Keywords

18.1 Introduction

Phytoremediation is the technique in which living plants are used for remediation of the contaminated soils, water, sediment, and ecosystem (Cunningham and Ow 1996). The utilization of fungus for remediation of the contaminated resources is fungal phytoremediation. Fungi survive about 5300 years (Gams and Stalpers 1994). Armillaria bulbosa is the longest and largest living fungal species in the world (Smith et al. 1992). Fungi play vital role in all ecosystems and are capable of regulating the nutrient as well as energy flow through their mycelial networks, and hence, they are considered as natural and true ecosystem engineers (Lawton and Jones 1995). The ecological and biochemical capacity of fungi to degrade environmental chemicals and decrease the risk associated with metals and metalloids through chemical modification or its bioavailability makes them as a potent bioremediation agent. However, to date, the ecological demands and ecophysiological strengths of fungi in bioremediation have not been potentially explored. Unlike bacteria, the fungal phytoremediation does not require absolute water phase as fungus can grow in the air-water interface. However, the water phase acts as a carrier for nutrient transport for hydrophobic organic contaminants.

Interaction of fungi with metals includes mobilization and immobilization in the mycosphere, sorption to cell walls, and uptake into fungal cell. Thereafter, chemical transformation, translocation, and metabolization along with reactions of pollutants on fungal enzymes such as extracellular oxidoreductases/cell-bound enzymes allow fungi to act on various metal pollutants (Harms et al. 2011; Prakash 2017). Hence, the role of filamentous fungi becomes important where translocation of essential factors necessitates for the transformation or detoxification of environmental chemicals. Conversely, requirement of fungal degradation is needed for pollutant classes, i.e., dioxins, 2, 4, 6-trinitrotoluene, synthetic drugs, or endocrine-disrupting chemicals found in medium as these are inefficiently degraded by bacteria (Harms et al. 2011; Macellaro et al. 2014; Mnif et al. 2011). Fungi can be used in the treatment of contaminated soil surface with organic/metal contaminants, water streams with trace organic contaminants and removal of metals from water stream, VOCs from air, and organic pollutants using isolated extracellular enzymes instead of whole fungi (Nguyen 2015; Pinedo-Rivilla et al. 2009).

Conversely, an increasing trend toward energy- and cost-efficient passive phytoremediation methods for the reclamation of contaminated natural resources, i.e., land, water, and air is the need of hour. The low degree of mechanical intervention in natural attenuation of natural resources especially soils favors the importance of filamentous fungi in sustainable fungal phytoremediation (Harms et al. 2011). Another aspect involves arbuscular mycorrhizal (AM) fungal association with plants, as these are integral, functioning parts in plant roots and enhance plant growth even under highly contaminated soils with heavy metals. AM fungi play an important role in metal tolerance and accumulation of heavy metals in the plants root growing on heavy metal-contaminated soils. Hence, isolation of stress-adapted indigenous AM fungi could be targeted as a potential biotechnological tool for inoculation of plants for degraded ecosystems. Major role of AM fungi attributed to the secretion of glomalin (a glycoprotein), stabilizing the aluminum in soil and in the roots of Gmelina plants, has been reported (Dudhane et al. 2012). There are several fungal species such as A. niger, A. pullulans, C. resinae, F. trogii, G. lucidum, Penicillium sp. (Loukidou et al. 2003; Say et al. 2003), R. arrhizus, and T. versicolor, which efficiently recover heavy metals from the contaminated environment. Heavy metal bioaccumulation potential of A. versicolor was observed 6 for 50 mg/L Cr (VI) and Ni (II) and 5 for Cu (II) ions with the 99.89, 30.05, and 29.06% removal yield, respectively at optimal pH by Taştan et al. (2010). Kumar Ramasamy et al. (2011) found that Aspergillus fumigates is very suitable for removal of Pb (II) ions from the electronic waste aqueous solution (containing Pb 100 mg/L) through batch sorption with adsorption capacity of 85.41%. El Zeftawy and Mulligan (2011) found that micellar-enhanced ultrafiltration MEUF could treat phosphorous-rich heavy metal wastewater with a transmembrane pressure of 69 kPa, at 25 °C and pH 6.9. Häyrynen et al. (2012) observed that pressure and cross-flow velocity significantly affects the flux of Cd and Cu in MEUF purification methods, while P was not retained (Landaburu-Aguirre et al. 2012). Thus, potential application of MEUF for heavy metal decontamination of nutrient-rich wastewaters has been recently justified (Mani and Kumar 2014).

