Mycoremedation as a Strategic Solution to the Decontamination of Heavy Metals in Soil

Summary

The anthropogenic contamination of soil is detrimental to human and environmental health. The quality and fertility of the earth’s soil are directly linked to human health through environmental pathways. This connection is evident as humans eat both the plants that grow in the soil and the animals that feed on these plants. Food chain contamination through the bioaccumulation of unwanted heavy metals threatens human well-being and highlights a critical need for remediation in affected areas. 

Traditional methods of remediation are heavily researched, and while effective, prove to be cost-inefficient and lead to unintended secondary pollution and the degradation of land. However, there is a potential for biological solutions that work with nature. Using mycoremediation by encompassing fungal bioaugmentation and bioremediation is a cost effective and natural solution.


Figure 1 Anthropogenic sources of heavy metal contamination in soil Adapted from “The effects of sunlight on plant growth,” by J. A. Smith and L. B. Doe, 2015, Journal of Botanical Research, 29(3), p. 115


The review presents research on specific fungi outlining the ability in heavy metal contaminant removal. Discussed are the resilience of fungi-related solutions in relative applications and mycelium or mycorrhizal relationships to the extraction of heavy metals. As a primary decomposer, fungi have shown to break down a wide range of complex chemicals, and sequester elements (Bhandari et al., 2021). Additionally, the role of microbial enzymes in mycoremediation for the processes of degradation, reduction, oxidation, and how these are related to the biosorption in effective removal of heavy metals is addressed.

Mycoremediation offers potential for use in various sectors including industry, waste management, agriculture and pesticides, homes and gardens, mining, and water treatment. Discussed are the applications or recommendations for each sector to highlight the versatility fungi offers in addressing environmental contamination.

Introduction


Heavy metal soil contamination, particularly in agriculture use, presents a significant global challenge. The issue directly corelates to human health through environmental pathways in farmland use and global supply chain. Industrialization, urbanization, and increasing financial pressures amplify  this problem on farm production. An agriculture official in China states: “millions of hectares [(which is larger than an acre)] of agricultural land in China could be withdrawn from production because of severe heavy-metal pollution” (Kiruba, 2014; Duggan, 2014). The causes include aerosol spread of high polluting energy sources from the rapid developments of the area, irresponsible conventional farming practices with use of pesticides and herbicides, and improper irrigation.

The bioaccumulation of heavy metals not only deteriorates the soil’s environmental quality but also diminishes its functionality. Consequently, human health and overall wellbeing are negatively impacted. Heavy metal exposure is linked to diseases such Parkinsons, Alzheimer’s, muscular dystrophy, an increased rate of cancer, and is known to negatively affect brain function, and other vital organs, according to an interdisciplinary toxicology report (Jaishankar et al., 2014).

Mycoremediation through deployment of bioremediation and bioaugmentation leverages the capabilities of fungi through scalable applications. Mycoremediation techniques assess the effectiveness of specific fungi species in the capsulation of heavy metals and their diverse adaptability (Aibeche et al., 2022; Bhandari et al., 2021; Javaid et al., 2011).

Review of literature

Heavy metal contamination in soil imposes a significant environmental challenge. The contamination is from causes that are either naturally occurring (considered biogenic) or anthropogenic. Anthropogenic sources, such as industrial activities, improper waste disposal, chemical industry, petrochemical plants, and mining make its way into the soil through atmospheric mixing and photo-chemical aging in both dry and wet deposition (Clemmensen et al., 2013; Ventura et al., 2021). Through the bioaccumulation and bioavailability of these deposits, plants can uptake these heavy metals, imposing health effects down the food chain (Hill, 2023).

Traditional methods of heavy metal removal are effective; however, they often lead to secondary pollution and the further degradation of the land and are not cost-effective solutions. In contrast, biological solutions such as mycoremediation provide a cost effective and efficient alternative (Nahid & Amin-ul, 2020). Considering these limitations, this has encouraged an exploration of fungal bioremediation or bioaugmentation as an alternative (Chahrazed, 2022).

As contrasted from traditional methods of heavy metal removal, mycoremediation offers a solution through two different processes. Bioremediation is the process of taking an existing (contaminated) area or environment and introducing beneficial nutrients tailored to the selection of microorganisms most prevalent in the bioremediation process. Bioaugmentation through fungi leverage the introduction of a certain species’ innate capabilities of biosorption, biomineralization, and bio-oxidation into an existing contaminated soil environment (Anderson, 2019). In mycoremediation, bioaugmentation offers a targeted treatment option without the use of chemicals, and if a selected species of fungi is found to not be already located in the desired soil location, as is often the case, it allows the use of the species through the careful introduction to a new environment (Kumar et al., 2023).


