Uptake of certain heavy metals from contaminated soil by mushroom—Galerina vittiformis

Uptake of certain heavy metals from contaminated soil by mushroom—Galerina vittiformis

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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: Received 8 May 2013 Received in revised form 21 October 2013 Accepted 23 October 2013

Remediation of soil contaminated with heavy metals has received considerable attention in recent years. In this study, the heavy metal uptake potential of the mushroom, Galerina vittiformis, was studied in soil artificially contaminated with Cu (II), Cd (II), Cr (VI), Pb (II) and Zn (II) at concentrations of 50 and 100 mg/kg. G. vittiformis was found to be effective in removing the metals from soil within 30 days. The 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 mushroom. The metal removal rates by G. vittiformis was analyzed using different kinetic rate constants and found to follow the second order kinetic rate equation except for Cd (II), which followed the first order rate kinetics. & 2013 Elsevier Inc. All rights reserved.

Keywords: Bioaccumulation factor Remediation Heavy metals Mushroom Soil contamination Galerina vittiformis

1. Introduction 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; ATSDRCERCLA 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).


Corresponding author. Fax: þ 91 8242 474 033. E-mail addresses: [email protected], [email protected] (B. Raj Mohan).

Over the last decades, biosorption has emerged as a promising 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 depuration 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

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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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the studies of their heavy metal interaction in soil, Gast et al. (1988) have reported that mushrooms can build up larger concentrations 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 mycofilteration 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 mechanism 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

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: BAF ¼

Conc: of metal in dried biomass ðmg=kgÞ 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 bioaccumulation 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.

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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3. Results and discussion


of the bioaccumaltion process in both mycelia and the fruting bodies of the macrofungi.

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 dumping 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 Basidiomycetes 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

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 contaminated with 50 and 100 mg of heavy metal/kg soil. The bioaccumulation 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 concentrations 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. 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 incubation 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

Table 1 Morphological characteristics of isolated fungal species. Fungal name

Morphological characteristics

Mushroom genus


M1 M2 M3 M4 M5

White colored with slight brownish spot on the center of cap Pure white colored fleshy stem Chocolate brown colored stem and cap Flesh colored stem and cap Large corel shape having golden yellow colored gills and white colored outer covering Small brownish small slender stem Reduced stem with yellow spores Dark brown small and slender stem Blackish large jelly cup appearance. Star like appendages with puff ball like sporangia bearing black spores.

Agaricus Sp Clitocybe Sp Unidentified Pholiota Sp Pleurotus Sp

In woodland, hedgerows and gardens In woodland, hedgerows and gardens In woodland In woodland, hedgerows and gardens Soil rich in decaying logs

Galerina Sp Pleurotus Sp Coprinus Sp Pachyella Sp Geastrum Sp

In mixed woods Soil rich in decaying logs In woodland, hedgerows and gardens In woodland, hedgerows and gardens In woodland, hedgerows and gardens

M6 M7 M8 M9 M10

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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Fig. 1. (A) Tolerance profile of fungal isolates at 1000 mg/l concentrations of metals 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.

Fig. 2. (A) Bioaccumulation profile of metals in Galerina vittiformis at different incubation time (100 mg/kg) and (B) soil pH. 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

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Table 2 Heavy metal content in fruiting body (Sporocarp) of various tolerant mushrooms. Sl. No Mushroom Species



Agaricus bisporousa Boletus edulisa Lepiota rhacodesb Paxillus rubicondulusa Agaricus bisporousa

Pb (4), Cd (3.48), Cu (5) Cu (66.4), Cd (6.58), Pb (3.03) Pb (66), Cd (3.7) Pb (0.69), Cd (0.78), Cu (51.0) Zn (16.8) Cu (107),Pb (1),Zn (57)

Srivastava et al. (2006)


Havlvella leucomelaenab Pleurotus spa

Pb (4.8), Cd (0) Pb (3.4), Cd (1.18), Cu (13.6), Zn (9.8)

Mitra (1994)


Tricholoma terreuma Havlvella leucomelaenab

Cu (5), Zn (179), Cd (0.56), Pb (4.4) Pb (3.1), Cd (1.1)

Demirbas (2002)


Paxillus involutusb Rhizopogonaceae luteolusa Omphalotous oleariusb Hygrophorous hedyriciib Ciocybe dealbatab Lepiota albab

Cu Cu Cu Cu Cu Cu


Tricholoma terreumb Agaricus bisporousa

Pb (4), Cd (1.6), Cu (35.8), Zn (48.0) Pb (0.8), Cd (0.78)


