Ecotoxicology and Environmental Safety ∎ (∎∎∎∎) ∎∎∎–∎∎∎

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Ecotoxicology and Environmental Safety

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Uptake of certain heavy metals from contaminated soil

by mushroom—Galerina vittiformis
Dilna Damodaran, K. Vidya Shetty, B. Raj Mohan n
Department of Chemical Engineering, National Institute of Technology Karnataka, Surathkal, Srinivasnagar 575025, India

art ic l e i nf o a b s t r a c t

Article history: Remediation of soil contaminated with heavy metals has received considerable attention in recent years.
Received 8 May 2013 In this study, the heavy metal uptake potential of the mushroom, Galerina vittiformis, was studied in soil
Received in revised form artificially contaminated with Cu (II), Cd (II), Cr (VI), Pb (II) and Zn (II) at concentrations of 50 and
21 October 2013
100 mg/kg. G. vittiformis was found to be effective in removing the metals from soil within 30 days. The
Accepted 23 October 2013
bioaccumulation factor (BAF) for both mycelia and fruiting bodies with respect to these heavy metals at
50 mg/kg concentrations were found to be greater than one, indicating hyper accumulating nature by the
Keywords: mushroom. The metal removal rates by G. vittiformis was analyzed using different kinetic rate constants
Bioaccumulation factor and found to follow the second order kinetic rate equation except for Cd (II), which followed the first
Remediation
order rate kinetics.
Heavy metals
& 2013 Elsevier Inc. All rights reserved.
Mushroom
Soil contamination
Galerina vittiformis

1. Introduction Over the last decades, biosorption has emerged as a promising

The invasion of industrialization, usage of chemicals in agriculture
and the improper waste disposal practices has accelerated soil
contamination round the globe. The most common soil contaminants
constitute heavy metals, herbicides, pesticides and hydrocarbons.
Among these, heavy metals owe a major share due to their
cytotoxicity, mutagenicity, and carcinogenic nature (Hamman,
2004; Mahavi, 2005). Many elements viz. arsenic, cadmium, mercury,
etc. are toxic to living organisms even at trace levels. Soil and ground
water quality data reported by Central Pollution Control Board, India
reveal that heavy metals like Cadmium, Lead, Mercury, Chromium,
Cobalt, Zinc, Nickel and Manganese are the key pollutants which
need immediate mitigation measures (Kamyotra, 2009; ATSDR-
CERCLA 2007). Cases of heavy metal contamination in river banks,
agricultural fields and landfills have been reported (Milenkovic et al.,
2005; Cheng, 2002). Several methods like, chemical precipitation,
coagulation with alum or iron salts, membrane filtration, reverse
osmosis, ion-exchange and adsorption are used to remove metals
from wastes (Francis et al., 1999; Salt et al., 1995). These processes are
suitable from a technological perspective, but are not economically
promising for large scale soil remediation (Chen et al., 2000; Diels
et al., 1999).
n
Corresponding author. Fax: þ 91 8242 474 033.
E-mail addresses: rajmohanbala@gmail.com,
balakrishnan.sreejith@gmail.com (B. Raj Mohan).
low cost methodology for the removal of metals from waste water,
where, microorganisms are employed to remove and recover heavy
metals from aqueous solutions (Chen et al., 2000; Durali et al., 2005;
Bardan et al., 2012; Morsy et al., 2010; Mistra et al., 2012). In this
process, the uptake of heavy metals and radioactive compounds
occurs due to physico-chemical interactions of metal ions with
cellular compounds of the biological entities (Kapoor et al., 1999).
Further, the metal removal mechanism by microorganisms are
complex processes that depends on the chemistry of metal ions, cell
wall compositions of microorganisms, cell physiology and phyto
chemical factors like pH, temperature, time, ionic strength and metal
concentration (Morsy et al., 2010).
Utilization of plants for elimination and uptake of heavy metals
for soil is another important remediation measure adopted. The
scope of phytoremediation as a solution to heavy metal pollution on
soil is often limited by factors like selectivity of plant, climatic
inhibitions, tolerance to heavy metals and contamination by depura-
tion back into the soil. The situation demands the need of a robust
methodology which can go hand in hand with other techniques for a
quicker, more effective and economical remediation.
In this context, the potential of macro fungi belonging to
Basidiomycetes holds promise as an effective biosorbent of toxic
metals from soil in a process referred to as mycoremediation.
Mushroom mycelia can serve as biological filters and as potential
sorbents since their aerial structures consist of large biomasses
with tough texture and affinity towards metals and other chemical
pollutants (Volesky and Holan, 1995; Sesli et al., 2008). Based on

0147-6513/$ - see front matter & 2013 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.ecoenv.2013.10.033