Figure 2 Image adapted from "Metagenomics to Bioremediation: Applications, Cutting Edge Tools, and Future Outlook," 1st ed., edited by Kumar et al., 2022 -- Illistration of Bioaugmentation


Current research in the field of fungal bioremediation suggests various single cell microorganisms’ ability to address heavy metal soil contamination such as R. Mucilaginosa RO7 and W. Anomalus WO2. These are yeasts capable of efficiently removing lead at rates of 98% or greater (Aibeche et al., 2022). Similarly, multicellular fungi, such as Pleurotus Ostreatus (oyster mushroom) have shown a remarkable ability in the uptake of copper, nickel, zinc, and chromium through mycoremediation, where fungal biomass is introduced in a contaminated environment to remove trace heavy metals or other contaminates (Li, et al., 2017).


Figure 3 Image adapted from "Metagenomics to Bioremediation: Applications, Cutting Edge Tools, and Future Outlook," 1st ed., edited by Kumar et al., 2022 -- Illistration of Bioremediation

One study from the journal article Bioremediation Potential and Lead Removal Capacity of Heavy Metal-Tolerant Yeast Isolated from Dayet Oum Ghellaz Lake Water, isolates seven strains of yeast for research, indicating their ability to sequestrate heavy metals from highly contaminated soils. The scientist tests each strain of yeast’s ability to intercellular sequestrate (the compartmentalization of metals to allow higher levels of tolerance) and to bioaccumulate for what metal tolerant strains could be candidates for further research into specifically lead bioremediation (Aibeche et al., 2022).

Arbuscular mycorrhizae (AM) extend beyond the ability of its symbiosis networking with plants, as AM fungi have shown an ability to immobilize metals, including non-essential heavy metals such as lead (Hoeksema et al., 2005; Whitfield et al., 2004). The adaptability of mycelial networks in AM fungi is critical in enhancing the efficiency of the bioremediation process (Worrich et al., 2016). This is particularly evident in AM fungi's symbiosis relationship with plants bolstering efforts of phytoremediation. The synergistic relationship between fungi and plants in current research suggests mycorrhizal symbiosis to enhance phytoremediation through improving soil quality and nutrient bioavailability, making phytoremediation efforts more effective  through the supporting growth of plants (Smith & Read, 2018).

Mycoremediation occurs  through the utilization of mycelium (the vegetative body of the fungi) and produces enzymes by the fungi to break down a wide range of contaminants or sequester heavy metals. Additionally, it has proven a versatile solution, with capabilities to degrade other contaminants such as pesticides, herbicides and polyaromatic hydrocarbons (PAHs), as suggested by David Hill at the University of Buffalo in a study conducted to examine mycoremediation in urban gardening alongside current lead-remediation policies and approaches (Hill, 2022). Fungi’s ability to degrade a broad spectrum of pollutants increasing its versatility and applicability in environmental remediation practices.

Studies highlight a specific relationship between mycelium and heavy metal extraction and breakdown. Current research on macro fungi—such as Pleurotus spp., which is both an edible and cultivated species of the basidiomycete group, have proven effective in extracellular sequestration of heavy metals through absorption, accumulation, and conversion, effectively removing them from the given environment (Mohamadhasani & Rahimi, 2022 As a primary decomposer, fungi serves a natural role and has an innate ability that can be exploited in the degradation of complex chemicals or sequestration of non-essential heavy metals. Cell walls of fungi and mycelium contain proteins and enzymes that can interact with metals (Rayma et al., 2021).

AM fungi have a strong role in heavy metal bioremediation as a barrier in the arbuscular stage in an environmental pathway. Research suggests its robust morphology and diverse metabolic capabilities can counteract the bioavailability of heavy metal toxicity in soil (Tomar et al., 2021). This ability of the mycorrhizal fungi immobilizes the metal, typically through the oxidation of the metal ion reducing Its toxicity through the deployment of biosorption (Chen et al., 2019; Li et al., 2017). The heavy metals are absorbed into the cell walls or stored in fungal tissues rather than remaining bioavailable in the soil.