18.2 Potential Sources of Heavy Metal Contamination and Associated Risks

18.2.1 Anthropogenic

Based on the relative higher densities (3.5–7.0 g/cm3), atomic weights, or atomic numbers (>20), metals are termed as heavy metals. Some heavy metals are essential nutrients (Fe, Co, Zn), relatively harmless (Ru, Ag, and Id), but potentially can be toxic in larger amounts or certain forms. Conversely, heavy metals, such as Cd, Hg, and Pb, are highly poisonous. The common source of heavy metals is antiseptics, fertilizers, sedimentation, cars, golf clubs, mobile phones, plastics, self-cleaning ovens, solar panels, and particle accelerators (Gupta et al. 2018; Singh et al. 2013; Hübner et al. 2010; Singh et al. 2017; Yadav et al. 2018b, c) (Table 18.1). The potential sources are atmospheric deposition; automobile exhausts, metal industries, mine spoils, river dredging and urban refuse disposal, pyrometallurgical industries, and fossil fuel combustion are also the main sources of heavy metals (Lottermoser 2010a, b; Matta et al. 2018; Prasad 2001) (Table 18.1). Industries such as microelectronics, plastics, refinery textiles, wood preservatives, agrochemicals (fertilizers and pesticides), sugar-based industries and waste disposal sewage sludge, landfill leachate, and fly ash disposal are also some of the chief sources of the heavy metals (Bhatia et al. 2015; Gupta et al. 2018; Singh et al. 2013a; Kumar et al. 2016; Singh and Kumar 2006; Yadav et al. 2018b, c) (Fig. 18.1).

Table 18.1 Sources of heavy metals and respective anthropogenic activities (adapted and modified from Yadav et al. 2017)
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Fig. 18.1
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Overview of sources of heavy metal pollution and its agroecological consequences. (Source: Srivastava et al. (2017))

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18.2.2 Water Resources

Water contamination due to heavy metals is a known threat and has been attributed to anthropogenic sources involving untreated domestic and industrial wastewater discharges, chemical spills, and agricultural residues (Malyan et al. 2014; Tchounwou et al. 2012). The outcome is poor water quality, degradation, and water borne-human health risks even at lower doses of heavy metals (Kumar et al. 2014; Micó et al. 2006; Wongsasuluk et al. 2014). Major heavy metals such as lead, mercury, chromium, cadmium, copper, and aluminum for water contaminations are originated through anthropogenic activates and natural incidents like seepage from rocks, volcanoes, and forest fires. Over a time period, heavy metals enter in the food chain through water, and there chronic effects could be manifested for many years and may exert several threats such as mental disorders, pain in joints, gastric disorders, and even cancer. Human population living near industries are more susceptible to heavy metal toxicity. Along with that, pregnant women and malnutritioned children are more vulnerable to heavy metal toxicity. Freshwater bodies are heavily affected by pathogens from untreated wastewater and heavy metals from mining and industrial release (Caravanos et al. 2016). It has been reported that more than 80% of the world’s wastewater is released to the environment without treatment, which is the major cause of nearly 58% diarrheal disease (major cause of child mortality) (Connor et al. 2017). Hence, it is of utmost importance in the coming future to mitigate this global threat of water toxicity with proper remediation measure, and techniques are required for the treatment of water. In that context, fungal phytoremediation serves as an environment-friendly, pocket-friendly, and reliable technique.

