Keywords

1 Anthropogenic Pollution and Soils

When talking about soil, we refer to the most superficial layers of the earth’s crust, which are capable of supporting plant growth, being the result of the action of environmental conditions on natural bodies and remains of living organisms, therefore representing a dynamic body made up of liquids, gases, mineral and organic solids, and living organisms. In its study, it must always be taken into account that it represents a very dynamic body formed by an abiotic component and a biotic one that is closely related to each other. This is very important in understanding its formation process and all those that take place continuously (nutrient cycle, decomposition of organic matter, degradation of pollutants, etc.) (Cachada et al. 2018). In this sense, the soil not only represents the main substrate for food production but is also a natural habitat of biodiversity, a store of nutrients, and a regulator of the water cycle (Cachada et al. 2018; Koul and Taak 2018).

Anthropogenic activity can seriously affect the functions of soils, mainly through the agricultural and forestry sectors, construction, tourism, and industrial activities, increasing in conjunction with the increase in the world population. This leads to an increase in the amount and intensity of soil use, causing compaction, erosion, salinization, pollution, acidification, and loss of organic matter and biodiversity (Cachada et al. 2018).

With regard to soil contamination, it represents a serious problem in world expansion after the Industrial Revolution, due to the massive use of agrochemicals, the burning of fossil fuels, and the expansion of industrial activity. A soil is considered contaminated when it does not carry out its own processes or cannot be used for its estimated use due to the presence of contaminants (Cachada et al. 2018). The main sources of anthropogenic soil contamination include solid wastes (domestic waste, market wastes, hospital wastes, kitchen wastes, slaughterhouse wastes, industrial wastes, livestock and poultry wastes, ceramic wastes, glass, and metals), agrochemicals (pesticides, fertilizers, hormones, and animal manure), radioactive wastes, chemical wastes (hydrocarbons, solvents, and measured metals), and mining and smelting (heavy metals) (Shankar 2017; Cachada et al. 2018; Koul and Taak 2018).

Soil pollution not only causes serious environmental effects but is also against health. Contaminants present in the soil can affect human health directly when inhaled or in contact with the skin, but the most common is that they enter through ingestion, by contaminating food and water (such as aquifers). The effects that they can have on health are very diverse depending on each specific pollutant; for example, exposure to heavy metals such as chromium, solvents, hydrocarbons, or pesticides can lead to the appearance of cancer, neuromuscular disorders, and/or congenital disorders. Similarly, soil pollutants affect ecosystems, reducing the reproductive capacity of organisms, their ability to feed themselves, and their growth and development, causing serious changes in their populations and communities. Therefore, soil pollution affects ecosystem functions, by modifying its living component (Shankar 2017; Koul and Taak 2018).

The main economic sector affected by soil pollution is agriculture, seriously affecting both productivity and the quality of crops. The proportion of contaminated soil continues to increase throughout the world, estimating current losses in crop yields by about 15–25% as a consequence of soil and water contamination. Pollutants can prevent the absorption of nutrients by the roots of crops, by interacting with them, modifying the soil pH and electrical conductivity, and causing the loss of soil fertility. In addition, many of these pollutants can be absorbed by plants and stored in their tissues, contaminating food, such as heavy metals. On the other hand, soil pollution can significantly affect the water supply to plants, by increasing the salinity of soils and preventing its infiltration/percolation (Saha et al. 2017; Koul and Taak 2018; Elbana et al. 2019). In this sense, it is important to highlight that agriculture is also an important source of soil and air pollution due to the use of agrochemicals, such as pesticides (Bauer et al. 2016).

1.1 Pesticides

Pesticides are chemical substances used on agricultural land and public and private areas in order to eliminate, avert, deter, control, and/or kill populations of biological agents that cause harm to human interest (Mahmood et al. 2016; Ozkara et al. 2016). Its use in the agricultural sector is above 5 billion pounds worldwide (Mahmood et al. 2016), although it is constantly increasing, due to the need for higher food productivity to feed the growing world population (Ozkara et al. 2016). At present, it is considered that 40% of agricultural production is lost as a result of pests, pathogens, and weeds, a percentage that would be higher without the use of pesticides, an important sign of their need today (Mahmood et al. 2016). Therefore, since the nineteenth century, the use of chemical pesticides in pest control has caused a widespread release of these xenobiotics into the environment. Specifically, more than 500 different pesticide formulations are currently in use, which affect not only their target organisms but many non-target organisms, including humans. In addition, many of these pesticides are hardly degraded and can persist up to 30 years in water or soils, such as organochlorine insecticides, which influences their easy probability of entering the food chain (Ozkara et al. 2016).