Fungi are incredibly resilient in nature and adaptable to non-native levels of pH, temperature, and moisture. This resilience allows effective implementation of bioaugmentation practices in highly polluted urban settings where the application may be most appropriate to remediation. Compared to microbial remediation, or phytoremediation, the mycelial networks extensive and adaptable size allows a greater surface area for the interactions and successful uptake of pollutants (Bhandari et al., 2021). This size enhances the efficiency of the bioremediation process when compared to other methods. 

The specific biochemical and genetic versatility of fungi through metabolic pathways allows a specific use for a diverse range of pollutants or specific heavy metals. Its ability to adapt in a variety of environments is essential for implementation of bioaugmentation where the pollutant concentration and types may vary (Taghavi et al., 2023; Tomar et al., 2021).


Species

Contaminants Removed

W. anomalus WO2 

Lead (Pb)

R. mucilaginosa RO7

Lead (Pb)

Pleurotus Ostreatus

Various Heavy Metals

Cortinarius species

Carbon (Carbon Sequestration)

Suillus species

Carbon (Carbon Sequestration)

Fungi (General)

Polyaromatic hydrocarbons, Herbicides, Pesticides, Heavy Metals

Arbuscular Mycorrhizal Fungi

Various Heavy Metals


The role of microbial enzymes to the efficacy of fungi for mycoremediation is essential in the process of degradation, oxidation, and reduction for environmental contaminants. Studies into the specific enzymes’ catalysts for this process include, most notably for soil, dehalogenases, which are able to remove halogens from a given substrate such as bromine or chlorine, and cytochrome P450—an enzyme also found in the liver—responsible for the breakdown of many drugs and chemicals (as shown in figure 5), are both endogenous and exogenous to its genetic makeup (Sobika et al., 2021; Brahmachari et al., 2023).


Figure 5 Cytochrome P450 catalyzed reaction. Adapted from “Microbial Enzymes Used in Bioremediation,” by S. Bhandari et al., 2021 (https://doi.org/10.1155/2021/8849512).


The enzymatic process of fungi is essential to the transformation and biosorption/bioaccumulation of heavy metals. Through a complex series of interactions, the toxicity of heavy metals is minimized. Research on fungal microbiology suggests heavy metals become bound in the cell walls of a wide range of fungi through biosorption via enzymatic reactions of the metal ions. The enzymatic transformation in this process can catalyze redox reaction that alter the oxidation state of the metal, increasing the stability and decreasing the toxicity by making it less bioavailable in the environmental pathways (Ramya et al., 2021; Amiy et al., 2015; Raja et al., 2017). Fungi have adapted this ability through a genetic necessity to protect their own cellular structure from the toxicity of heavy metals.

Quality soil development is associated with high levels of organic carbon and nitrogen in soil that is readily bioavailable and created through the decomposition or organic matter attributed in part to fungi (Di Lonardo et al., 2020). The bioavailability of nutrients through the process of nutrient cycling is crucial to the development of plants. It is through this process that nutrients necessary for the life of plants are given and non-essential heavy metals are sequestered and rendered obsolete in terms of bioavailability through the oxidation of the metal ions (Robinson et al., 2021). This relationship between pedogenesis and mycoremediation enhances the potential applications of this process.

Recommendations

Mycoremediation as a tool for bioremediation of heavy metals offers a sustainable approach that is applicable to a variety of situations, from home gardens to agriculture and pesticides, mine tailings, water treatment, and waste management.

Industry

Current processes of metal recovery are  expensive and produce adverse pollution, such as leaching through solvent extraction (Adeyemi et al., 2023). Alternatively, bioleaching as a bioprocess over conventional processes, eliminates undue pollution, while additionally aiding in precious metal waste streams through more efficient recycling of the metals (Liang & Gadd, 2017).

Industrial waste treatment management can more efficiently address bioavailability of heavy metals before contaminating soil using fungi through liquid media as a catalyst. According to Jaishankar and his colleagues this practice was studied in “electroplating, paint, leather, metal, and tanning industries” for heavy metals: “Pb, Cd, Cr and NI…isolated from sewage, sludge and industrial effluents” (Jaishankar et al., 2014). High scalability with minimal research is possible when used in an isolated setting, making this an appealing market-based alternative to traditional methods.

