The Bioaccumulation of Some Heavy Metals in the Fruiting Body of Wild Growing Mushrooms

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DOI: 10.15835/nbha3824736 · Source: DOAJ
Abstract
Due to their effective mechanism of accumulation of heavy metals from soil, the macrofungi show high concentrations of metals in their fruiting body. According with this ability, the mushrooms can be used to evaluate and control the level of environmental pollution, but also represent danger for human ingestion. We analyzed some macrofungi species from a wooded area to establish the heavy metal concentrations and ability of bioaccumulation and translocation for Zn, Cu and Sn in fruiting body. The metallic content was established by the Inductively Coupled Plasma-Atomic Emission Spectrometry method (ICP-AES). The minimal detection limits of method is 0.4 mg/kg for Zn and Cu and 0.6 mg/kg for Sn. Heavy metals concentrations in the fruiting body ranged between 6.98-20.10 mg/kg for Zn (the higher value was for Tapinella atrotomentosa); 16.13-144.94 mg/kg for Cu (the higher value was for Hypholoma fasciculare); and 24.36-150.85 mg/kg for Sn (the higher value was for Paxillus involutus). The bioaccumulation factor has important values (higher than 1) only for copper in all the analyzed species (between 1.30 and 8.86) and for tin in Paxillus involutus species (1.19). The translocation factor shows that zinc and tin were accumulated in higher concentrations in cap of mushrooms and the copper had higher concentrations in stipe.

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Not. Bot. Hort. Agrobot. Cluj 38 (2) 2010, Special Issue, 147-151
Print ISSN 0255-965X; Electronic 1842-4309
Notulae Botanicae Horti Agrobotanici
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Introduction
e mushrooms are consumed because of their chemi-
cal and nutritional properties, as for their therapeutic
and preventing disease characteristics due to the chemi-
cal composition (Agrahar-Murugkar and Subbuakshmi,
2005; Manzi et al., 2001). ere is a well-established con-
sumer acceptance of cultivated mushroom, such as Agari-
cus bisporus, Pleurotus spp., Lentinus edodes and other, but
some specic groups of people, seasonally, are traditionally
eating wild mushrooms (Diez and Alvarez, 2001).
Accurate food composition data are estimating the
adequacy of essential nutrients intakes and assessing expo-
sure risk from intake of toxic non-essential metals (Onian-
wa et al., 2001; Soylak et al., 2005). Trace elements above
threshold concentration level, can cause morphological
abnormalities and reduce growth and increase mortality
and mutagenic eects in human bodies (Olumuyiwa et al.,
2007). e bioavailability of iron in mushrooms is there-
fore high and human body can absorb up to 90% of the
present iron (Kalač and Svoboda, 2000).
Because of these, it is necessary to investigate the level
of metals concentration in the wild growing mushrooms.
ey are known to accumulate high levels of several heavy
metals like copper, mercury, lead, zinc and cadmium
(Kalač and Svoboda, 2000).
Numerous data on metals concentrations in the fungal
fruiting bodies were published (Alonso et al., 2003; Coc-
chi et al., 2006; Garcia et al., 1998; Isildak et al., 2004;
Soylak et al., 2005; Svoboda et al., 2006). Because the
macro fungi are integral part of the forest ecosystems,
sometimes the soil-to-mycelium transfer of metals de-
pends on relationship between mycelium and symbiotic
plants species aecting element absorption and transloca-
tion (Malinowska et al., 2004). In addition, the metals are
distributed unevenly within the fruiting body, the highest
concentrations have been observed in the spore-forming
part, but not in the spore, a lower content in the rest of the
cap and the lowest level in the stipe (omet et al., 1999).
High level of metals concentration was observed near met-
als polluted area and metals smelter (Collin- Hansen and
Andersen, 2003; Kalač et al., 1996; Svoboda et al., 2000).
e purpose of this paper is to identify the level of
toxic elements like copper, zinc and tin which are concen-
trated in the fruiting body of some mushrooms collected
from a forest area of Carpathian Mountain, Bucegi Massif.