18.3 Role of Heavy Metals in Living Beings

Heavy metals such as chromium (glucose metabolism), cobalt (metabolism), copper and iron (oxygen and electron transport), zinc (hydroxylation reactions) (Nieboer and Richardson 1978), manganese and vanadium (enzyme regulation), nickel (cell growth), and selenium (antioxidant and hormone production) (Emsley 2011) are important for certain biological processes. Molybdenum (catalysis of redox reactions), cadmium (in marine diatoms), tin (growth in a few species), and tungsten (metabolic processes of archaea and bacteria) may be required for growth of different species (Emsley 2011). A deficiency and excess of any of these above-discussed heavy metals may impart heavy metal poisoning of living beings (Venugopal and Luckey 1978). Hence, excess amount of heavy metals could dysfunction various physiological and biological effects in the human beings which have been elaborated in next sections.

18.4 Possible Impacts of Heavy Metal Contaminations

18.4.1 On Humans

Non-essential metals can escape control mechanisms such as binding to specified cell constituents, cellular processes malfunctioning, compartmentalization, homeostasis, oxidative deterioration, and transport, and therefore, they have toxic and further lethal effects (Gupta et al. 2018). The important health symptoms of heavy metal toxicity in human are central nervous system disorders, dementia in adults, emotional instability, insomnia, intellectual disability in children, kidney diseases, liver diseases, depression, vision disturbances, and increased morbidity and mortality rate (Jain et al. 2015; Yadav et al. 2018b, c). The metal toxicity depends on the generation of oxidative stress (increased reactive oxygen species (ROS) and reactive nitrogen species (RNS) production; depletion of intracellular antioxidant stores and free radical scavengers) (Jan et al. 2015). Heavy metals toxicity due to occupational exposure mainly responsible for multiple organ systems and toxicity levels mainly depends on the form and type of the heavy element, on route and duration of the exposure, and, to a greater extent, on a person’s individual susceptibility (Jan et al. 2015) (Fig. 18.2).

Fig. 18.2
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Trophic transfer of toxic HMs from soil to plants to humans and organism’s food to humans and their toxicity. (Adapted with permission from Saxena et al. (2019))

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18.4.2 On Plants

Heavy metal contamination in soil and water resources affects growth and yield performance as well as nutritional quality of plants to a great extent. For the plants which are grown in close vicinity to the contaminated soil and water or at the contaminated site, metals cause physiological dysfunctioning and biochemical alterations (Sharma et al. 2012a; 2012b). In case of vegetables requiring high moisture percentage, the use of heavy metal-contaminated irrigation water is one of the major causes for high metal toxicity in plants. Some of the heavy metals at a lower concentration are required for optimum performance of plants; however, excess amount may cause toxicity, e.g., chromium (Yadav et al. 2018b, c). Common features pertaining to metal toxicity are reduced biomass reduction, leaf chlorosis, and root growth and seed germination inhibition (Ghani 2011). Cr toxicity considerably affects the physio-biochemical processes in barley, cauliflower, citrullus maize, wheat, and vegetables (Ghani 2011). ROS signalling and oxidative damage affect enzymes like catalase; cytochrome oxidase and peroxidase with iron as their component are affected by chromium toxicity. The catalase activity stimulated with an excess supply of chromium-inducing toxicity has been studied, concerning nitrate reductase activity, photosynthesis, photosynthetic pigments, and protein content in algae (Nath et al. 2008). Pb and Cd also affect the gas exchange attributes, ROS system, cause chlorophyll deterioration, and ultimately the overall performance of major agricultural crop worldwide (Anjum et al. 2015; Mobin and Khan 2007; Pinho and Ladeiro 2012; Zhu et al. 2007). The microbes are ubiquitous in nature and have been reported from diverse sources including extreme habitats (Yadav et al. 2015a, b, c, 2017b) and as plant microbiomes (Kour et al. 2019b; Yadav 2018; Yadav et al. 2016). These microbes have potential applications in agriculture, industry, pharmaceutical, and environment (Kour et al. 2019a; Yadav et al. 2017a, 2018a, 2019a, b).

