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DOI: 10.19675/j.cnki.1006-687x.2019.04021

Uddin M, Zhang D, Proshad R, Haque MK. Role of mushrooms in soil mycoremediation: a review [J]. Chin J Appl Environ Biol, 2020, 26 (2): 460-468

Role of mushrooms in soil mycoremediation:

a review
Minhaz Uddin2, Dan Zhang1, Ram Proshad1 & M. K. Haque3
1
Institute of Mountain Hazards and Environment, Chinese Academy of Sciences & Ministry of Water Conservancy, Chengdu 610041, China
2
School of Environmental Science and Engineering, Tianjin University, Tianjin 300072, China
3
Department of Crop Science and Technology, University of Rajshahi, Rajshahi-6025, Bangladesh

Abstract Bioremediation is an innovative and promising technology available for the removal and recovery of
heavy metals from contaminated media. Bioremediation uses organisms to absorb heavy metals at low cost
and with no secondary pollution. Bioremediation by macrofungi that degrade pollutants or wastes is referred
to as mycoremediation. Macrofungi, like mushrooms, can produce enzymes and have the ability to degrade
and accumulate a wide range of toxic metals. In this paper, the research status and advances in the field of
mycoremediation using different mushroom species are reviewed. Generally mushrooms use three effective
strategies to recover contaminated or polluted soils: biodegradation, bioconversion, and biosorption. Mushrooms
can degrade and recycle wastes and pollutants to their mineral constituents and convert wastes, sludge, and
pollutants into useful forms. In addition, they can uptake heavy metals from substrates via biosorption, which is
a very effective method to reclaim polluted lands. Different wild and cultivated mushroom species are used in
mycoremediation, which can degrade large quantities of organic and inorganic pollutants and produce vendible
products. Mycoremediation is still in its infancy, but it has notable remediation potential for pollutants or metals
in soil. Mushroom species that can biodegrade, bioconvert, or absorb pollutants and metals effectively should
be given the highest preference. Further research is needed to verify that this method is an easy, cost effective,
and eco-friendly tool.
Keywords bioremediation; mycoremediation; heavy metal; mushroom

1 Introduction and accumulate a considerable amount of heavy metals

Mushrooms are available as both wild growing and
cultivated species. These macrofungi have been considered
a special food since the earliest times in many countries.
Mushrooms can grow everywhere on biological, agricultural,
and industrial wastes or can be grown in toxic metal-
polluted lands. Mushrooms are considered to be a source
of proteins and bio-active molecules with helpful therapeutic
applications while being useful in preventing diseases, such
as hypertension, hypercholesterolemia [1], and cancer [2].
Mushrooms are very rich in nutritional components, some of
which have been compared with animal proteins like those
from eggs, milk, and meat [3]. Mushrooms produce single
cell proteins, which are easily digestible and more or less
free of cholesterol.
Mushrooms are not only an important dietary product,
they are also used as a low-cost, effective mycoremediation
tool because of their role in the biodegradation, biosorption,
and bioconversion of contaminants [4-6]. Mushrooms uptake
when they grow on toxic metal-polluted substrates or soil.
In addition, mushrooms can accumulate heavy metals from
toxic metal-contaminated surfaces [7]. Akin et al. [8] measured
the concentrations of Cd, Cr, Cu, Pb, and Zn in Lactarius
deliciosus, Russula delica, and Rhizopogon roseolus and
obtained mean values of 0.72, 0.26, 28.34, 1.53, and 64
mg/kg, respectively. Furthermore, maximum Cd, Cu, Pb,
and Zn concentrations were found in R. delica, while the
Cr level was greatest in L. deliciosus. A pot experiment
tested the influence of bacterial inoculation on the growth
of Coprinus comatus, the content of Ni in C. comatus, Ni
speciation in soil, fluoranthene dissipation, soil enzymatic
activity, bacterial populations, and community structure.
With an inoculation of bacteria, the fresh weight of C.
comatus, concentration of Ni in C. comatus, and dissipation
rates of fluoranthene increased by 17.73%-29.38%, 68.97%-
204.97%, and 34.84%-60.90%, respectively [9].
Zhang Dan et al. [10] studied wild growing mushroom
species to investigate the bioaccumulation of heavy metals.