A comparison between the level of heavy metals in the ed-
ible mushrooms and the toxic mushrooms will be done to
underline the possible danger of the wild growing mush-
rooms consumption.
e Bioaccumulation of Some Heavy Metals in the Fruiting Body of
Wild Growing Mushrooms
Carmen Cristina ELEKES
1)
, Gabriela BUSUIOC
1)
, Gheorghe IONITA
2)
1)
Valahia University of Targoiste, Faculty of Enironmental Engineering and Biotechnologies,
Bd. Regele Carol I, no. 2, Romania; cristina_elekesh@yahoo.com
2)
Valahia University of Targoiste, Faculty of Materials Engineering, Mechatronics and Robotics, Bd. Regele Carol I, no. 2, Romania
Abstract
Due to their eective mechanism of accumulation of heavy metals from soil, the macrofungi show high concentrations of metals
in their fruiting body. According with this ability, the mushrooms can be used to evaluate and control the level of environmental
pollution, but also represent danger for human ingestion. We analyzed some macrofungi species from a wooded area to establish the
heavy metal concentrations and ability of bioaccumulation and translocation for Zn, Cu and Sn in fruiting body. e metallic content
was established by the Inductively Coupled Plasma-Atomic Emission Spectrometry method (ICP-AES). e minimal detection limits
of method is 0.4 mg/kg for Zn and Cu and 0.6 mg/kg for Sn. Heavy metals concentrations in the fruiting body ranged between 6.98-
20.10 mg/kg for Zn (the higher value was for Tapinella atrotomentosa); 16.13-144.94 mg/kg for Cu (the higher value was for Hypholoma
fasciculare); and 24.36-150.85 mg/kg for Sn (the higher value was for Paxillus inolutus). e bioaccumulation factor has important
values (higher than 1) only for copper in all the analyzed species (between 1.30 and 8.86) and for tin in Paxillus inolutus species (1.19).
e translocation factor shows that zinc and tin were accumulated in higher concentrations in cap of mushrooms and the copper had
higher concentrations in stipe.
Keywords: macromycetes, bioaccumulation, translocation factor, zinc, copper, tin
Elekes, C. C. et al. / Not. Bot. Hort. Agrobot. Cluj 38 (2) 2010, 147-151
148
Results and discussion
Soil characteristics
e metal concentrations in the fruiting body of mush-
rooms vary over a wide range within the species, because
of many factors aecting the absorption and accumulation
rate. e soil properties, such as pH, redox potential, or-
ganic matter content, clay mineralogy, caution exchange
capacity of the soil phase, competition with other metal
ions and composition of the soil solution inuence the ab-
sorption of metals in mushrooms (Angeles Garcia et al.,
2009).
Some of the soil characteristics from the sites where the
mushrooms were harvested are present in Tab. 1. e hu-
midity of the analyzed sites has the mean value of 47.53%
because of the high ratio of leaf litter in the analyzed sub-
stratum, and the soil pH reaction is 6.70 due to the high
content of the biological material. e mean amount of
trace metals in the soil was for Zn higher than the nor-
mal value for an organic soil (57-100 mg/kg), and did not
reached this limit for Cu (1-115 mg/kg) (Kabata-Pendias
and Pendias, 1993).
Metal concentrations in mushrooms
In the culinary domain, the mushrooms are very appre-
ciated because of their concentration in minerals. Besides
water (75-95% fresh weight), they has an important con-
tent of carbohydrates (39% dry weight), proteins (17.5%
dry weight) and a low content of lipids (2.9% dry weight)
(Lati et al., 1996). e amount of dry matter of mush-
rooms is species dependent, but also depends on the age
and meteorological condition. A mean percentage of dry
weights for each species of analyzed mushrooms are: Bo-
letus griseus - 26.25%, Collybia butyracea - 33.59%, Tap-
inella atrotomentosus - 9.07%, Paxillus inolutus - 18.01%,
Hypholoma fasciculare - 18.23% and Tricholoma avoi-
rens - 16.17%.
Zinc is one of the important trace metals for a normal
growth and development of humans and mushrooms are
known as well accumulators for this element. Zinc content
in the analyzed mushrooms from Bucegi Massif varies in
the fruiting body of each species. e results obtained for
the zinc concentration (Fig. 1) are in accordance with the
Materials and methods
Biological material
Six species of wild growing mushrooms were harvest
from a wooded area, near Sinaia city, from Bucegi Mas-
sif of Carpathian Mountains. All these macro fungus were
found in deciduous forest, at 800 m altitude, relatively
close to the road Targovisite-Sinaia. ey growth in a cold
period, in November, on the soil, but the mycelium was
founded also in the mixture of litter wood and leaves. e
analyzed species are edible (Collybia butyracea and Boletus
griseus), non-edible (Tapinella atrotomentosus and Paxil-
lus inolutus) or toxic (Hypholoma fasciculare and Tricho -
loma avoirens). e harvested mushrooms were mature,
with sporophore, and were collected the whole fruiting
bodies, caps and stipes.