18.5 Phytoremediation of Contaminated Soils/Water Resources

In general, phytoremediation is the process of bioremediation using plant species called hyperaccumulators to reduce the toxic contaminants in the environment. This is a novel advanced technology, considered as eco-friendly having lesser investment cost. Current scenario explains the feasibility and accountability of this technique. Many plant species are being used as hyperaccumulators, and new species are being explored (Ali et al. 2013). Eventually, phytoremediation is an interdisciplinary branch that requires knowledge for soil composition, soil microbiology and environment engineering, plant physiological processes, and in recent development use of lower plant groups as a sustainable system for the bioremediations of toxic heavy metals (Pisani et al. 2011). Some of the species of the plants used in phytoremediation are Robinia pseudoacacia and Sesbania drummondii for Pb, Stanleya pinnata for Se, etc. (Yang et al. 2016).

18.6 Fungal Phytoremediation

As its name explains, fungal phytoremediation or mycoremediation is a form of bioremediation where the degradative abilities of fungi are utilized to remove or neutralize the harmful contaminants present in soil and water. It is a relatively new form of bioremediation where its use only spans a few decades, beginning as early as 1966 (Matsumura and Boush 1966), but it is known or being practiced to a lesser extent. Malathion (an insecticide and neurotoxin) breakdown was successfully done using Trichoderma viride and Pseudomonas (Matsumura and Boush 1966). There are several mushroom species identified till date to remove the heavy metals from the contaminated resources. The important species are Galerina vittiformis (Cu, Cd, Cr, Pb, and Zn), Hypholoma capnoides (Ti, Sr, and Mn), and Marasmius oreades (bismuth and titanium). The other important fungal species which are having high fungal phytoremediation potentials are Agaricus bisporus, Lentinus squarrosulus, Phanerochaete chrysosporium, Pleurotus ostreatus, Pleurotus tuber-regium, P. ostreatus, P. pulmonarius, and Trametes versicolor (Adenipekun and Lawal 2012; D’Annibale et al. 2005).

In this chapter, the sources of different heavy metals (HMs) with adverse effects in major countries on human health along with the permissible limits of HMs has been highlighted to have the understanding on the current scenario of fungal phytoremediation works (Table 18.2). Similarly, the different groups of fungus having remediation potential for the most potent heavy metals have been highlighted in Table 18.3. Further, the categorical classification of different fungus and their importance in particular metal have been worked out with extensive literature survey in order to target potential fungal phytoremediation techniques for the metal contamination in soil. In addition to that for the mechanistic understanding on growth conditions, enzyme production, type of compound degradation has been explored (Table 18.4). The bioconversion efficiency of wastes by some fungal species has been reported worldwide (Table 18.5).

Table 18.2 Sources of heavy metals (HMs) and their target organs in human with adverse effects in major countries along with the permissible limits of HMs
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Table 18.3 Categorical classification of fungal species targeting metal remediates for fungal phytoremediation
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Table 18.4 Some commonly used fungal species, for mechanistic understanding on growth conditions, enzyme production, type of compound degradation, and key references
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Table 18.5 Bioconversion of waste by fungal species
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18.6.1 Mechanistic Approach of Fungal Phytoremediation