Please cite this article as: Damodaran, D., et al., Uptake of certain heavy metals from contaminated soil by mushroom—Galerina
vittiformis. Ecotoxicol. Environ. Saf. (2014), http://dx.doi.org/10.1016/j.ecoenv.2013.10.033i
2 D. Damodaran et al. / Ecotoxicology and Environmental Safety ∎ (∎∎∎∎) ∎∎∎–∎∎∎
the studies of their heavy metal interaction in soil, Gast et al.
(1988) have reported that mushrooms can build up larger con-
centrations of heavy metals such as lead, cadmium and mercury in
comparison to plants. The fungal mycelia usually spread over the
available area and accumulates metal ions in their cytosol under
suitable conditions. The mycelia mimic the roots of the plants in
extracting heavy metals from contaminated soil, known as myco-
filteration that leads to mycoremediation of contaminated soil. The
bioaccumulation of heavy metals in macro fungi are affected by
certain environmental factors and life cycle of the mushroom viz.,
humus, pH, metal concentration, size and age of the fruiting body,
age of mycelia, type and amount of enzymes and proteins
produced by the mushrooms (Srivastava et al., 2006; Sesli et al.,
2008; Falandysz et al., 2012).
Thus it can be inferred that fungi possess an effective mechan-
ism that capacitates the uptake some trace elements from the
contaminated soil more efficiently than plants. The present paper
reports the bioaccumulation potential of G.vittiformis, a macro
fungus isolated from municipal waste dump yards for the removal
of heavy metals like Cu (II), Cd (II), Cr (VI), Pb (II) and Zn (II) from
the metal contaminated soils in-vitro.
2. Materials and methods
2.1. Isolation of fungal strains
The macro fungi belonging to Basidiomycota phylum are generally known as
Basidiomycetes. These macro fungi that can yield fruiting bodies were collected
from various municipal waste dump yards of Dakshina Kannada District, Karnataka,
India. The mushrooms (fruiting body) were excised using sterile scalpel, washed
with deionized water and surface sterilized using 70 percent alcohol. Sub-culturing
of these mushrooms were done by inoculating the explants, i.e. the totipotent
regions on to petriplates containing Sabourauds dextrose agar medium (SDA) Bai
and Abraham (2002) amended with 100 mg/L of individual heavy metals, Cu (II),
Cd (II), Cr (VI), Pb (II) and Zn (II). Initially the mushrooms were identified based on
their morphological characteristics with reference to mycology literature (Moser,
1983; Breitenbach and Kranzlin, 1995; Bushnell and Hass, 1941) and further
confirmed by 500–600 base pairs ITS analysis.
2.2. Tolerance and screening studies
Heavy metal tolerance test of the isolated mushroom species were carried out
to estimate the concentration of heavy metal ions which macro fungi can tolerate
and produce mycelia. It can be assessed by spot plate assay. The spot plate method
helps to identify the maximum tolerant metal ion concentration in SDA plates
along with the addition of the test metals with concentrations ranging from
100 mg/L to 1000 mg/L were prepared. The isolated fungal species were inoculated
on metal laden SDA and incubated for 5 days at 26 7 2 1C. The growth patterns of
the fungal species were observed and the tolerant concentrations of heavy metals
were determined by visual observation (Aboulroos et al., 2006; Chen et al., 2000).
The fungal species that showed good tolerance against most of the heavy metals
was chosen for further screening studies. The screening process emphasized on the
ability of the fungal species to yield fruiting bodies during the spawning phase of
the Casing studies Martínez-Carrera et al., (2000).
2.3. Preparation of stock solutions
10,000 mg/L of aqueous stock solutions of Cu (II), Cd (II), Cr (VI), Pb (II) and Zn
(II) were prepared by dissolving analytical grade of CuSO4, CdSO4, K2Cr2O7, PbNO3
and ZnNO3 in deionized water, respectively. The stock solutions were used to
contaminate the soil to attain the desired concentrations of these heavy metals (50
and 100 mg/kg of soil) uniformly in the soil media (Oei, 1996; Orazio et al., 2010).
The uniformity of the concentration of the metals was also examined by grid
sampling and analysis.
2.4. Heavy metal bioaccumulation studies in Galerina vittiformis
2.4.1. Heavy metal bioaccumulation studies at mycelial stage of Basidiomycetes
The macro fungi were grown in troughs containing laterite soil ( 42 mm)
artificially contaminated with known concentrations of heavy metals. To analyze
the bioaccumulation capacity of the mycilial stage, 15 ml of basal salt media
consisting of CaCl2, MgSO4, KH2PO4, NH4NO3 and glucose (1 percent) were added
Please cite this article as: Damodaran, D., et al., Uptake of certain heavy metals from contaminated soil by mushroom—Galerina
vittiformis. Ecotoxicol. Environ. Saf. (2014), http://dx.doi.org/10.1016/j.ecoenv.2013.10.033i
to 10 g of soil containing heavy metals at concentrations of 50 and 100 mg/kg to
make the soil slurry for attaining uniform metal distribution. The system was
maintained at pH 6.8 for fungal mycelial growth and incubated at 26 72 1C for
seven days (Cho et al., 2000; Sesli and Tuzen, 1999). The mycelial mat thus obtained
was washed thoroughly with sterile water to remove the traces of the soil media.
The biomass was then dried in a hot air oven at 60 1C until a consistent weight was
obtained. The soil portion, after separation from the biomass was also dried in
similar manner and the metal concentrations of both the dry biomass and soil were