In this sense, the risks derived from the use of chemical pesticides considerably exceed the benefits obtained, having drastic effects in aquatics and terrestrial ecosystems, affecting animal and plant biodiversity by acting on non-target species. Among the different groups, insecticides are the most harmful pesticides for the environment, followed by fungicides and herbicides, due to their toxicity (Mahmood et al. 2016). The pesticides most frequently detected in soils are contaminated with organophosphorus pesticides (OPs), having been detected in more than 90% of soils in China. Organochlorine pesticides (OCs) include many products banned around the world, but due to their persistence, they are easily detected in soils today, as is the case with 2,2-bis(4-chlorophenyl)-1,1,1-trichloroethane pesticides (DDTs). On the other hand, the pesticides most implicated in poisoning problems on the planet are the anti-cholinesterase pesticides, which include both organophosphates and carbamates. Almost 70% of pesticides used in agriculture continuously contaminate soil and water through their residues. About 40% are herbicides, 30% insecticides, and the remainder include all pesticides used against plant pathogens (Sun et al. 2018).

The uncontrolled use of pesticides causes serious damage to biodiversity, both directly and by accumulating in the food chains. The most common is to report a reduction in the amount and variety of weeds, shrubs, and insects in the ecosystem, but the populations of higher animals such as birds are also reduced. As regards human health, the World Health Organization has indicated that 3 million cases of pesticide poisoning and more than 20 thousand deaths are registered annually. Its effects on health are highly variable and dependent on various factors, although they can immediately cause headaches, respiratory tract irritation, digestive problems, or signs on the skin such as rash and blisters, while its effects are chronically reflected in damage to the immune system, neurological, cancer, or reproductive problems, among others (Mahmood et al. 2016).

1.2 Heavy Metals

The term heavy metals includes all those elements with a density greater than 4 g cm−3, which includes both metals and metalloids (such as arsenic). Although some of them represent essential elements in many biological processes, in high concentrations they can be very harmful to the environment and health. This is because they are not degradable and easily accumulate in organisms. For this reason, in Europe, heavy metals are considered the main pollutants of soil and water (Vareda et al. 2019). The origin of environmental pollution by heavy metals can be found in natural processes, such as erosion, weathering, or volcanoes, although its main source is human activity, which includes textile and paint industries, mining, smelting, wastewater, or use of agrochemicals (Mishra and Nautiyal 2009).

The effect of heavy metals in the environment can be very serious, as a consequence of their persistence and ubiquity. Its toxicity affects all the components of the ecosystem, since they are accumulated in the tissues and pass easily to the different steps of the trophic chain. In soils and waters, high concentrations of heavy metals cause a decrease in soil microbial biomass, diversity, and activities (Abdu et al. 2017). As far as human health is concerned, exposure can occur through ingestion, inhalation, or contact with the skin, causing serious damage to the central nervous system and various vital organs or cancer (Varhdan et al. 2019). As examples, excessive exposure to chromium (Cr) is related to cancer, to mercury (Hg) is related to immune and nervous diseases, to lead (Pb) is related to cardiovascular and neurological diseases, or to cadmium (Cd) is related to cancer or endocrine damage (Mishra and Nautiyal 2009).

In agriculture, the entry of heavy metals is due to irrigation with wastewater, fertilization with livestock manure, and the use of agrochemicals (Rai et al. 2019). The main route of entry of heavy metals into plant tissues is through the roots by absorption, being easily transported by the vascular bundles to the entire plant. Their toxic effect can be highly variable depending on the ability to tolerate their presence, but they generally inhibit germination, growth, and development, by deactivating different enzymes and causing stress responses, such as the accumulation of reactive oxygen species (ROS), which causes serious losses of productivity in crops (Rai et al. 2016; Bhardwaj et al. 2020).

2 Mycoremediation

Bioremediation is defined as the use of different organisms, usually microorganisms or plants, to remove or neutralize the pollutants present in the environment. In the case of microorganisms, their main mechanism of action is based on the production and release of enzymes that interact with pollutants and degrade them completely or convert them into less harmful products (Dangi et al. 2019).