In fungal phytoremediation, mechanism of fungal partner is very important to understand. Fungal phytoremediation has got several mechanistic pathways for bioremediation process. In general, fungus increases the ability of roots to absorb more heavy metals. Its mechanism could be devised as (i) avoidance and (ii) sequestration mechanisms. Avoidance ameliorates the metal toxicity though decreasing the concentration of metal by biosorption, precipitation, and uptake or efflux. Conversely, sequestration involves the formation of compounds for intracellular chelation (−) and further dilution in plant tissues due to plant growth, exclusion from uptake through precipitation, and chelation in the rhizosphere (Danesh et al. 2013). Both of these mechanisms may play part or even could counteract. Overall, the reduction in absorption owing to retention and immobilization takes part in fungal structures or mycorrhizal roots. The activation of specific/nonspecific transporters and pores play the part in the plasma membrane in plants and fungi, chelation in the cytosol and the sequestration into the vacuoles of plants as well as in fungal cells. Further, transportation and exportation occur through the fungal hyphae, involving both active and passive transportation into the mycorrhizae (Fig. 18.3).

Fig. 18.3
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Mechanisms involved in remediation of HM-contaminated soil by HMT-PGP microbes-plant interaction. (Sources: Mishra et al. (2017))

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Fungal phytoremediation is proven to be efficient, where the abilities of hyperaccumulators diminished. One of the limitations of hyperaccumulators is to accumulate less concentration of contaminants due to their small biomass while fungi can accumulate more due to their some molecular mechanisms. Hence, intervening the interaction of hyperaccumulator plant with fungi and other legume plant and herbs could help us to use it as a potent strategy for phytoremediation (Yang et al. 2016). Therefore, further exercise is required for explaining the molecular mechanisms underlying.

18.6.2 Factors Influencing the Fungal Phytoremediation

Several factors influencing the fungal phytoremediation include species of plant and fungi, their association strength, plant-soil interaction, physical and chemical properties of soil, and biophysical aspects such as temperature, pH, salinity, soil microbes, and metal characteristics (Fig. 18.4).

Fig. 18.4
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Relationships among the factors affecting phytoremediation efficiency. (Adapted with permission from Saxena et al. (2019))

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18.6.2.1 Temperature

The fungi are having their different temperature range for growth based on different habitat, such as mesophilic (5–35 °C), psychrophilic (below °C), thermophilic (above 40 °C), etc. With the change in the temperature, the bioavailability of the heavy metals is also changed. An increase in soil temperature tends to speed up the concentration of metals in the soil due to increase rate of organic matter degradation. It was observed that high temperature is favorable for the absorption of heavy metals. However, the temperature also affects the growth of fungi. So, fungi with high temperature tolerance will be beneficial for the bioremediation process (Yadav et al. 2018b, c). Fe and Mn are mobile in alternating in dry and wet conditions (Boisselet 2012).

18.6.2.2 pH

pH is an important parameter which controls the availability of heavy metals to get remediated. Heavy metals are present in a dissolved state if the pH of the solution is at 2–3. However, the bioavailability, dissolution, and precipitation of each metal have its own intrinsic capacity along with the pH range.

18.6.2.3 Redox Potential

The redox potential affects the state of oxidation of the metals, as different forms show different behaviors in solubility. Anaerobic conditions in deeper parts of the soil for oxidoreductive reactions of microorganisms can accelerate the heavy metal degradation. Redox potential along with pH affects the fungal-phyto interactions with the soil components by altering the sorption capacity and influencing stability of complexes.

18.6.2.4 Heavy Metals Bound with Hydrocarbon

Some of the heavy metals are present in the bound form of the other compounds such as polycyclic aromatic hydrocarbons (PAH). The remediation of such metals can be achieved only after degradation of the host compound. Some fungal species such as Agaricus bisporus, Pleurotus ostreatus, and Ganoderma lucidum are observed to degrade the hydrocarbons in petroleum. Pleurotus ostreatus is beneficial in degrading the PAH (García-Delgado et al. 2015).

18.6.2.5 Other Growth Requirements

Apart from the temperature, other factors such as moisture percentage, sugar and other organic materials, oxygen, amino acids, vitamins, fatty acids, etc. are also important for fungal growth. The change in these requirements can also enhance/limit the fungal phytoremediation potential.