Analytical methods
For each mushroom, we sample 6-9 exemplars from dif-
ferent places and the substratum near the mycelium, down
to the depth of 5 cm. Both the samples of mushrooms and
soil, and them processing were did with plastic, glass and
pottery instruments to avoid any metal contacts that can
inuence the results.
Aer harvesting, the mushrooms were clean up by the
soil particles, dried at 60ºC and then grinding to ne pow-
der. e soil root surrounding samples were dried at 40ºC
until the complete process, then grinding to a ne powder
and sieved at 250 µm (conform SR ISO 11464).
e Inductively Coupled Plasma - Atomic Emission
Spectrometry method (ICP-AES), did the estimation of
metallic content in the analyzed mushroom and them
soil. For the analyzes with ICP-AES method, the biologi-
cal samples (mushrooms) were mineralized, in Berghof
microwave digestor, by mixture with 10 ml of nitric acid
concentrated 65% and 2 ml of hydrogen peroxide, and for
the soil samples were done hot extractions with nitric acid
1:1.
In present paper, the metals contents of mushrooms
were establish with a 110 Liberty Spectrometer type of
Varian brand. To disintegrate the sample in constituents
atoms or ions is used a plasma source, which will stir up
them on superior energetic layer. ey will revert to the
initial form by the emission of characteristic energy pho-
ton, emission recorded by an optical spectrometer. e
radiation intensity is proportional with each element con-
centration in the sample and is intern calculated by a cou-
ple of calibration curves to obtain directly the measured
concentration.
e concentrations represent the mean of many exem-
plars and are expressed in mg of metal related with kg of
dry soil or plants. e minimal detection limits of the de-
vice ranged according the analyzed element and was 0.4
mg/kg for Cu and Zn; 0.6 mg/kg for Sn.
Tab. 1. Humidity (%), pH and heavy metals contents (mg/kg)
in the studied sampling points of soil from the Bucegi Massif,
Romania
Soil parameters Mean Range Minimum Maximum
Zn
130.80 67.71 94.63 162.34
Cu
46.02 100.56 9.68 110.24
Sn
495.14 1234.69 58.68 1293.37
pH
6.69 0.44 6.48 6.90
Humidity 47.11 26.48 31.48 57.96
Elekes, C. C. et al. / Not. Bot. Hort. Agrobot. Cluj 38 (2) 2010, 147-151
149
concentrations from literature, which have been reported
in the range of 28.6-179.0 mg/kg (Rudawska and Leski,
2005), 43.5-205.0 mg/kg (Sesli et al., 2008) or 45-188
mg/kg (Tuzen, 2003). e zinc concentration is higher in
the cap of the fruiting body than in stipe for all the ana-
lyzed species of mushrooms. For B. griseus and T. avo-
virens, the zinc concentration in the stipe was under the
detection limit of method.
e highest concentration of zinc was founded in non-
edible and toxic species of mushrooms, T. atrotomentosa
(30.05 mg/kg) and T. avoirens (31.85 mg/kg), and the
lowest concentrations of this element were founded in the
edible species, B. griseus and C. butyracea.
Copper concentrations in the accumulating mush-
rooms species are usually 100-300 mg/kg of dry matter,
which is not considered a risk for human health (Kalač and
Svoboda, 2000) and a concentration higher than those in
vegetable should be considered as a nutritional source of
this element (Sesli et al., 2008). For wild growing mush-
rooms, the copper content range between not detectable’
and 169.80 mg/kg, in agreement with the literature val-
ues 15.5-73.8 mg/kg (Sesli et al., 2008), 12-181 mg/kg
(Tuzen, 2003) or 13.4-50.6 mg/kg (Soylak et al., 2005).
In g. 1 we can see the dierences of copper accumulation
in the fruiting body of mushrooms, according with them
edibility. e lower copper concentrations were founded
in the edible mushrooms, and the highest concentrations
in the toxic species of analyzed mushrooms. In addition,
the copper is accumulated in higher quantities in the stipe
of the fruiting body, for all the analyzed species of mush-
rooms.
e concentration of tin in the wild growing species
of mushrooms ranged between 48.73 mg/kg for B. griseus
and 301.70 mg/kg for P. inolutus, the lowest concentra-
tions are also in the edible species of mushrooms. is ele-
ment is accumulated in the cap of the fruiting body; and
the concentrations in the stipe of analyzed mushrooms
were under the detection limit of method.