Received: 2019-04-09 Accepted: 2019-06-28

Supported by the National Natural Science Foundation of China (41571315)
Corresponding author (E-mail: daniezhang@imde.ac.cn)
Role of mushrooms in soil mycoremediation: a review
They found that Cu, Pb, Cd, and As content in Termitomyces
microcarpus were 135.00, 13.28, 65.30, and 1.60 mg/kg,
respectively. Agaricus bisporus showed a higher affinity to
absorb Cr, Cu, Cd, and Zn. In addition, maximum Zn content
was found in Pulveroboletus amarellus and was 142.00 mg/
kg in the fruiting body. Several studies for reducing metal
concentrations with mushrooms have also been conducted.
According to Xu et al., a pot experiment was performed to
investigate the combined effects of 2,4,5-trichlorophenol
(TCP) and metals on the growth of Clitocybe maxima, and
an accumulation of heavy metals as well as the dissipation
of TCP were observed [11]. The results showed a negative
effect of contamination on the fruiting time and biomass of
C. maxima. TCP decreased significantly in soils, accounting
for 70.66%-96.24% and 66.47%-91.42% of the initial
extractable concentration in planted soil and unplanted soil,
respectively, which showed that the dissipation of TCP was
enhanced by mushroom planting [11].
Zhao et al. developed an effective bottom-up metal
removal system, which was based on the synergy between
the immobilization of metal-resistant bacteria and the
extraction of the bio-accumulator Stropharia rugoso-
annulata [12] . The results demonstrated that the system
significantly increased the proportion of acid soluble Cd
and Cu and improved the soil micro-ecology (i.e., microbial
counts, soil respiration, and enzyme activity). The maximum
extraction of Cd and Cu was 8.79 mg/kg and 77.92 mg/kg,
respectively. In addition, details of the possible mechanisms
of metal removal were discussed, and it was found to be
positively correlated with acetic acid (HoAc) extractable
metals and soil micro-ecology. Meanwhile, the dilution
effect in S. rugoso-annulata probably played an important
role in the metal removal process [12].
Mushroom mycelia spread over the surfaces where
they grow and extract metal ions under suitable conditions.
The mycelia extract metals from polluted soil, which leads to
a type of mycoremediation known as mycofiltration. Mycelia
act like plant roots and extract toxic metals. According to
Srivastava et al. [13] and Sesli et al. [2], heavy metal uptake
by mushrooms is affected by some environmental factors
and the physiology of the mushroom species, such as the
pH, metal ion concentration, nature of the fruiting body, age
of the mycelia, and the enzymes and proteins present in
mushrooms.
Fig. 1 Primary stages of the degradation process of polycyclic aromatic hydrocarbons (PAHs) by fungi (image modified from Field et al. [27])
Vol. 26 No. 2 Apr 2020 461
The inf luenc e of chelators and sur factants on
the bioaccumulation of heavy metals in the mushroom
Tricholoma lobayense Heim from multiple contaminated
soils was studied. The results showed that a high
concentration of EDTA (5 mmol/kg) reduced mushroom
biomass by 26%, while the concentrations of Pb, Cu, and
Cd in the fruiting bodies increased by 15-88-, 0.8-3.3-, and
0.5-0.6-fold, respectively, when only EDTA was added [14].
2 Remediation through mushrooms
Mushrooms use three effective methods to reclaim and
ameliorate polluted lands: biodegradation, bioconversion,
and biosorption.
2.1 Biodegradation
Mushrooms have the ability to accumulate heavy
metals with their rich network of hyphae. Each mushroom
has a specific capacity and genetically induced ability
to absorb heavy metals from the soil [15]. Mushrooms are
utilized in mycoremediation because of particular features
associated with the potential uptake of heavy metals [16].
Hammel et al. [17] reported that mushrooms have the ability
to degrade polycyclic aromatic hydrocarbons (PAHs).
The degradation and subsequent recycling of wastes or
pollutants by living organisms to their mineral constituents
is called biodegradation, while mineralization converts
compounds to simple and inorganic forms. A large number
of studies have investigated the degradation ability of
various mushrooms and their enzymes. Nyanhongo
et al. [18] reported that mushrooms can produce extracellular
peroxidases, ligninases, cellulases, pectinases, xylanases,
and oxidases. Furthermore, mushrooms can degrade
PAHs [19] , plastic [20] , organic and synthetic dyes [21-22] ,
2,4-dichlorophenol [23], crude oil [24], malachite green [25], and
radioactive cellulosic-based waste [26].
2.2 Bioconversion
Research on the conversion of wastes, sludge, and
pollutants into useful forms is ongoing in many countries.
The bioconversion process is based on utilizing sugar from
cellulose and hemicellulose to form macrofungi metabolites
that are essential for the growth and survival of macrofungi.
Wild mushrooms are a potential source of secondary
metabolites and enzymes. Secondary metabolites help