measured using atomic absorbtion spectrometer (Model AAS: GBC-6000) as
described in Section 2.5.3.
2.4.2. The effect of pH and incubation time on bioaccumulation of heavy metals using
G. vittiformis
Major factors affecting the bioaccumulation of heavy metals are pH and
incubation time (Morsy et al., 2010; Chen et al., 2000). Hence, the effect of soil
pH (ranging from 5 to 8) and incubation time of the system for heavy metal
accumulation were carried out by flask studies. The fungi were grown in flasks
containing the soil slurry for a period of 40 days, harvested at every 5 days intervals
and analyzed for metal concentration in both soil and biomass by AAS.
2.4.3. Determination of heavy metal concentration in soil and mycelia
The dried biomass was subjected to microwave assisted digestion (Haswell
1991). The heavy metal content in the digested biomass was analyzed using atomic
absorption spectrometer (AAS Model AAS: GBC-6000, Australia) and was expressed
as a ratio of the mass of the heavy metal to that of the biomass (mg/kg). As for the
heavy metal concentration in soil, the oven dried soil was digested with 2 ml of 65
percent HNO3 and 6 ml of HCl per gram of soil at 600 W in microwave digester
(MARS: CEM, USA). The digest was filtered and after making up the volume of the
filtrate to 50 ml, the metal content in the digest was analyzed using AAS (Srivastava
et al., 2006).
2.4.4. Heavy metal bioaccumulation in the fruiting bodies of Basidiomycetes
The Basidiomycetes that showed better accumulation of heavy metals in the
mycelial stage were selected for Spawning studies. Casing process was carried out
in Plastic trays of 25  20  5 cm3 dimensions, sterilized with 70 percent alcohol.
3.8 cm thickness of soil layer was prepared by using salts of PbNO3, CdSO4, CuSO4,
K2Cr2O7 and ZnNO3 i.e., heavy metals Cu (II), Cd (II), Cr (VI), Pb (II) and Zn (II), and
added to the soil at concentrations of 50 and 100 mg/kg along with saw dust as the
bulking agent, in the ratio of 3:1 (w/w) for lab scale bioaccumulation studies.
Spawns were grown in the dark at 20–24 1C and 80–90 percent relative humidity
for a period of 25 days with periodical monitoring. At the end of the 25th day, the
fruiting bodies were harvested using sterile forceps and allowed to dry at room
temperature. The one gram of dried sample was digested using 4 ml of 65 percent
HNO3 and 2 ml of 30 percent H2O2 in a microwave digestion system(1200 W for
15 min) (Tuzen et al., 2007; Falandysz et al., 2012). The digested mixtures were
cooled and 20 ml of deionized water was added to it. Further the mixture was
heated for 4 h at 150 1C and made up to a volume of 25 ml with deionized water.
These samples were filtered and analyzed for metal contents using, AAS (Oei 1996;
Haswell 1991).
2.5. Determination of bioaccumulation factor (BAF)
The bioaccumulation factor (BAF)/ Efficiency factor is defined as:
Conc: of metal in dried biomass ðmg=kgÞ
BAF ¼
Conc: of metal in the soil ðmg=kgÞ
The ratio of the metal concentration in the bioaccumulator to the metal
concentration in its environment is considered to be the measure of bioaccumula-
tion efficiency. BAF value greater than 1 indicates high accumulation potential of
mushrooms (Vanloon and Lichwa, 1973; Scragg, 2005; Durali et al. 2005). Hence
the BAF values for the mushrooms were estimated for the given metals. The
bioaccumulation factor was calculated for both mycelia and fruiting bodies after 30
days of incubation. For the determination of bioaccumulation factor in the fruiting
body, the metal concentrations in the soil and the fruiting body were analyzed after
harvesting the matured fruiting bodies.
2.6. Kinetics of metal removal
To study the removal rate of heavy metals from the soil using the mushrooms,
it is grown in metal contaminated soil slurry (50 mg/kg) under favorable conditions
for 40 days. The biomass is recovered every day after initial 5 days of incubation
(lag phase of growth). The biomass was then dried in oven (Orbiteck, India), these
dried biomass were acid digested using microwave digesters and the heavy metal
content were analyzed using AAS. The data obtained were analyzed with various
equations to deduce the mechanism.
 D. Damodaran et al. / Ecotoxicology and Environmental Safety ∎ (∎∎∎∎) ∎∎∎–∎∎∎
3. Results and discussion
3.1. Isolation of fungal strains
Ten fungal species were collected from two different municipal
waste deposited areas of Dakshina Kannada District, Karnataka,
India. The habitat, edibility and species of these isolates are
presented in Table 1. All the 10 isolates were found to fall under
Basidiomycetes. Out of 10 isolates, 9 fungal isolates found to have
successful growth on Sabourauds Dextrose Agar medium (SDA).
However, the literature also reveals that very few researchers have
isolated heavy metal accumulating mushrooms from waste dump-
ing sites with a perspective of health effects on consumption of
these mushrooms (Susan et al., 2008; Chen et al., 2009; Dermirbas
et al., 2002; Elekes et al., 2010; Krebs et al., 1999; Soylak et al.,
2005). Thus the isolation of mushrooms based on their heavy
metal tolerance was screened for further studies.
3.2. Heavy metal tolerance study
All the succesfull isolates were tested for their maximum
tolerence level to different heavy metals, (Cu (II), Cd (II), Cr (VI),
Pb (II) and Zn (II)) in the soil slurry. The isolates of Basidomycetes
were grown on 100, 200, 500, 800, and 1000 ppm concentrations
