http://www.cibj.com/ DOI: 10.19675/j.cnki.1006-687x.2019.04021

Uddin M, Zhang D, Proshad R, Haque MK. Role of mushrooms in soil : 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 is an innovative and promising technology available for the removal and recovery of 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: , 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 when they grow on toxic metal-polluted substrates or soil. Mushrooms are available as both wild growing and In addition, mushrooms can accumulate heavy metals from cultivated species. These macrofungi have been considered toxic metal-contaminated surfaces [7]. Akin et al. [8] measured a special food since the earliest times in many countries. the concentrations of Cd, Cr, Cu, Pb, and Zn in Lactarius Mushrooms can grow everywhere on biological, agricultural, deliciosus, Russula delica, and Rhizopogon roseolus and and industrial wastes or can be grown in toxic metal- obtained mean values of 0.72, 0.26, 28.34, 1.53, and 64 polluted lands. Mushrooms are considered to be a source mg/kg, respectively. Furthermore, maximum Cd, Cu, Pb, of proteins and bio-active molecules with helpful therapeutic and Zn concentrations were found in R. delica, while the applications while being useful in preventing diseases, such Cr level was greatest in L. deliciosus. A pot experiment [1] [2] as hypertension, hypercholesterolemia , and cancer . tested the influence of bacterial inoculation on the growth Mushrooms are very rich in nutritional components, some of of Coprinus comatus, the content of Ni in C. comatus, Ni which have been compared with animal proteins like those speciation in soil, fluoranthene dissipation, soil enzymatic from eggs, milk, and meat [3]. Mushrooms produce single activity, bacterial populations, and community structure. cell proteins, which are easily digestible and more or less With an inoculation of bacteria, the fresh weight of C. free of cholesterol. comatus, concentration of Ni in C. comatus, and dissipation Mushrooms are not only an important dietary product, rates of fluoranthene increased by 17.73%-29.38%, 68.97%- they are also used as a low-cost, effective mycoremediation 204.97%, and 34.84%-60.90%, respectively [9]. tool because of their role in the biodegradation, biosorption, Zhang Dan et al. [10] studied wild growing mushroom and bioconversion of contaminants [4-6]. Mushrooms uptake 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: [email protected]) Role of mushrooms in soil mycoremediation: a review Vol. 26 No. 2 Apr 2020 461