Pseudevernia furfuraceaeb Scorpiurum circintumb

Al (12.51), As(0.23), Cd (0.19), Cu (2.5), Cr(0.11),Pb (5.1), Zn(17.9), Mn(12.9) 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)


Aspergillus foeitidusb

Al (32.5), Co (5.95), Cr (6.23), Mg (44.9), Zn (2.4), Ni (189.5)

Ge et al. (2011)


Poria Spb Nectria cinnabarinaa Gonoderma lucidiuma Paragyrodous sphaerosporousa Polyporous frondosisa

Zn (90.3), Cu (30.8), Pb (1.0), Mn (31.3), Cd (0.1) Zn (30.1), Cu (29.3), Pb (1.9), Cd (0.2), Mn (19.3) Zn(60.1), Cu (43.8), Pb (0.7), Mn (30.4), Cd (0.31) Zn (115), Cu (34.4), Pb (0.4), Mn (37.3), Cd (0.2)

Ita et al. (2006) Sesli and Denchev (2008)


Phellinus badiusb Phellinus sanguineusb

Cd (110), Cu (60), Hg (61), Ni (56) Cd (80), Cu (42), Hg (35), Ni (66)


Tricoloma terreumb Boletus badiusa Russula delicaa

Pb (3.64), Cu (34.86), Cd (0.67), Zn (54.13), Cr (2.54) Cu (44.54), Pb (4.48), Cd (0.91), Zn (34.17), Fe (264.62), Cr (2.86) Cu(19.55), Pb (2.02), Cd (1.22), Zn (38.5), Cr (6.95)


Pleurotous platypusa Agaricus bisporousa

Cd (34.9), Pb (27.10) Cd (33.7), Pb (29.67)


Lactarius deliciousa Rhizopogon roseolousa Russula delicaa

Cd (0.26), Cr (0.12), Cu (6.15), Pb (0.73), Zn (76.7) Cd (0.18), Cr (0.10), Cu (21.2), Pb (2.03), Zn (36.7) Cd (0.42), Cr (0.27), Cu (52.2), Pb (0.77), Zn (58.2)

Sarcosphaeera crassaa Cantharellus cibariusa Suillus luteusa Morchella rigidaa Agarocybe aegeritaa

Ag Ag Ag Ag Ag

Agaricus arvensisa Agaricus silvicola1 Macrolepiota procerab Lycoperdon perlatuma

Cd (117) Cd (67.9) Pb (53.8) Pb (50)

Galerina Spb

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



16 a

Metal content in sporocarp, mg kg-1 of dry wt.

Turkekuel et al. (2004)

(57.0), Pb (1.6.0), Fe (991), Cd (0.84), Pb (3) (13), Zn (30), Mn (13), Fe (620), Cd (0.26), Pb (2.8). (21), Zn (27), Mn (36), Fe (95), Cd (1.3), Pb (5.2). (37), Zn (97),Mn (11), Fe (395), Cd (1.2), Pb (2.7) (41), Zn (115), Mn (30), Fe (386), Cd (0.86), Pb (3.2) (29), Zn (86), Mn (22), Fe (779), Cd (0.8), Pb (5.8)

Yilmaz and Melek (2003), Kalac and Svoboda (2000)

Zhu et al. (2011)

Zn (120.1), Cu (34.4), Pb (0.4), Mn (37.3), Cd (0.2) Baldrian (2003), Falandysz et al. (2012)

Isildak et al. 2007 Vimala et al. 2009

(0.044), As (8.03), Cd (0.016), Cr (0.98), Pb(0.02) (0.022), As (0.03), Cd (0.036), Cr (0.69), Pb (0.04) (0.015), As (0.15), Cd (0.034), Cr (0.15), Pb (0.06) (0.087), As (0.24), Cd (0.007), Cr (0.44), Pb (0.02) (0.074), As (0.44), Cd (0.010), Cr (0.25), Pb (0.018)

Cayır et al. (2010), Sesli and Denchev (2008)

Konuk et al. (2007)

Petkovsek and Pokorny (2013)

Edible 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


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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 mushroom 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

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 mushrooms, 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 (summarized 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).

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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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 bioaccumulation 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.


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 mycoremediation 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

Table 3 Bioaccumulation Factor (BAF) for metals in mushroom, G.vittiformis. Organisms


Conc. (mg/kg)









1.044 1.334



0.29 0.98

Cr(VI) F.Bb






















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

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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 screening 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 establishment 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 bioaccumulation 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), mycoremediation 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.

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