of the above metioned metals. The concentrations of the heavy
metals in soil that showed little/no growth of the mycelia was
identified by the spot plate method. The metal concentartions
used in bioaccumulation studies were lower than those used for
tolerence study. However, the mushrooms that showed higher
MICs for metals were selected for further bioaccumulation studies.
Thus, out of 10 isolated Basidomycetes, six isolates were found to
have high tolerence for all the heavy metals under study and the
tolerance profile were found to be in the order, M2, M3, M5, M6,
M7 and M9 (Fig. 1(A)). Maximum tolerence for Cu (II) was
exhibited by M6 at 300 mg/ml; for Cr (VI) by M7 at 900 mg/L;
for Cd (II), Zn (II) and Pb (II) by M5 at 700 mg/ml, 800 mg/ml and
1000 mg/ml respectively. However, M6, M7 and M9 also exhibited
tolerance level upto 900 mg/ml for Pb (II).
3.3. Bioaccumulation studies
The macro fungi, G.vittiformis belonging to the genera Basidiomy-
cetes show an haplodiplontic life cycle in which two stages occur i.e
mycelial stage and fruiting bodies. Where the mycelial is common
and fruiting bodies do occur only in favorable environment. However
the fruiting body is the fleshy one where higher biomass can
accumulate accpreciable quantities of heavy metals compared to
the mycelia forms. Hence the present study monitored the efficiency
Table 1
Morphological characteristics of isolated fungal species.
Fungal Morphological characteristics
name
M1 White colored with slight brownish spot on the center of cap
M2 Pure white colored fleshy stem
M3 Chocolate brown colored stem and cap
M4 Flesh colored stem and cap
M5 Large corel shape having golden yellow colored gills and white
colored outer covering
M6 Small brownish small slender stem
M7 Reduced stem with yellow spores
M8 Dark brown small and slender stem
M9 Blackish large jelly cup appearance.
M10 Star like appendages with puff ball like sporangia bearing
black spores.
Please cite this article as: Damodaran, D., et al., Uptake of certain heavy metals from contaminated soil by mushroom—Galerina
vittiformis. Ecotoxicol. Environ. Saf. (2014), http://dx.doi.org/10.1016/j.ecoenv.2013.10.033i
3
of the bioaccumaltion process in both mycelia and the fruting bodies
of the macrofungi.
3.3.1. Mycelial studies
The mushrooms M5, M6 and M9 showed higher tolerance
potential and were successful in spawn production after 30 days of
incubation which is an indication that they can be established
in-vitro. Hence, these three mushrooms were selected for further
bioaccumulation studies and were grown on soil slurry contami-
nated with 50 and 100 mg of heavy metal/kg soil. The bioaccu-
mulation profile of heavy metals (Cu (II), Cd (II), Cr (VI), Pb (II) and
Zn (II) ) at an initial concentration of 100 mg/kg of soil by the
above three isolate are shown in (Fig. 1(B)). It was found that the
mushroom M6 is efficient in bioaccumulating metals viz. Cu (II),
Cd (II) and Pb (II) compared to M5 and M9. However, M5 was
found to have better bioaccumulation of Zn (II) than M9 and M6
while M9 showed least accumulation for all the heavy metals.
A similar trend was observed at 50 mg/kg heavy metal concen-
trations in soil. From the results, it can be concluded that
mushroom M6 is more efficient in bioaccumulating heavy
metals from soil compared to the other two. The sequence of
bioaccumulation potential of M6 during its mycilial stage under
the given condition is found to be Cd (II) 4 Pb (II) 4 Cu (II) 4
Zn (II) 4 Cr (VI).
Mushrooms M5, M6 and M9 were identified by 500–600 base
pairs ITS analysis and found to be Pleurotus ostreatus, Galerina
vittiformis and Pachyella clypeata respectively.
3.3.1.1. Effect of incubation time. The incubation time required for
maximum bioaccumulation for metal concentrations at 50 and
100 mg/kg of soil were analyzed. Since from the initial studies was
observed that the yield of the biomass and heavy metal
concentration in the biomass were found to remain constant for
concentrations higher than 100 mg/kg of soil. The results obtained
for 100 mg/kg of soil are shown in Fig. 2(A) and are found to be as
follows: Cu (II) 553 mg/kg, Cd (II) 618 mg/kg, Cr (VI) 298 mg/kg,
Pb (II) 595 mg/kg and Zn (II) 368 mg/kg. The accumulations of
heavy metals at 50 mg/kg concentration of heavy metals within a
period of 30 days are Cu (II) 590 mg/kg, Cd (II) 780 mg/kg, Pb (II)
699 mg/kg and Zn (II) 443 mg/kg respectively were found to get
accumulated in the fruiting body.
It was also found that there was hardly any metal accumulation
by M6 for the first 10 days of incubation whereas, a significant
amount of accumulation was observed for the rest of the incuba-
tion period. The mushroom G. vittiformis is found to be more
efficient in accumulating heavy metals when compared to other
edible mushroom species studied by Isildak et al. (2004), Zhu et al.
(2011) and Dermirbas (2001), hence it is evident that non edible
species of mushrooms accumulate higher concentrations of heavy
Mushroom genus Habitat
Agaricus Sp In woodland, hedgerows and gardens
Clitocybe Sp In woodland, hedgerows and gardens
Unidentified In woodland
Pholiota Sp In woodland, hedgerows and gardens
Pleurotus Sp Soil rich in decaying logs
Galerina Sp In mixed woods
Pleurotus Sp Soil rich in decaying logs
Coprinus Sp In woodland, hedgerows and gardens
Pachyella Sp In woodland, hedgerows and gardens
Geastrum Sp In woodland, hedgerows and gardens
4 D. Damodaran et al. / Ecotoxicology and Environmental Safety ∎ (∎∎∎∎) ∎∎∎–∎∎∎