They found that Cu, Pb, Cd, and As content in Termitomyces The influence of chelators and surfactants on microcarpus were 135.00, 13.28, 65.30, and 1.60 mg/kg, the bioaccumulation of heavy metals in the mushroom respectively. Agaricus bisporus showed a higher affinity to Tricholoma lobayense Heim from multiple contaminated absorb Cr, Cu, Cd, and Zn. In addition, maximum Zn content soils was studied. The results showed that a high was found in Pulveroboletus amarellus and was 142.00 mg/ concentration of EDTA (5 mmol/kg) reduced mushroom kg in the fruiting body. Several studies for reducing metal biomass by 26%, while the concentrations of Pb, Cu, and concentrations with mushrooms have also been conducted. Cd in the fruiting bodies increased by 15-88-, 0.8-3.3-, and According to Xu et al., a pot experiment was performed to 0.5-0.6-fold, respectively, when only EDTA was added [14]. investigate the combined effects of 2,4,5-trichlorophenol (TCP) and metals on the growth of Clitocybe maxima, and 2 Remediation through mushrooms an accumulation of heavy metals as well as the dissipation of TCP were observed [11]. The results showed a negative Mushrooms use three effective methods to reclaim and effect of contamination on the fruiting time and biomass of ameliorate polluted lands: biodegradation, bioconversion, C. maxima. TCP decreased significantly in soils, accounting and biosorption. for 70.66%-96.24% and 66.47%-91.42% of the initial 2.1 Biodegradation extractable concentration in planted soil and unplanted soil, Mushrooms have the ability to accumulate heavy respectively, which showed that the dissipation of TCP was metals with their rich network of hyphae. Each mushroom [11] enhanced by mushroom planting . has a specific capacity and genetically induced ability [15] Zhao et al. developed an effective bottom-up metal to absorb heavy metals from the soil . Mushrooms are removal system, which was based on the synergy between utilized in mycoremediation because of particular features [16] the immobilization of metal-resistant bacteria and the associated with the potential uptake of heavy metals . [17] extraction of the bio-accumulator Stropharia rugoso- Hammel et al. reported that mushrooms have the ability annulata [12]. The results demonstrated that the system to degrade polycyclic aromatic (PAHs). significantly increased the proportion of acid soluble Cd The degradation and subsequent recycling of wastes or and Cu and improved the soil micro-ecology (i.e., microbial pollutants by living organisms to their mineral constituents counts, soil respiration, and enzyme activity). The maximum is called biodegradation, while mineralization converts extraction of Cd and Cu was 8.79 mg/kg and 77.92 mg/kg, compounds to simple and inorganic forms. A large number respectively. In addition, details of the possible mechanisms of studies have investigated the degradation ability of of metal removal were discussed, and it was found to be various mushrooms and their enzymes. Nyanhongo [18] positively correlated with acetic acid (HoAc) extractable et al. reported that mushrooms can produce extracellular metals and soil micro-ecology. Meanwhile, the dilution peroxidases, ligninases, cellulases, pectinases, xylanases, effect in S. rugoso-annulata probably played an important and oxidases. Furthermore, mushrooms can degrade [19] [20] [21-22] role in the metal removal process [12]. PAHs , plastic , organic and synthetic , Mushroom mycelia spread over the surfaces where 2,4-dichlorophenol [23], crude oil [24], malachite green [25], and they grow and extract metal ions under suitable conditions. radioactive cellulosic-based waste [26]. The mycelia extract metals from polluted soil, which to 2.2 Bioconversion a type of mycoremediation known as mycofiltration. Mycelia Research on the conversion of wastes, sludge, and act like plant roots and extract toxic metals. According to pollutants into useful forms is ongoing in many countries. Srivastava et al. [13] and Sesli et al. [2], heavy metal uptake The bioconversion process is based on utilizing sugar from by mushrooms is affected by some environmental factors and hemicellulose to form macrofungi metabolites and the physiology of the mushroom species, such as the that are essential for the growth and survival of macrofungi. pH, metal ion concentration, nature of the fruiting body, age Wild mushrooms are a potential source of secondary of the mycelia, and the enzymes and proteins present in metabolites and enzymes. Secondary metabolites help mushrooms. mushrooms compete and adapt to untoward conditions,

O O O O O

Fig. 1 Primary stages of the degradation process of polycyclic aromatic hydrocarbons (PAHs) by fungi (image modified from Field et al. [27]) 462 26卷 第2期 2020年4月 Minhaz Uddin et al. and these metabolites are also used for the production paper, and pharmaceutical industries. Wild macrofungi of antibiotics, antifungals, nematicides, and vitamins. supply various enzymes, such as produced by Macrofungi use enzymes to biodegrade and biotransform the Lactarius sp. [37], Lentinula boryana, and Pycnoporus of wood to access cellulose and hemicellulose chains. sp. [38]. In addition, metaloendo-peptidases from Tricholoma The enzymes degrade lignocellulosic material into sugar saponaceum are able to hydrolyze fibrinogen and fibrin [39]. monomers for the production of ethanol by a fermentation Trametes versicolor, Irpex lacteus, and Phlebiopsis process using yeast, which is of industrial interest [28]. sp. were found to be useful for lignin degradation with the Lignocellulosic waste can be used for mushroom help of their oxidative activities. This particular ability of cultivation and a bioconversion product can be produced these wild strains may be useful for the paper industry [40]. (i.e., a mushroom). Mushroom cultivation in industrial wastes Carbohydrates like β-glucans are used in medicine. Some provides protein rich mushroom fruiting bodies and also wild mushrooms, such as Cortinarius violaceus (L. ex Fr.) helps to solve pollution problems. According to Kulshreshtha Gray, Laccaria amethystina (Cooke), Trametes versicolor, et al. [29], citrinopileatus successfully grows on and Piptoporus betulinus, produce glucans [41]. Some studies industrial waste from handmade paper and produces high have reported valuable by-products from wild macrofungi, quality protein rich fruiting bodies. Jonathan et al. [30] worked and these are listed in Table 1. with Pleurotus tuber-regium, which grows on trees and 2.3 Biosorption produces vendible products. Lentinula edodes is another The removal of metals or contaminants by mushrooms mushroom species that is able to successfully convert from an aqueous solution is called biosorption. eucalyptus waste to useable products [31]. Two mushroom Gavrilescu [38] reported that biosorption is based on the species, Pleurotus eous and Lentinus conatus, were sorption of metallic ions from effluents by mushrooms with cultivated by Rani et al. [32] on rice straw and banana waste, a significant tolerance for metals. Mar’in et al. [48] reported and they reported that the rice and banana waste could be that dead mushroom biomass offers certain advantages bioconverted to usable products. Lechner and Papinutti [33] over living cell biomass with regard to the biosorption found that lentinus tigrinus can bioconvert wheat straw. In process. Kapoor and Viraraghavan [49] found that the addition, Volvariella volvacea results in a good production of uptake of heavy metals depends on the physico-chemical fruiting bodies when it grows on banana leaves [34]. Gaitán- interactions of metallic ions with the cellular compounds of Hernández et al. [35] cultivated Lentinula edodes and found biological species. Biosorption is a very popular method that this species has the ability to bioconvert barley and due to its maximum uptake capacity and low cost. Many wheat straw to maximum yield within 6 days. mushroom species remove pollutants or heavy metals using Kozarski et al. [36] reported that wild or domestically biosorption. For example, P. tuber-regium biosorbs heavy cultivated macrofungi have the ability to bio-transform metals from heavy metal-contaminated soil [50]. In addition, vegetal biomass into valuable commercial substances, Fomes fasciatus efficiently biosorps Cu (II) ions, and hot- namely enzymes (e.g., hydrolases and oxidative enzymes), alkali treatment was found to increase its affinity for Cu (II) carbohydrates (e.g., β-glucans), proteins (e.g., lectins), and ions [51]. Furthermore, Pleurotus platypus, A. bisporus, and secondary metabolites (e.g., lovastatin). Potential products Calocybe indica are efficient biosorbents for the removal of from macrofungi are also very useful for human activities. Cu, Zn, Fe, Cd, Pb, and Ni from aqueous solutions [6], while For example, enzymes are required in the food, , possesses the biosorption ability to