mushrooms compete and adapt to untoward conditions,
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462 26卷 第2期 2020年4月
and these metabolites are also used for the production
of antibiotics, antifungals, nematicides, and vitamins.
Macrofungi use enzymes to biodegrade and biotransform the
lignin of wood to access cellulose and hemicellulose chains.
The enzymes degrade lignocellulosic material into sugar
monomers for the production of ethanol by a fermentation
process using yeast, which is of industrial interest [28].
Lignocellulosic waste can be used for mushroom
cultivation and a bioconversion product can be produced
(i.e., a mushroom). Mushroom cultivation in industrial wastes
provides protein rich mushroom fruiting bodies and also
helps to solve pollution problems. According to Kulshreshtha
et al. [29], Pleurotus citrinopileatus successfully grows on
industrial waste from handmade paper and produces high
quality protein rich fruiting bodies. Jonathan et al. [30] worked
with Pleurotus tuber-regium, which grows on trees and
produces vendible products. Lentinula edodes is another
mushroom species that is able to successfully convert
eucalyptus waste to useable products [31]. Two mushroom
species, Pleurotus eous and Lentinus conatus, were
cultivated by Rani et al. [32] on rice straw and banana waste,
and they reported that the rice and banana waste could be
bioconverted to usable products. Lechner and Papinutti [33]
found that lentinus tigrinus can bioconvert wheat straw. In
addition, Volvariella volvacea results in a good production of
fruiting bodies when it grows on banana leaves [34]. Gaitán-
Hernández et al. [35] cultivated Lentinula edodes and found
that this species has the ability to bioconvert barley and
wheat straw to maximum yield within 6 days.
Kozarski et al. [36] reported that wild or domestically
cultivated macrofungi have the ability to bio-transform
vegetal biomass into valuable commercial substances,
namely enzymes (e.g., hydrolases and oxidative enzymes),
carbohydrates (e.g., β-glucans), proteins (e.g., lectins), and
secondary metabolites (e.g., lovastatin). Potential products
from macrofungi are also very useful for human activities.
For example, enzymes are required in the food, textile,
Fig. 2 Bioconversion pathway to produce by-products with wild mushrooms (image modified from Conceição et al. [28]). (1) Wood is
decayed by wild mushrooms, which are natural decomposers. (2) Wild mushrooms bioconvert the nutrients of dead wood into important bioactive
molecules. (3) Mushrooms use enzymatic weapons to bioconvert materials. (4) This special arsenal biotransforms plant cell wall components.
(5) Cell wall components are biotransformed into oligomers and monomers. (6) Oligomers and monomers undergo a fermentation process. (7)
Ethanol and organic acids are produced.
Minhaz Uddin et al.
paper, and pharmaceutical industries. Wild macrofungi
supply various enzymes, such as laccase produced by
Lactarius sp. [37] , Lentinula boryana, and Pycnoporus
sp. [38]. In addition, metaloendo-peptidases from Tricholoma
saponaceum are able to hydrolyze fibrinogen and fibrin [39].
Trametes versicolor, Irpex lacteus, and Phlebiopsis
sp. were found to be useful for lignin degradation with the
help of their oxidative activities. This particular ability of
these wild strains may be useful for the paper industry [40].
Carbohydrates like β-glucans are used in medicine. Some
wild mushrooms, such as Cortinarius violaceus (L. ex Fr.)
Gray, Laccaria amethystina (Cooke), Trametes versicolor,
and Piptoporus betulinus, produce glucans [41]. Some studies
have reported valuable by-products from wild macrofungi,
and these are listed in Table 1.
2.3 Biosorption
The removal of metals or contaminants by mushrooms
from an aqueous solution is called biosorption.
Gavrilescu [38] reported that biosorption is based on the
sorption of metallic ions from effluents by mushrooms with
a significant tolerance for metals. Mar’in et al. [48] reported
that dead mushroom biomass offers certain advantages
over living cell biomass with regard to the biosorption
process. Kapoor and Viraraghavan [49] found that the
uptake of heavy metals depends on the physico-chemical
interactions of metallic ions with the cellular compounds of
biological species. Biosorption is a very popular method
due to its maximum uptake capacity and low cost. Many
mushroom species remove pollutants or heavy metals using
biosorption. For example, P. tuber-regium biosorbs heavy
metals from heavy metal-contaminated soil [50]. In addition,
Fomes fasciatus efficiently biosorps Cu (II) ions, and hot-
alkali treatment was found to increase its affinity for Cu (II)
ions [51]. Furthermore, Pleurotus platypus, A. bisporus, and
Calocybe indica are efficient biosorbents for the removal of
Cu, Zn, Fe, Cd, Pb, and Ni from aqueous solutions [6], while
Pleurotus ostreatus possesses the biosorption ability to
Role of mushrooms in soil mycoremediation: a review Vol. 26 No. 2 Apr 2020 463