e bioaccumulation factor
e bioaccumulation factor represents the pollutant
concentration in mushrooms comparing with the environ-
ment concentration (in soil) (Scragg, 2005). e bioac-
Tab. 2. e bioaccumulation factor of edible and non-edible wild growing species of mushrooms
Bioaccumulation
factor
Edible species Non-edible species Toxic species
Boletus griseus
Collybia
butyracea
Tapinella
atrotomentosa
Paxillus
involutus
Hypholoma
fasciculare
Tricholoma
avovirens
Zn
Cap
0.0885 0.0892 0.3258 0.0988 0.2199
0.2655
Stipe 0 0.0834 0.1101 0.0906 0.0862
0
Cu
Cap
0 1.5823 0 5.2789 2.2705
2.6297
Stipe 3.1314 4.8738 2.6001 12.4508 3.2104
4.0097
Sn
Cap 0.259 0.1663 0.1967 2.3877 0.23 0.0867
Stipe 0 0 0 0 0 0
Fig. 1. e metal concentrations in the fruiting body of some wild growing mushrooms
Elekes, C. C. et al. / Not. Bot. Hort. Agrobot. Cluj 38 (2) 2010, 147-151
150
Conclusions
e zinc and copper contents of the soil from the
wooded area of Bucegi Massif are comparable, even higher
than the maximum values of metals concentration in this
category of soil. e toxic analyzed species grew on the soil
with higher content of heavy metals than the edible spe-
cies.
e lowest content of heavy metals was founded in
edible species of mushrooms, and the highest in the toxic
species. e concentrations of these elements increased
with the increasing of the toxicity of analyzed species of
mushrooms.
e bioaccumulation factor is comparable for the ana-
lyzed species of mushrooms concerning the three heavy
metals, which means that the concentrations in mush-
rooms edible, non-edible or toxic, increase with the in-
crease of metal content in the soil.
Acknowledgments
is work was supported by CNCSIS - UEFISCSU,
project number PNII - IDEI 624/2008
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pH
Zn Cu Sn
Zn -0.9771
a
0.8602
d
0.3681
d
0.1904
a
Cu 0.257
a
-0.4581
d
-0.2703
d
0.4705
d
Sn 0.2631
a
-0.4685
d
-0.4726
d
0.1724
a
a
p < 0.001;
b
p < 0.005;
c
p < 0.01;
d
p < 0.05
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and pH with the metal concentration in the fruiting body
(Pearson’s coecient)
Mushroom
concentrations
Soil concentration
pH
Zn Cu Sn
Zn
Cap
-0.7631
a
0.8205 0.6594
d
0.1610
d
Stipe -0.3526
a
0.2011
d
-0.4471
d
0.3283
Cu
Cap
-0.0976
d
0.4445 0.1304
0.5120
Stipe -0.6113 0.6939
b
0.1457 0.5596
b
Sn
Cap -0.1614 -0.2825
d
-0.0136 0.4558
d
Stipe * * * *
a
p < 0.001;
b
p < 0.005;
c
p < 0.01;
d
p < 0.05; *the concentration in mushrooms
is under the detection limit of method
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    • "Moreover, the inability of human system to excrete them through homeostatic filtration mechanism further leads to their accumulation in the body that eventually complicates the situation. Worldwide several workers have investigated the heavy metal concentration in many wild growing mushrooms (Isildak et al. 2004, Elekes et al. 2010, Magdziak et al. 2013, Mazurkiewicz & Podlasinska, 2014, Dulay et al. 2015). However, from India, few scanty studies have been carried out on heavy metal accumulation by wild macrofungi (Das, 2005, Mallikarjuna et al. 2013) and as far as our literature survey could ascertain no work has been done on heavy metal estimation from the state so far. "
    [Show abstract] [Hide abstract] ABSTRACT: The fruiting bodies of wild mushrooms show high concentrations of heavy metals due to their efficacious mechanism of accumulation of these elements from soil. In accordance with this ability, three wild macrofungi viz., Macrolepiota procera (edible species), Amanita augusta (non-edible species), Boletus subvelutipes (poisonous species) and their respective soil samples collected from different forest areas of Jammu Province were analysed for the presence of six heavy metals (Zn, Cu, Mn, Fe, Cd, Pb). The metallic content was established by Atomic absorption spectrophotometer (AAS) and Inductively coupled Plasma–Atomic Emission spectrometry method (ICP AES). The results of heavy metals concentration are given in mg of metal per kg of dry matter and demonstrate important variation between the level of concentration in edible, non edible and toxic species. Moreover, the mean element distribution varied depending upon the part of fruiting body of macrofungi. In A. augusta these elements were detected under permissible limits for consumption. On the contrary, high ratio of zinc, copper, manganese, iron, lead and cadmium were found in A. augusta and B. subvelutipes indicating that these elements are accumulated at much higher levels in these wild growing mushrooms. Thus, it is worthwhile to evaluate the metal content in the wild macrofungi to assess their contribution to the daily intake of several toxic elements so that it would adjudicate the mushrooms for its nutritive value in terms of minerals and also define the limits of safety. As mushrooms have been known to possess good nutraceutical and pharmaceutical potential, a detailed analysis of their sporocarps is desirable before their incorporation into routine diet, drugs and medicine.