18.6.2.6 Fungal Species

Different fungal species are having different capacity to remediate the heavy metals from the soil and water based on their internal genetic constitutes and external growth and environmental factors. To check the any new/existing species remediation potential, the arsenic test (preliminary assessment) will serve as good choice. Later on, the heavy metals-based potential check can be made and compared with the existing data. However, some of the fungal species can serve as a bioindicator of particular heavy metals. In this case, these species serve as the reference species for the remediation potential. For example, Lycoperdon perlatum may be employed as a bioindicator of heavy metals and selenium in soil pollution (Quinche 1990).

Filamentous fungi are known to possess higher adsorption capacities for heavy metal removal (Singh and Gauba 2014). Trichoderma and Mortierella species isolated from the soil and Aspergillus and Penicillium species isolated from marine and terrestrial environments, respectively, have the high ability to remediate contaminated environment (Thenmozhi et al. 2013). Arbuscular mycorrhizal fungus Glomus mosseae formed a symbiotic associate of P. vittata L. and possessed substantial resistance to arsenic toxicity by increasing the plant biomass, and this mycorrhiza can enhance the arsenic sink. Mycorrhiza can be a potential tool for fungal phytoremediation by choosing the native species of fungi/host and alteration in the association by changing any of the fungi/host or controlling factors or inoculation of the new fungal strains. This can be achieved through re-vegetation on the contaminated sites such as mine areas.

18.7 Precaution Prerequisite

Some prerequisite precautions are needed for successful achievement of fungal phytoremediation which involves selection of correct fungal species for targeted metal contamination for developing a screening protocol (Matsubara et al. 2006). Among these precautions, major points have been prescribed in general which should be considered. These involve as follows:

  • The catabolic activity and capacity of organisms involved to transform the target compound(s) and bring the concentrations to levels that meet regulatory standards

  • The rate of bioremediation

  • The possible production of toxic by-products at dangerous levels during the remediation process

  • Adaptability of the process to site conditions (environmental and anthropogenic)

  • Economic viability of the process

18.8 Conclusion and Future Prospects

As explained above, fungal phytoremediation is a very potent technology for sustainable bioremediation of contaminated soils and water. In general, it is still in infancy in laboratory conditions and greenhouse, which limits the outcome to the actual field condition pertaining to multiple factors. Hence, the assessment of the efficiency rate of fungal phytoremediation must be tested in field condition in order to commercialize this green technology by evaluating the different plant for targeted heavy metal. Similarly, there are few lags in this eco-friendly remediation technology such as to increase the growth rate of plants, increase the biomass of such plants for maximum absorption of heavy metals, and take a look on possible hazards on food chain. Field experiments should be devised to explore the hyperaccumulators from where these metals can be harvested easily and feasible techniques to harvest these metals without exerting a negative impact on environment. Also, the key to mycoremediation is determining the right fungal species to target a specific pollutant. Desirable traits should be identified from the hyperaccumulator and fungi genome. Such gene can be selected by the conventional techniques or new technologies of hybridization such as protoplast fusion. Identification of genes coding for different toxicants from different hyperaccumulators and their transformation in same plant can develop SUPERBUG plant for phytoremediation. Besides the several constraints and limitations, fungal phytoremediation appears to be the most potent, eco-friendly, economical, and environmentally attractive option of bioremediation in heavy metal-contaminated soils and water resources. Many fungal species can grow under various contaminated conditions, thus enabling remediation in the contaminated environment that may not be suitable for other organisms. Based on our review of the subject and key questions raised on the concerned topic, we do not conclude that it could solve the issues of metal or hydrocarbon contamination completely. Conversely, a synergistic approach involving proactive policy designing in the field of fungal phytoremediation ranging from lab-based desirable trait based targeted metal contaminations with a particular fungal species, after testing it in green houses it has a potential to be replicated in the field environment for the future safety of soil, plant, water resources and rising human population prone to future heavy metal contaminations.