Table 1 Bioconversion of vegetal biomass by-products

Wild macrofungi Figure Remark Reference

This species bioconverts hardwood kraft pulp to

Phlebia sp. [42]
ethanol

Cerrena unicolor converts synthetic medium to

Cerrena unicolor [43]
antioxidant and antimicrobial molecules

Produce tannin, saponin,

Rigidoporus microporus [44]
alkaloid, steroid, cardiac glycoside

Produce laccase
Lactarius sp. [45]

Cow dungmanure + sisal waste is bioconverted by this

Coprinus cinereus [46]
species to laccase, lignin peroxidase, and xylanase

Laccase, lignin peroxidase, and manganese peroxidase

Trametes versicolor is found from kraft pulp + potato dextrose broth after [40]
bioconversion by this species

Pycnoporus Sabouraud dextrose agar is converted to antimicrobial

[47]
cinnabarinus metabolite by this species

remove cadmium [52], and Pleurotus sajor-caju can biosorb
Zn from contaminated sites [53].
Mushrooms or macro fungi can uptake pollutants
or heavy metals via bioaccumulation and biosorption
processes. Compared to that of plants and vegetables,
the fruiting bodies of mushrooms can bioaccumulate
large concentrations of heavy metals, as reported by
Gast et al. [54]. Mushrooms use mycelium to uptake heavy
metals from substrates. The metal content in fruiting
bodies is considerably affected by many factors, such as
mycelium age, substrate composition, and the life span of
fructification. Thomet et al. [55] observed maximum metal
concentrations in the sporophores but not the spores,
intermediate metal content in the cap, and the lowest
metal content in the stipe. According to Kalac et al. [56],
wild grown A. bisporus usually uptake more metals than
cultivated Agaricus species. They also added that excess
metallic content can be found in mushrooms from ore
mining-contaminated sites. The uptake of Cd by Volvariella
volvacea and P. sajor-caju can be reduced due to the
interaction of Cu and Cd at lower concentrations, but it
can increase Cu uptake [57]. However, much is yet to be
elucidated of the transport process of metals from mycelium
to the fruiting bodies. Previous studies have reported that
certain mushrooms have the potential to be biosorbents of
metals, and these are presented in Table 2 along with their
respective metal concentrations.
464 26卷 第2期 2020年4月 Minhaz Uddin et al.

3 Barriers to mycoremediation
The mycoremediation of polluted lands by mushrooms
is an eco-friendly remediation approach and requires
low costs, small areas, and minimally trained personnel.
When mycoremediation is carried out in a given site, there
is no need to transport the heavy metals to treatment
sites, which reduces the transport cost. However, some
problems associated with carrying out mycoremediation
are present. Mushrooms need time to remove toxic metals
and pollutants from ecosystems and need a considerable
amount of time to acclimate. In addition, the toxicity level in
the mushrooms themselves is a concern. Toxicity levels in
mushrooms increase due to biosorption and biodegradation
when they grow on wastes or polluted substrates. Toxicity
reduction depends on the ability of mushrooms to degrade
wastes or pollutants [71]
with their different enzymes. Many

Table 2 Heavy metal uptake capacity of different mushroom species from previous studies
Mushroom species Figure Edibility Heavy metal con. in fruiting bodies (mg/kg dry weight) Reference
[58]
Cu 107, Cd 1.7, Pb 2.1, Zn 57.2, Mn 25.9, Fe 290, Cr 6.5, Ni 7.9
[59]
Pb 0.46, Cd 0.70, Hg 0.04, Fe 15.8, Cu 6.61, Mn 2.27, Zn 9.32
Agaricus bisporus Edible
[60]
Pb 2.41, Cd 3.48, Hg 0.60, Cu 5.22,Mn 22.3, Zn 17.8, Fe 126
[56]
Cd 3.5

Pb 1.6, Cd 11.0, Hg 0.3, Cu 31.0 [61]