Fig. 2. (A) Bioaccumulation profile of metals in Galerina vittiformis at different

Fig. 1. (A) Tolerance profile of fungal isolates at 1000 mg/l concentrations of metals
incubation time (100 mg/kg) and (B) soil pH.
and (B) Bioaccumulation profile of fungal isolates M5, M6 and M9 mycelia at
100 mg/kg metals in soil.

metals from the soil in compari nter parts thus preventing the
heavy metal accumulation in the food chain (Table 2). The
significant (Cu (II), Cd (II), Cr (VI), Pb (II) and Zn (II)) accumulating
efficiency of the mycelial stage of G. vittiformis within a short
period of 30 days, attests the potential of this nonedible macro
fungi as an efficient bio accumulator when compared to other
fungal species mentioned in the literature.
3.3.1.2. Effect of pH. Soil pH can be regarded as one of the critical
parameters in controlling the growth and accumulation of heavy
metals by fungi (Chen et al., 2000; Wuyep et al., 2007). To examine
the effect of pH on the bio-accumulation capacity of G. vittiformis, the
mushroom was subjected for bioaccumulation studies of Cu (II), Cd
(II), Cr (VI), Pb (II) and Zn (II) metals from soil slurry at different pH
values ranging from pH 5 to pH 8 for a period of 30 days.

Please cite this article as: Damodaran, D., et al., Uptake of certain heavy metals from contaminated soil by mushroom—Galerina
vittiformis. Ecotoxicol. Environ. Saf. (2014), http://dx.doi.org/10.1016/j.ecoenv.2013.10.033i
 D. Damodaran et al. / Ecotoxicology and Environmental Safety ∎ (∎∎∎∎) ∎∎∎–∎∎∎ 5

Table 2
Heavy metal content in fruiting body (Sporocarp) of various tolerant mushrooms.

Sl. No Mushroom Species Metal content in sporocarp, mg kg-1 of dry wt. References

1 Agaricus bisporousa Pb (4), Cd (3.48), Cu (5) Srivastava et al. (2006)

Boletus edulisa Cu (66.4), Cd (6.58), Pb (3.03)
Lepiota rhacodesb Pb (66), Cd (3.7)
Paxillus rubicondulusa Pb (0.69), Cd (0.78), Cu (51.0) Zn (16.8)
Agaricus bisporousa Cu (107),Pb (1),Zn (57) Turkekuel et al. (2004)

3 Havlvella leucomelaenab Pb (4.8), Cd (0) Mitra (1994)

Pleurotus spa Pb (3.4), Cd (1.18), Cu (13.6), Zn (9.8)

4 Tricholoma terreuma Cu (5), Zn (179), Cd (0.56), Pb (4.4) Demirbas (2002)

Havlvella leucomelaenab Pb (3.1), Cd (1.1)

5 Paxillus involutusb Cu (57.0), Pb (1.6.0), Fe (991), Cd (0.84), Pb (3)

Rhizopogonaceae luteolusa Cu (13), Zn (30), Mn (13), Fe (620), Cd (0.26), Pb (2.8). Yilmaz and Melek (2003), Kalac and Svoboda (2000)
Omphalotous oleariusb Cu (21), Zn (27), Mn (36), Fe (95), Cd (1.3), Pb (5.2).
Hygrophorous hedyriciib Cu (37), Zn (97),Mn (11), Fe (395), Cd (1.2), Pb (2.7)
Ciocybe dealbatab Cu (41), Zn (115), Mn (30), Fe (386), Cd (0.86), Pb (3.2)
Lepiota albab Cu (29), Zn (86), Mn (22), Fe (779), Cd (0.8), Pb (5.8)

6 Tricholoma terreumb Pb (4), Cd (1.6), Cu (35.8), Zn (48.0) Zhu et al. (2011)

Agaricus bisporousa Pb (0.8), Cd (0.78)

7 Pseudevernia furfuraceaeb Al (12.51), As(0.23), Cd (0.19), Cu (2.5), Cr(0.11),Pb (5.1), Zn(17.9), Mn(12.9)
Scorpiurum circintumb Al(17.51), As (0.32), Cd(0.35), Cu (3.2), Cr (1.1), Pb(6.3), Zn (46.1), Mn (46.7) Basile et al. (2008)

8 Aspergillus foeitidusb Al (32.5), Co (5.95), Cr (6.23), Mg (44.9), Zn (2.4), Ni (189.5) Ge et al. (2011)

9 Poria Spb Zn (90.3), Cu (30.8), Pb (1.0), Mn (31.3), Cd (0.1)

Nectria cinnabarinaa Zn (30.1), Cu (29.3), Pb (1.9), Cd (0.2), Mn (19.3) Ita et al. (2006)
Gonoderma lucidiuma Zn(60.1), Cu (43.8), Pb (0.7), Mn (30.4), Cd (0.31) Sesli and Denchev (2008)
Paragyrodous Zn (115), Cu (34.4), Pb (0.4), Mn (37.3), Cd (0.2)
sphaerosporousa
Polyporous frondosisa Zn (120.1), Cu (34.4), Pb (0.4), Mn (37.3), Cd (0.2)

10 Phellinus badiusb Cd (110), Cu (60), Hg (61), Ni (56) Baldrian (2003), Falandysz et al. (2012)
Phellinus sanguineusb Cd (80), Cu (42), Hg (35), Ni (66)

11 Tricoloma terreumb Pb (3.64), Cu (34.86), Cd (0.67), Zn (54.13), Cr (2.54)

Boletus badiusa Cu (44.54), Pb (4.48), Cd (0.91), Zn (34.17), Fe (264.62), Cr (2.86) Isildak et al. 2007
Russula delicaa Cu(19.55), Pb (2.02), Cd (1.22), Zn (38.5), Cr (6.95)