Mycoremediation is based on the use of fungi for the elimination of pollutants from the environment or, at least, their adverse effects (Gupta et al. 2017). Through the secretion of enzymes and other chemical compounds that modify the chemical bioavailability of heavy metals, organic chemicals, and radionuclides, fungi are able to degrade these pollutants. In this way, fungi metabolize and immobilize contaminants in the mycosphere or store them in their own cells (Singh et al. 2020). The main groups of enzymes produced by fungi and involved in the degradation of pollutants include the extracellular oxidoreductases (such as tyrosinases, laccases, manganese peroxidases, lignin peroxidases, etc.), involved in giving fungi the ability to grow on recalcitrant substrates; cell-bound enzymes (such as cytochrome P450s), involved in the formation of intracellular metabolites; and different transferase enzymes (such as nitroreductases, quinone reductases, etc.), involved in the conjugation of pollutants to form nontoxic compounds that are released into the environment (Singh et al. 2020).

Fungi are capable of surviving in a wide diversity of different habitats, even in massively contaminated places, from where there are several groups that are isolated as possible bioremediation agents. Lignocellulosic materials are mainly biodegraded by white-rot fungi, which has been reported with the ability to bioremediate environments contaminated with endocrine disrupting chemicals, such as pesticides, as a consequence of the action of their ligninolytic enzymes on contaminants. In the bioremediation of heavy metals, marine fungi stand out, capable of inactivating their toxic ions with strategies similar to those used to tolerate the high salinity of their habitat of origin. Finally, the other large group of fungi used in bioremediation is encompassed by those that are isolated from those extreme environments where the pollutant is present, for example, wastewater from mining, known as extremophilic fungi (Deshmukh et al. 2016; Singh et al. 2020).

Fungal species capable of biodegrading almost all biodegradable pollutants have been described. As far as toxic recalcitrant compounds are concerned, we are talking about organic compounds that are very persistent in the environment and that have, in a remarkable way, carcinogenic capacity. These pollutants are mainly biodegraded by fungi such as Curvularia, Aspergillus , Mucor, or Penicillium , thanks to the high production of lipases, as in the case of hydrocarbons. Regarding heavy metals, fungi have the highest tolerance and bioremediation capacity against Cd, Cu, and Ni, and they are also capable of mycoremediating various pollutants that present them, such as dyes or pesticides. Regarding municipal solid wastes, their fermentation for the production of biogas and compost applicable as organic fertilizer in agriculture is being considered. In this sense, greater efficiency is required in the process, thanks to the hydrolytic enzymatic machinery of different fungal species, which include cellulases, proteases, amylases, and lipases (Deshmukh et al. 2016; Singh et al. 2020).

Although the ability of various unique species to biodegrade pollutants in soils and waters has been described, the process can be very slow, without completely eliminating pollutants from the site. Furthermore, fungal inoculants require an adaptation time to the contaminated environment to be able to develop and act effectively. In this sense, the accessibility and bioavailability of the contaminant can also significantly reduce the efficiency of the mycoremediation under field conditions process. Furthermore, the partial degradation of certain organic compounds, such as pesticides, can lead to the formation of new pollutants that are more toxic to the environment. For this reason, many authors highlight the importance of using bioremediation consortia formed by fungi and bacteria, greatly increasing their effectiveness and reducing all possible associated limitations. Also, there is even the possibility of transforming endogenous microorganisms in the contaminated environment with genes that allow them to biodegrade the pollutants (Gupta et al. 2017).

2.1 Pesticides

Bioremediation of pesticides in the environment can be carried out by both plants and microorganisms. The main site of pesticide phytoremediation is the rhizosphere, where there is also great microbial bioremediation activity. Therefore, plants are capable of directly degrading the pesticides present in the soil, as well as indirectly, by providing nutrients to their rhizospheric microbiota. In addition, plants can assimilate pesticides and store them in their tissues, degrade them internally through their own enzymatic machinery or that of their endophytic microbiota, and/or transform them into volatile forms that they release into the atmosphere (Eevers et al. 2017).