Choice with
Armillaria mellea
caution
Pb 1.28, Cd 2.48, Hg 0.91, Cu 21.1, Mn 26.8, Zn 76.8 [62]

Pb 0.96, Cd 1.03, Hg 0.13, Fe 31.1 [59]

Boletus edulis Edible
Cu 4.7, Mn 2.9, Zn 26.2 [63]

Calvatia
Edible Fe 924, Cu 25, Mn 28, Zn 58, Pb 1.5, Cd 1.1 [8]
excipuliformis

Edible
Lepiota rhacodes Hg 8, Pb 66, Cd 3.7 [63]

Paxillus involutus Inedible Pb 1.6.0, Cu 57.0 [56, 61]

Pleurotus sajor-caju Edible Pb 7.0 , Cd 33.0 µg/g [45]

Pb 0.11, Cd 0.55, Hg 0.31, Fe 48.6, Cu 5.0, Mn 10.3, Zn 19.3； [59]

Pleurotus ostreatus Edible
Pb 3.24, Cd 1.18, Hg 0.42, Fe 86.17，Cu 13.6, Mn 6.2, Zn 29.8 [62]
Role of mushrooms in soil mycoremediation: a review Vol. 26 No. 2 Apr 2020 465

Table 2 (Continued)

Mushroom species Figure Edibility Heavy metal con. in fruiting bodies (mg/kg dry weight) Reference

Psalliota campestris Edible Pb 1.85, Cd 5.55 [64]

Pb 4.8, Cd 2.0, Hg 0.21, Fe 54.5, Cu 10.8, Mn 12.1, Zn 19.3 [59]

Russula delica Edible Cu 73.0, Zn 57.0, Mn 9.6, Fe 244, Co 1.5, Cd 0.31, Ni 3.2, Pb 2.7 [65]

Pb 3.1, Cd 1.1, Hg 0.26, Cu 13.6,Mn 6.6, Zn 32.6, Fe 74.8 [60]

Pb 19.08 ± 2.84, Cu 17.57 ± 0.69, Cd 0.55 ± 0.06 [66]

Coprinus comatus Edible -6
Cu 16.78 × 10 [67]
Cd 10.83×10 -6

Cr 21.5 [68]
Lentinus edodes Edible
Cd 3 mmol/L [69]
Fe 3 mmol/L

Fe 4520.70-3179.15
Zn 98.43-45.92
Cu 95.43-21.70
Mn 37.31-11.46
Pleurotus eryngii Edible [70]
Ni 28.80-10.90
Pb 25.95-17.38
Cr 18.35-4.25
Co 5.02-1.39

studies have reported that mushrooms growing on polluted
substrates contain high quantities of metals in their fruiting
bodies. Due to the low to intermediate concentrations of
heavy metals in substrates, mushroom mycelial growth may
be stunted, and higher heavy metal concentrations may
inhibit growth. However, some heavy metals are not harmful
and can act as growth stimulators (e.g., Zn and Fe). Jain et
al. [72] reported that high concentrations of all heavy metals
reduced sporocarp production in P. sajor-caju. Purkayastha
and Mitra [73] found that Co and Pb caused the highest
reduction in the fructification of V. volvacea and P. sajor-
caju. In addition, mycelial protein content was reduced in A.
bisporus and P. ostreatus due to the uptake of Hg, Cd, Pb,
and Zn [74].
4 Conclusion
From the current review, a great deal of evidence
indicates that mushrooms have effective mechanisms of
heavy metal uptake and can degrade different types of
wastes, which is very promising for future mycoremediation
technologies. Major metal-accumulating, waste-detoxifying,
and pollutant-degrading species have been the focus of
mycoremediation research around the globe. However,
mycoremediation is still an emerging technology. In my
personal view, scientists should first try to cultivate high
metal-absorbing mushroom species before low-absorbing
mushroom species in waste-containing or polluted sites
so that the uptake of the pollutants or metals can be
minimized. The toxicity and metal content in mushrooms
should be critically assessed so that non-toxic mushrooms
may be consumed and health risks avoided. However, in
mycoremediation, preference should be given to those
species that can biodegrade, bioconver t, or absorb
pollutants ef fectively. Fur ther research is needed to
support the widespread use of mushrooms as potential
mycoremediation tools.
Acknowledgement
The authors would like to thank Dr. Md. Saiful Islam,
Depar tment of Soil Science, Patuakhali Science and
Technology University, Bangladesh, for his support and
suggestions for this review paper.
466 26卷 第2期 2020年4月
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