAT) (Shen et
al. 2014). Palmitic acid has many applications especially in cosmetics, detergents and emollient
(Rabasco-Álvarez & González-Rodríguez 2000). Oleic acid regulates membrane lipid structure and
in turn controls G protein-mediated signaling, which leads to reduction of blood pressure (Terés et
al. 2008).
Table 7 Fatty acid methyl esters (FAMEs) of uncooked and cooked Amanita sp. (g/100 g lipid)
(n=5, mean±SD; t-test: *p<0.01; **p<0.001).
Uncooked
Cooked
Saturated fatty acid
Palmitic Acid (C16:0)
50.4±6.1
64±2.25*
Stearic Acid (C18:0)
14.3±2
23.3±1.7*
Unsaturated fatty acid
Oleic Acid (C18:1)
23.3±1.5**
9.5±1.25
Total saturated fatty acids (TSFA)
64.7
87.3
Total unsaturated fatty acids (TUFA)
23.3
9.5
Ratio of TUFA-TSFA
0.36
0.10
Conclusions
This study addressed nutritional profile of traditionally consumed tender wild mushroom
Amanita sp. occurring in the lateritic scrub jungles of southwestern India in uncooked and cooked
stage. It is endowed with adequate protein, sufficient fibre, moderate quantity of carbohydrates and
low total lipid content. Sodium, potassium and iron in uncooked as well as cooked Amanita sp.
surpassed NRC-NAS (1989) recommended pattern with favourable Na-K ratio (<1). Except for
cystine and tryptophan, the essential amino acids (EAA) are comparable or surpass the soybean and
wheat, which fulfilled the FAO-WHO (1991) stipulated pattern. The total EAAS and total amino
acid ratio has improved in cooked samples denotes its superiority. The in vitro protein digestibility
was high in uncooked samples with good EAA score, protein digestibility corrected to amino acid
score and favourable protein efficiency ratios (>2). Palmitic, stearic and oleic acids were the major
fatty acid methyl esters in uncooked as well as cooked samples. The present study justified the
value of traditional knowledge on nutritional advantages of tender sporocarps of Amanita sp.
consumed by the tribals and local dwellers of southwestern India. Future studies on its bioactive
potential and functional properties will open up possibilities of its utilization as food source or
incorporation with other food stuffs to enhance the quality attributes.
Acknowledgements
The authors are grateful to Mangalore University to accomplish this study in the Department
of Biosciences. GAA is greatly acknowledges the award of INSPIRE Fellowship, Department of
Science and Technology, New Delhi, Government of India. KRS is grateful to the University
Grants Commission, New Delhi, India for the award of UGC-BSR Faculty Fellowship during the
65
tenure of this study. The authors appreciate referees and editors for meticulous editing of this
manuscript.
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The amount and composition of ash remaining after combustion of plant material varies considerably according to the part of the plant, age, cultural treatment etc. Thus, in a young leaf the ash may constitute approximately 5 per cent of the dry weight while in the mature leaf it may be 15 per cent. The ash content of the wood (of the order of 5 per cent) is usually much lower than that of the bark (up to 20 per cent).