Regarding the bioremediation of pesticides through the use of microorganisms, numerous investigations have been carried out in recent years, and even complete books have been dedicated, such as the one edited by Singh, in 2016. In this sense, they have described very diverse microbial communities capable of mineralizing, transforming, or degrading pesticides, being the bacteria the group with the largest number of species described so far. As bacterial examples, various species of the genus Pseudomonas are capable of degrading pesticides such as the herbicide 2,4-dichlorophenoxyacetic acid (2,4-D), organochlorine pesticide like endosulfan and lindane, or organophosphorus insecticide chlorpyrifos. In the group of cyanobacteria, different Microcystis and Anabaena have been described with the ability to biodegrade organophosphorus and organochlorine insecticides or the glyphosate herbicide . As regards fungi, for example, various species of white-rot fungi have been described with the ability to degrade various pesticides like atrazine, aldrin, diuron, DDT , chlordane, gamma-hexachlorocyclohexane (γ-HCH), dieldrin, lindane, heptachlor, metalaxyl, mirex, or terbuthylazine (Prabha et al. 2017; Parween et al. 2018).

The mechanisms used by fungi to biodegrade pesticides present in soils and waters include their polar hydroxylation and demethylation, esterification, dehydrogenation, hydroxylation, and dioxygenation, for which it is essential to have a significant enzymatic capacity (Maqbool et al. 2016; Spina et al. 2018).

2.2 Heavy Metals

Regarding heavy metals, without entering into metallic pollutants, such as hydrocarbons or dyes, there are also contaminated environments that can be bioremediated through the use of plants and/or microorganisms. Plants remove heavy metals from soils and waters after absorbing them by the roots through their phytoaccumulation in different tissues and organs, their phytodegradation through different enzymes and metabolic pathways, and their phytovolatilization through their transformation to volatile forms that they release into the atmosphere, thanks to its phytostabilization and thanks to its transformation into nontoxic forms by root exudates (Muthusaravanan et al. 2018).

Today, heavy metal removal by microorganisms represents a series of advantages over other strategies, such as its simple-to-use, low cost, high adsorption capacity and large availability (Yin et al. 2019). In the case of bacteria, they are capable of acting against the toxic effects of heavy metals in the environment by producing siderophores that chelate them, as different Pseudomonas species do with Pb, or by producing metal-binding proteins, called metallothioneins, by different species of Bacillus in the presence of Pb (Choudhary et al. 2017). As regards fungi, the main fungal species involved in the mycoremediation of heavy metals are included within the genera Aspergillus , Trichoderma , and Penicillium . For this, they use strategies based on extracellular sequestration by extracellular polymeric substances, such as chitosan, or on intracellular sequestration by storing them in vacuoles (Choudhary et al. 2017; Ul Hassan et al. 2017).

2.3 Other Pollutants

Many other pollutants related to pesticides and heavy metals can be present in the environment and are susceptible to being eliminated by the action of fungi, such as hydrocarbons, aromatic amines, or radioactive wastes.

Hydrocarbons are classified as aliphatic or aromatic according to their chemical structure, both types being present in oil and natural gas, as sources of origin. These compounds are not only used as fuel but also represent the raw material for many substances in the chemical industry, such as dyes, solvents, varnishes, etc. Although resulting from biogenic and geological processes, petroleum hydrocarbons become severe pollutants when dispersed in the environment. Polycyclic aromatic hydrocarbons (PAHs) are benzene rings fused pollutants widely present in nature and with carcinogenic activity, while aliphatic hydrocarbons are related to affectations of the nervous system. The way in which fungi degrade hydrocarbons intra- and extra-cellularly is through enzymes that oxidize them, to form water and nontoxic or less toxic residues (Conejo-Saucedo et al. 2019; Daccò et al. 2020a; Li et al. 2020).

Aromatic amines (AAs), and their derivative compounds, are organic pollutants from very diverse industries specialized in the production of dyes, refined oils, cosmetics, agrochemicals, adhesives, medicine, etc. Due to their origin, they are widely present in the environment, posing a serious danger, as they are carcinogenic compounds. This group of chemicals also includes several groups of pesticides, due to their chemical structure. The main way by which fungi are able to eliminate them from the environment is based on their N-acetylation by enzymes N-acetyltransferases (de Lima et al. 2018). However, yeasts capable of supporting their toxicity and reducing radioactivity have already been used, through the release of carboxylic acids and the formation of biofilms (Tkavc et al. 2018).

3 Trichoderma and Bioremediation

The genus Trichoderma includes a group of fungal species widely distributed throughout the world due to their rapid growth, their ability to use different substrates and to tolerate the presence of different contaminants (Sharma et al. 2019; Hu et al. 2020). Its main current economic interest is based on its use as a biocontrol agent in agriculture and as a producer of enzymes in different industries (Jangir et al. 2017), although in recent years its relevance in other sectors has been increasing, as a promoter of plant growth and tolerance to abiotic stresses (Poveda et al. 2019a; Poveda 2020), source of genes for use in biotechnology (Poveda et al. 2019b), or mycoremediator.