13 Pleurotous platypusa Cd (34.9), Pb (27.10) Vimala et al. 2009

Agaricus bisporousa Cd (33.7), Pb (29.67)

14 Lactarius deliciousa Cd (0.26), Cr (0.12), Cu (6.15), Pb (0.73), Zn (76.7)

Rhizopogon roseolousa Cd (0.18), Cr (0.10), Cu (21.2), Pb (2.03), Zn (36.7) Cayır et al. (2010), Sesli and Denchev (2008)
Russula delicaa Cd (0.42), Cr (0.27), Cu (52.2), Pb (0.77), Zn (58.2)

15 Sarcosphaeera crassaa Ag (0.044), As (8.03), Cd (0.016), Cr (0.98), Pb(0.02)

Cantharellus cibariusa Ag (0.022), As (0.03), Cd (0.036), Cr (0.69), Pb (0.04) Konuk et al. (2007)
Suillus luteusa Ag (0.015), As (0.15), Cd (0.034), Cr (0.15), Pb (0.06)
Morchella rigidaa Ag (0.087), As (0.24), Cd (0.007), Cr (0.44), Pb (0.02)
Agarocybe aegeritaa Ag (0.074), As (0.44), Cd (0.010), Cr (0.25), Pb (0.018)

15 Agaricus arvensisa Cd (117)

Agaricus silvicola1 Cd (67.9) Petkovsek and Pokorny (2013)
Macrolepiota procerab Pb (53.8)
Lycoperdon perlatuma Pb (50)

16 Galerina Spb Cd (850), Pb(900), Cu (800), Zn (700), Cr (30)

a
Edible
b
Non edible.

The maximum accumulations for 50 mg/kg were found to be as
follows: Cu (II) (240 mg/kg), Cd (II) (390 mg/kg), Cr (VI) (58 mg/kg), Pb
(II) (690 mg/kg) and Zn (II) (380 mg/kg) at pH 5.5. For 100 mg/kg, the
maximum concentrations were Cu (II) (590 mg/kg), Cd (II) (783
mg/kg), Cr (VI) (213 mg/kg), Pb (II) (670 mg/kg) and Zn (II) (553
mg/kg) at pH 5.5 (Fig. 2(B)). Results infer a higher accumulation of
higher concentrations by G. vittiformis under slightly acidic conditions.
The results obtained are in accordance with reports of Dermirbas
(2002) and Gast et al. (1988) who reported the effect of pH on heavy
metal accumulation for mushrooms like Pleurotus Sp., Agaricus Sp.,
Aspergillus Sp., Rhizopus Sp. etc. At soils having pHs0 above 7, the metal
uptake recovery was found to be remarkably less. This may be due to
the fact that at a higher pH metals might exist in hydroxide colloids
form that comprises of large molecular size and have difficulty in cell
permeation. Moreover the availability of the metals to the mushroom
mycelia may also reduce as they might precipitate at alkaline pH (Niu
et al., 2007). Thus changes due to osmotic pressure and hydrolyzing
effects might retard the metal uptake process from the soil under
alkaline pH conditions (Zhu et al., 2011; Dermirbas, 2001; Durali et al.,
2005; Sesli et al., 2008).
3.3.2. Bioaccumulation in fruiting bodies of mushrooms
As the isolate G. vittiformis showed maximum bioaccumulation
compared to M5 and M9, it was established in in-vitro condition by
Spawning (seeds of Basidomycetes), followed by Casing with soil-saw
dust mixture. The soil-saw dust mixture was artificially contaminated
with metals at different concentrations. Fig. 3(A) and (B) show the