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    Article · Oct 2015
    • "The concentration of zinc is about 2-fold higher in fungal mycelium and about 3-fold higher in sporocarps than in bulk soil (Vinichuk, 2012b). Alonso et al. (2003) and Elekes et al. (2010) also find a similar concentration of 62 "
    [Show abstract] [Hide abstract] ABSTRACT: Introduction This study focuses on the distribution of radiocesium (137Cs) and selected metals in soil fractions and soil fungi of boreal forest ecosystems. The accumulation of selected metals in soil fractions: bulk soil, rhizosphere, soil-root interface and fungal mycelium and sporocarps of mycorrhizal fungi were compared in a Swedish forest. Special attention is given to radiocesium released into the environment as a result of nuclear weapons testing and the Chernobyl accident in 1986, and alkali metals, potassium (K), rubidium (Rb), and cesium (133Cs), whose chemical behavior can be expected to be similar to 137Cs. The behavior of 137Cs in forest ecosystems differs from other ecosystems due to the abundance of fungal mycelia in soil, which contribute to the persistence of the Chernobyl radiocesium in the upper horizons of forest soils, as the fungi enhance uptake of these elements into host plants. Even many years after fallout, people in Sweden consume wild fungi and game obtained from these contaminated forests. Substantial research has been conducted in Sweden after the fallout from nuclear weapons testing and the Chernobyl accident and some results presented in this book are published in a series of several articles and book chapters in collaboration with Profs K. J. Johanson, H. Rydin, and Dr. A. Taylor (Vinichuk et al. 2004; 2010a; 2010b; 2011a; 2011b). Fungi are effective in accumulating a wide range of metals, as well as radioactive isotope 137Cs. Many trace elements, including some micronutrients, such as mercury (Hg), lead (Pb), cadmium (Cd), copper (Cu), nickel (Ni), and cobalt (Co) are generally considered the most toxic, and numerous studies indicate accumulation of metals by fungal sporocarps (Mietelski et al. 2002; Campos et al. 2012). However, the contribution of wild growing mycelia and soil fractions, such as the rhizosphere and soil-root interface, with metal accumulation and distribution within forest soil is not well studied. Therefore, we attempted to quantify the Introduction VI uptake and distribution of selected metals in the soil-mycelium-sporocarps compartments in various transfer steps: bulk soil, rhizosphere, soil-root interface, fungal mycelium, and sporocarps. The relationships between the concentrations of metals studied in bulk soil, soil mycelia, and fungal sporocarps were estimated. The 137Cs activity concentration and mass concentration of alkali metals K, Rb, and 133Cs were also analyzed within individual Sphagnum plants (down to 20 cm depth) in boreal ombrotrophic bogs in the northern hemisphere. The distribution of Cs (133Cs and 137Cs), K, and Rb in the uppermost capitulum and subapical segments of Sphagnum mosses were compared to determine the possible mechanisms involved in radiocesium uptake and retention within Sphagnum plants. This book attempts to summarize the knowledge acquired from studies within Sweden and to place them in a larger context, and to update data on metals concentrations in fungal compartments of forest soil, especially in wild growing mycelium. The discussion of the summarized results addresses the issues of radiocesium (137Cs) activity concentrations, K, Rb, and stable 133Cs concentrations in soil fractions, fungal compartments and Sphagnum plants (Chapter 2); alkali Earth metals calcium (Ca) and strontium (Sr) (Chapter 3); transition metals chromium (Cr), cobalt (Co), nickel (Ni), copper (Cu), zinc (Zn), cadmium (Cd), Mercury (Hg), and lead (Pb) (Chapter 4); semimetals arsenic (As) (Chapter 5); and, actinides thorium (Th) and uranium (U) (Chapter 6).
    Full-text · Book · May 2015
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