In its interaction with the plant, Trichoderma behaves as a root endophyte , colonizing only the outermost layers of the root, due to a plant defense response mediated by salicylic acid, which prevents the fungus from reaching the vascular bundles and behaving like a systemic pathogen (Alonso-Ramírez et al. 2014; Poveda et al. 2020a). In this way, Trichoderma is also capable of activating systemic plant defenses against the attack of pests and/or pathogens (Poveda et al. 2020b) and acts as a biofertilizer (Zhang et al. 2018a).

One of the characteristics that make Trichoderma a good alternative for its use in agriculture is its resistance to various fungicides, which allows its inclusion of integrated crop protection management programs. Some of the fungicides to which Trichoderma is resistant are azoxystrobin, metalaxyl, carbendazim, chlorothalonil, copper oxy chloride, mancozeb, boscalid, cyazofamid, myclobutanil, pentachloronitrobenzene, propamocarb, or trifloxystrobin, among others (Shashikumar et al. 2019; Widmer et al. 2019). Similarly, Trichoderma is able to tolerate the presence of many different contaminants, which, together with its ability to eliminate them or reduce their toxicity, make it an effective mycoremediator agent.

How generally Trichoderma strains are selected to be used for mycoremediation is based on isolation from contaminated environments, where it is certain that he is able to survive (Tripathi et al. 2013). This is because Trichoderma is capable of obtaining resources from a wide variety of different substrates, as well as surviving extreme conditions, which makes it a better alternative than many other microorganisms used in bioremediation (Solanki et al. 2019).

Following, the different studies carried out in the mycoremediation of pesticides, heavy metals, and other pollutants by using different strains of Trichoderma (which have been compiled in Table 1) will be explained. This process of bioremediation by Trichoderma is carried out by different mechanisms, depending on the chemical nature of the specific pollutant, including, mainly, biosorption/bioaccumulation, biovolatilization by enzymatic conversation , and phytobial remediation, or microbe-assisted phytoremediation (Tripathi et al. 2013).

Table 1 Trichoderma as a mycoremediation agent for pesticides, heavy metals, and other pollutants, indicating the study carried out and its mechanism of action
Full size table

4 Trichoderma and Pesticides

First studies that determine the ability of Trichoderma to degrade different pesticides began in the 1990s (Katayama and Matsumura 1993), but it is in the last 20 years when the mechanisms involved and the wide diversity of pesticides on which it is capable of act.

Fungicides currently represent the only effective control strategy for various plant diseases. Its massive, repeated, and uncontrolled use leads to its excessive accumulation in soils, with very negative effects on the environment (Baćmaga et al. 2019). Both in vitro and in field, the ability of Trichoderma to degrade this group of compounds by up to 85% in 5 days has been reported (Sharma et al. 2016; Podbielska et al. 2020). This is a consequence of the action of the cytochrome P450 enzyme, implicated in the degradation of the fungicide climbazole (Manasfi et al. 2020).

With regard to insecticides, T. atroviride is capable of degrading in vitro up to 96% of compounds such as the organophosphate insecticide dichlorvos or the neonicotinoid insecticide imidacloprid (Tang et al. 2009; He et al. 2014). Dichlorvos (O, O-dimethyl-2,2-dichlorovinyl phosphate) is an insecticide that causes serious damage to aquatic ecosystems due to its water solubility, being efficiently degraded by the enzymes hygromycin B phosphotransferase and a paraoxonase-like enzyme of T. atroviride (Tang et al. 2009; Sun et al. 2019). On the other hand, the capacity of T. asperellum to favor a degradation of up to 75% in 5 days of the organophosphate insecticide phoxim has been described, by favoring an increase in glutathione S-transferase, peroxidase , and polyphenol peroxidase activity in tomato roots (Chen et al. 2020).