Please cite this article as: Damodaran, D., et al., Uptake of certain heavy metals from contaminated soil by mushroom—Galerina
vittiformis. Ecotoxicol. Environ. Saf. (2014), http://dx.doi.org/10.1016/j.ecoenv.2013.10.033i
6 D. Damodaran et al. / Ecotoxicology and Environmental Safety ∎ (∎∎∎∎) ∎∎∎–∎∎∎
Fig. 3. (A)Galerina vittiformis mycelia showing primodias after 20 days of incubation with metals, and (B) Fruiting body initiation after 25 days of incubation in tray systems.
Fig. 4. Bioaccumulation of metals by Galerina vittiformis fruiting bodies from soil at
an initial metal concentration of 50 mg/kg of soil.
primodias and fruitng body initials of G. vittiformis. From the
observations made during casing studies, it was found that mush-
room G. vittiformis failed to produce fruiting bodies at higher
concentrations (100 mg/kg and above) of certain metals Cr (VI),
Cu (II) and Zn (II). The results of bioaccumulation studies at 50 mg/
kg concentration are presented in Fig. 4. The fruiting bodies formed
after 25 days of the incubation period were harvested and analyzed
for their heavy metal content. The soil in the trays were also analyzed
for heavy metal at the end of 30days where no further fruiting bodies
Please cite this article as: Damodaran, D., et al., Uptake of certain heavy metals from contaminated soil by mushroom—Galerina
vittiformis. Ecotoxicol. Environ. Saf. (2014), http://dx.doi.org/10.1016/j.ecoenv.2013.10.033i
are produced. The levels of heavy metals accumulated in the fruiting
bodies are as follows Cu (II) 800 mg/kg, Cd (II) 852 mg/kg, Cr (VI)
30 mg/kg, Pb (II) 900 mg/kg and Zn (II) 700 mg/kg.
Mushroom G. vittiformis was found to yield significant number
of fruiting bodies in the soil contaminated with the heavy metals
like Cd (II) and Pb (II) at concentration 100 mg/kg of soil. Thus at
higher concentrations of certain metals mushroom0 s heavy metal
accumulation potential gets reduced due to reduction in the
biomass by either reduction in number or absence of fruiting
bodies (due to metal toxicity). The bioaccumulation potential of
fruiting bodies of G. vittiformis were found to be in the following
order Pb (II) 4 Cd (II) 4Cu (II) 4Zn (II) 4Cr (VI).
To determine the site of heavy metal accumulation in mush-
rooms, the metal content of the dried biomass of both pileus and
stalk were analyzed separately using AAS. Results reveal a higher
accumulation of metal in the pileus region of the mushroom in
comparison to its stalk (Fig. 5). An accumulation efficiency of
about 70–80 percent of heavy metals (Cu (II), Cd (II), Cr (VI), Pb (II)
and Zn (II)) was observed in the fleshy pileus rather than its stalk.
Similar phenomena have been observed by various researchers in
their studies on metal accumulation by mushrooms (Zhu et al.,
2010, Falandysz et al., 2012; Chen et al., 2009, Falandysz et al.,
2007, Yilmaz and Melek, 2003, Cayer et al., 2010; Soylak et al.,
2005: Durali et al., 2005: Sesli et al., 2008).
The bioaccumulation potential of G. vittiformis was found to be
higher than those mushroom species reported in literature (sum-
marized in Table 2), even though the comparison cannot be
justified as the metal concentrations in the soil environment is
not reported in most of the cases. Our results reveal that non
edible mushroom species accumulate higher amounts of metal
ions than the edible species: however, the bioaccumulation profile
indicates that metal accumulation capability is species specific and
mainly depends on its accumulation mechanism (Wuyep et al.,
2007; Niu et al., 2007; Zhu et al., 2011; Dermirbas, 2001; Yilmaz
and Melek, 2003; Durali et al., 2005; Mitra, 1994; Turkekuel et al.,
2004;Soylak et al., 2005).
 D. Damodaran et al. / Ecotoxicology and Environmental Safety ∎ (∎∎∎∎) ∎∎∎–∎∎∎
3.4. Determination of biaccumulation factor (BAF)
The BAF of mushroom G.vittiformis both in mycelial form and in
fruiting bodies from the soil are represented in Table 3. It was
observed that BAF values for G. vittiformis decreases with increase
in initial metal concentration, indicating a reduced bioaccumula-
tion capability due to enhanced metal stress. The BAF values of
G. vittiformis for Cu (II), Cd (II), Pb (II) and Zn (II) were found to be
above one at an initial metal concentration of 50 mg/kg indicating
its applicability as bioremediating agent. Based on the values of
BAF presented in Table 3, the mushroom G. vittiformis can be
regarded as hyperaccumulator for metals like Cu (II), Cd (II), Pb (II)
and Zn (II). However, G. vittiformis cannot be considered as a good
bioremediating agent for Cr (VI) as its BAF value is less than one
even though it is tolerant for higher concentrations (i.e upto
400 mg/kg) of Cr (VI). The BAF values for mycelial stage of G.
vittiformis were found to be lesser than those with the fruiting
bodies for all the metals under study. Hence, fruiting body stage of
the life cycle of G. vittiformis can be considered to have higher
potential in remediating the soil compared to that of the mycelial
stage. Thus harvesting the fruiting bodies leads to easy removal of
heavy metals from the soil which can be considered as an added
advantage of mycoremediation in bioremediation of soil.
Fig. 5. Concentrations of heavy metals in stalk and pileus tissues of mushroom
Galerina vittiformis.
Table 3
Bioaccumulation Factor (BAF) for metals in mushroom, G.vittiformis.
Organisms Conc. (mg/kg) Cu(II) Cd(II)
Ma F.Bb Ma
G.vittiformis 50 0.82 1.75 1.044
1.334
100 0.65 0.29
0.98
Ma-Mycelia, F.Bb- Fruiting bodies.
Please cite this article as: Damodaran, D., et al., Uptake of certain heavy metals from contaminated soil by mushroom—Galerina
vittiformis. Ecotoxicol. Environ. Saf. (2014), http://dx.doi.org/10.1016/j.ecoenv.2013.10.033i
7
The BAF values of the fruiting bodies of G. vittiformis for Cd (II)
and Pb (II) metals at 100 mg/kg concentrations were found to be
remarkably higher in spite of the observation that the mushroom
failed to yield fruiting body for the the same concentration of other
metals. Thus, it can be inferred that the toxicity of heavy metals, Cu,
Cr and Zn on G. vittiformis was severe enough to supress and skip
the yield of fruiting bodies. Our results are in concordance with
reports of Tuzen (2003) on bioaccumulation of heavy metals like Cd