Waste management

The U.S. is one of the leading producers of electronic waste, with unquestionably unethical disposal practices. Fungi’s ability to sequester both precious and heavy metals (as well as poly-based materials) suggests use in finding domestic alternatives to sending e-waste to other countries. Complex materials, like e-waste, with a variety of metals and materials means metal tolerant fungi, such as Penicillium Simplicissimum cannot solely account for the remediation, but do offer promising outcomes when combined with additional strains that account for the deficiencies of another (Srivastava et al., 2022).

Given specific species’ proven adaptability and resilience to harsh climates, the introduction of fungi to landfill sites can bioremediate the heavy metals and other pollutants that have leached into the ground, lowering the long-term polluting effect, or offering a solution closer to carbon-neutral in the conversion or repair of landfill sites to repurposed uses.

Homes and Gardens

Mycoremediation in home settings for contaminated soil caused through municipal services or ordinances (such as spraying), or past industrial activity jeopardize gardens due to certain plant and vegetables’ ability to uptake heavy metals and introduce them to environmental pathways. Phytoremediation can be effective for the removal of unwanted substances; however, incidentally, this puts human health at risk through the unintentional consumption of contaminated plants not intentionally used for this purpose. A study from the University at Buffalo suggests “mycelium has shown tremendous promise as a solution to cleaning up environmental pollutants in soil…using dried mycelium membranes…that are premanufactured” (Hill, 2022). An insertable and removeable material is both marketable to home consumers and does not require prior intensive expertise into cultivation of mycelium or mushrooms. This study focused primarily on mycelium cell walls’ ability to uptake and retain lead.

Agriculture and Pesticides

Pesticides and fertilizers historically contain heavy metals such as arsenic, cadmium, and lead, according to the Minnesota Department of Health (MN Dept. of Health, 2023). The effect is bioavailable non-essential heavy metals contaminating fields with a need for the reclamation of the soil. Species identified for both their ability to sequester heavy metals and to aid in the breakdown of historical pesticides would prove most suitable for this application. Species Aspergillus Niger is identified to break down endosulfan, a pesticide used primarily in India, and has shown to be effective in sequestering heavy metals (Bhalero & Puranik, 2007). The introduction of mycoremediation practices can have a positive compounding effect on the health of the public through the detoxification of the food supply.

Mining

Mine tailings are a known cause of pollution subject to “aeolian dispersion” leading to a “significant source of air pollution in the form of particulate matter” as published by the Environmental Health Perspective (Mendez & Maier, 2008). Explored in this article is the phytostablization of mine tailing, particularly in closed mines of arid or semiarid environments, where conditions are most suitable to aeolian dispersion. Mycoremediation offers a complimentary solution that could both stand alone or increase the efficiency of revegetation through the symbiosis of plant and fungi relationship.


Figure 6 Earthworks. (n.d.). [Diagram of acid mine drainage process]. Acid Mine Drainage


Acid mine drainage (AMD) threatens local soil, water, and wildlife, and is considered irreversible (Bogush & Лазарева, 2011). However, the leaching of heavy metals may be addressed through biofiltration with fungi. Although current research is limited to the use of algae, biochar, and bacteria (or microbial processes) of filtration, the potential for Mycoremediation suggests research is necessary given the properties of known fungi on the topic. 

Water Treatment

In relation to both AMD and municipal applications, water treatment and wastewater treatment could benefit from the incorporation of fungi into the filtration processes to remove heavy metals before water or runoff is used or recycled. This process is known as mycofiltration. The technology has already reached a level of commercial viability as deployed by the Wandle Trust in the United Kingdom in 2014 by demonstrating the installation of  mycofiltration sacks where surface water would be most polluted along a local body of water (Wandle Trust, 2014).

The continuation of research and implementation of this technology would serve to better filter storm water runoff where pollutants can be found in high concentrations in storm drains, filtering the water before it reaches large bodies of water. 

Conclusion

Soil contamination is a multifaceted and pervasive issue with profound implication on environmental and human health. Mycoremediation presents a novel and sustainable solution in junction with existing remediation processes without secondary pollution.

Mycoremediation through bioaugmentation and bioremediation presents economically appealing and ecologically neutral or beneficial approaches to heavy metal remediation that is both novel and innovative to environmental restoration and conservation.  The applications are diverse, and encompass a broad range of potential uses, from the revitalization of home gardens, the enhancement of existing practices in water treatment and filtration, or waste management.

Mycoremediation is an essential necessity in environmental management strategies that demands continuation in research and implementation for the future of environmental policy. 

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