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

3 Barriers to mycoremediation are present. Mushrooms need time to remove toxic metals and pollutants from and need a considerable The mycoremediation of polluted lands by mushrooms amount of time to acclimate. In addition, the toxicity level in is an eco-friendly remediation approach and requires the mushrooms themselves is a concern. Toxicity levels in low costs, small areas, and minimally trained personnel. mushrooms increase due to biosorption and biodegradation When mycoremediation is carried out in a given site, there is no need to transport the heavy metals to treatment when they grow on wastes or polluted substrates. Toxicity sites, which reduces the transport cost. However, some reduction depends on the ability of mushrooms to degrade problems associated with carrying out mycoremediation 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 and pollutant-degrading species have been the focus of substrates contain high quantities of metals in their fruiting mycoremediation research around the globe. However, bodies. Due to the low to intermediate concentrations of mycoremediation is still an emerging technology. In my heavy metals in substrates, mushroom mycelial growth may personal view, scientists should first try to cultivate high be stunted, and higher heavy metal concentrations may metal-absorbing mushroom species before low-absorbing inhibit growth. However, some heavy metals are not harmful mushroom species in waste-containing or polluted sites and can act as growth stimulators (e.g., Zn and Fe). Jain et so that the uptake of the pollutants or metals can be [72] al. reported that high concentrations of all heavy metals minimized. The toxicity and metal content in mushrooms reduced sporocarp production in P. sajor-caju. Purkayastha should be critically assessed so that non-toxic mushrooms and Mitra [73] found that Co and Pb caused the highest may be consumed and health risks avoided. However, in reduction in the fructification of V. volvacea and P. sajor- mycoremediation, preference should be given to those caju. In addition, mycelial protein content was reduced in A. species that can biodegrade, bioconvert, or absorb bisporus and P. ostreatus due to the uptake of Hg, Cd, Pb, pollutants effectively. Further research is needed to and Zn [74]. support the widespread use of mushrooms as potential 4 Conclusion mycoremediation tools.

From the current review, a great deal of evidence Acknowledgement indicates that mushrooms have effective mechanisms of The authors would like to thank Dr. Md. Saiful Islam, heavy metal uptake and can degrade different types of Department of Soil Science, Patuakhali Science and wastes, which is very promising for future mycoremediation Technology University, Bangladesh, for his support and technologies. Major metal-accumulating, waste-detoxifying, suggestions for this review paper. 466 26卷 第2期 2020年4月 Minhaz Uddin et al.

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