(II) and Zn (II) from soil using Agaricus macrosporous, Agaricus
silvicola and Stropharia rugosoannulata. Hence, the mycoremedia-
tion of heavy metal contaminated soil can be considered to be
specific for metal concentration and mushroom species.
3.5. Removal kinetics for metal ions
Metal uptake by fungi involves various processes like metal
desorption from soil particles, transport of soluble metals to the
stalk of the mushrooms through the mycelial surfaces via diffusion
or mass flow, and metal translocation from stalks to fruiting
bodies.
To study the kinetics of metal removal using G. vittiformis we
assume that the preliminary mechanism for accumulation of
heavy metals in to the cells is adsorption. The bioaccumulation
values obtained for 40 days were plotted for Langergren pseudo
first and second order kinetic equations. The R2 values obtained for
Langergren pseudo first order kinetic equation are Cd(II): 0.9217,
Cu (II): 0.6524, Zn (II): 0.8661, Pb(II): 0.9618. From this data it is
clear that among the studied metal ions only Cd (II) obeys pseudo
first order kinetics while all other metals follow pseudo second
order kinetic equation (Cd(II): 0.8556, Cu (II): 0.9632, Zn (II):
0.9244, Pb(II): 0.9648). That may be because of the sorption of
cadmium ion onto the surface of the mushroom mycelia. Similar
results were obtained in the studies of biosorption of heavy metals
on to live cells; Lee et al. (1996) explained the adsorption
phenomenon of methylene blue dye on water hyacinth root with
pseudo first order equation. Similarly the removal of Cr (VI) and Cr
(III) using Moss was also explained by Lee et al. 1996. The metal
removal mechanism was explained by psedo first order reactions
as reported by various researchers like Panday et al., 1985; Gupta
et al., 1990; Namasivayam and Yamuna, 1992; Ho et al., 2004.
Experimental data for all the studied metal ions were also
tested with pseudo-second-order kinetic equation, and their R2
values are Cd(II): 0.8556, Cu (II): 0.9632, Zn (II): 0.9244, Pb(II):
0.9648 All the studied metal ions except Cd (II) showed higher R2
values, indicating that the removal mechanism is majorly
governed by surface phenomenon and later depends on the
accumulation capacity of the mushroom species. Many researchers
have reported similar results for metal recovery from both soil and
water (Sari et al., 2011; Ho, 2006).
3.5.1. Intra particle diffusion kinetics
Experimental data were also represented in intra particle
diffusion model and shows a good fit with an R2 value ranging
Cr(VI) Pb(II) Zn(II)
F.Bb Ma F.Bb Ma F.Bb Ma F.Bb
0.22 0.449 0.96 1.24
0.76 1.06
0.08 0.057 0.69 0.89
0.68 0.53 0.69
8 D. Damodaran et al. / Ecotoxicology and Environmental Safety ∎ (∎∎∎∎) ∎∎∎–∎∎∎
from 0.8556 to 0.9556. The R2 values for intra particle diffusion
kinetics were as followes Cd(II): 0.9556, Cu (II): 0.8668, Zn (II):
0.9452, Pb(II): 0.8552. From this data it is evident that the
intercept of all the diffusion equation did not pass through the
origin for all the studied metals indicating that the intra particle
diffusion is not the rate limiting step for the removal process. In
the case of both Zn (II) and Cd (II) the intercept value is negative
which indicates that they do not agree to the existing intra particle
diffusion model.
4. Conclusions
 Removal of Cu (II), Cd (II), Cr (VI), Pb (II) and Zn (II) metals from
contaminated soil using newly isolated macro fungi, G. vittiformis
were investigated in single metal systems.
 The newly isolated strains of macro fungi were initially
screened based on heavy metal tolerance, followed by screen-
ing for their bioaccumulation potential.
 The mushroom G. vittiformis (M6) have higher accumulation
potential in both mycelial and fruiting body stages of its life
cycle when compared to P. clypeata (M5.) and P. ostreatus (M5).
 The soil pH and incubation time was found to have significant
effect on bioaccumulation of metals from the soil slurry during
the mycelial stage of the mushroom, G. vittiformis.
 Wild non-edible mushroom species like G. vittiformis were
found to be more efficient in accumulating the heavy metals
from soil compared to certain edible species like Pleurotus Sp
and Agaricus Sp, thus enhancing the significance of establish-
ment of mycoremediation in large scale.
 Higher BAF values were observed during the presence of
fruiting bodies in the mycelial stage of the mushroom species
indicating the significance of the fruiting bodies in the bioac-
cumulation process, owing to the possession of larger biomass
and better ease of separation from the soil following
remediation.
 The metal removal kinetic data for metal ions like Cu (II), Pb (II)
and Zn (II) follows pseudo- second order equation indicating
the removal mechanism being a function of both metal ions
and nature of mushroom species. In the case of Cd (II), removal
kinetic data follows pseudo-first order equation indicating that
the removal is the function of metal ion transport from the soil
and does not depend on the nature of the mushroom species.
 Applying the removal kinetic data to the intra particle diffusion
equation reveals that the rate of metal ion diffusion through
the cell membrane is not the rate limiting step and hence the
uptake of heavy metals from the soil may be governed by the
diffusion of metals in the soil.
Based on the above mentioned results, it can be concluded that
the wild mushroom species, G. vittiformis is efficient in soil
remediation of heavy metals. Taking into consideration that plants
like Brassica junceae, Phaseolous vulgaris, Triticum aestivum etc.
take much longer duration viz. 3 or 6 months to remove the metals
from the soil (Long et al., 2010; Wuyep et al., 2007), mycoremedia-
tion using G. vittiformis can be considered an alternative to other
known methods for remediating heavy metal contaminated soil.
Appendix A. Supplementary material
Supplementary data associated with this article can be found in the
online version at http://dx.doi.org/10.1016/j.ecoenv.2013.10.033.
Please cite this article as: Damodaran, D., et al., Uptake of certain heavy metals from contaminated soil by mushroom—Galerina
vittiformis. Ecotoxicol. Environ. Saf. (2014), http://dx.doi.org/10.1016/j.ecoenv.2013.10.033i
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