Herbicides are a group of pesticides widely used on all crops. Its presence in soils and waters causes serious environmental damages, mainly against the microorganisms present and when entering the food chain (Singh and Singh 2016). Glyphosate has been the most widely used herbicide in the last 30 years, as a consequence of the development of specifically resistant transgenic crops. Its toxicity is described as particularly harmful to animals as it occurs in the food chain, although its carcinogenic capacity has not been fully demonstrated (Xu et al. 2019). In this sense, T. viride and T. inhamatum have been described with the ability to degrade glyphosate, both in vitro and in the field, up to 70%, due to its use as a phosphorus resource and the action of urease enzymes (Arfarita et al. 2013, 2016; Kunanbayev et al. 2019). Alachlor herbicide has also been described as possibly carcinogenic, but it is certainly an endocrine-disrupting compound. Its total degradation in 7 days has been reported by various species of Trichoderma through its dechlorination and hydroxylation, intervening cytochrome P450 and laccase enzymes; as it happens with metolachlor , another chloroacetanilide herbicide (Nykiel-Szymańska et al. 2018, 2020).

Finally, there is a group of pesticides that can be used against a wide variety of pathogens and pests, the so-called broad spectrum. Pentachlorophenol has been used as a general biocide for many different purposes, becoming very harmful to the environment and health, by forming an important reservoir source of dioxins and furans (Verbrugge et al. 2018). T. harzianum has been reported as a potent mycoremediation agent for this pesticide through the methylation of phenolic compounds, degrading it to 100% in 7 days, in vitro and in soil (Rigot and Matsumura 2002; Vacondio et al. 2015). Moreover, the bioremedial capacity of Trichoderma can be used to obtain compounds of interest in different industries. Through the dehalogenation of the broad spectrum pesticide 3-chloropropionic acid, Trichoderma is capable of forming propionic acid, an additive widely used in animal feed and in the manufacture of biodegradable polymers (Edbeib 2020).

5 Trichoderma and Heavy Metals

As in the case of pesticides, the first studies that demonstrated the ability of Trichoderma to eliminate heavy metals from the environment date from the 1990s (Krantz-Rülcker et al. 1996). The main mechanism used by Trichoderma to heavy metals mycoremediation is its biosorption.

Cadmium (Cd) is a non-essential trace metal , very toxic for the environment and health. In humans, Cd can cause lung cancer in long-term exposure or kidney and bone damages in high exposure (Liu et al. 2017). Through the biosorption of Cd, Trichoderma species, such as T. asperellum or T. harzianum , are capable of reducing its presence in vitro by up to 90% in 21 days (Mohsenzadeh and Shahrokhi 2014; Hoseinzadeh et al. 2017; Maurya et al. 2019). As a consequence, Trichoderma is capable of increasing the tolerance in Cd-contaminated soils of crack willow (Salix fragilis) (Adams et al. 2007), spinach (Herliana et al. 2018), or Arabidopsis thaliana (Zhang et al. 2018b), also increasing Cd phytoaccumulation in oilseed rapes (Brassica napus and B. juncea) (Cao et al. 2008; Wang et al. 2009).

Lead (Pb) is a toxic metal from waste batteries and paint, mining and smelting activities, and combustion of fossil fuels. It is a very harmful element for health, since it is a powerful neurotoxic that can lead to death (Arnemo et al. 2016). Several species of Trichoderma have been reported with the ability to reduce the amount of Pb in vitro above 95% in 21 days due to its biosorption (Siddiquee et al. 2013; Tansengco et al. 2018; Maurya et al. 2019), in which the functional groups of its polysaccharides, with a high affinity for metal ions, are involved (Sun et al. 2020). Through this mechanism, it has been described how earthworms are capable of eliminating the Pb present in the soil, by having T. brevicompactum in their intestine (Zhang et al. 2020). Another mechanism reported in Trichoderma has been the formation of metal carbonates by different enzymatic activities (such as phosphatase , dehydrogenase, cellulase , urease, amylase , and invertase), removing 70% of Pb in contaminated soils (Govarthanan et al. 2018, 2019). In this way, T. harzianum and T. asperellum are capable of improving the tolerance of S. fragilis, A. thaliana , and Suaeda salsa in soils contaminated with Pb, reducing oxidative stress in the plant (Adams et al. 2007; Zhang et al. 2018b; Li et al. 2019).

Copper (Cu) is an essential element for plants as it is involved in numerous physiological processes. However, high levels of Cu are very harmful for plant growth, being also toxic for animals (Rehman et al. 2019). In vitro, Trichoderma is able to remove the Cu present up to 85% in 120 h (Yazdani et al. 2009; Tansengco et al. 2018; Kumar and Dwivedi 2021), also observed in T. brevicompactum in intestinal earthworms (Zhang et al. 2020), although in soil its capacity is reduced to 20% removal (Pehlivan et al. 2020). By means of biosorption of Cu mediums, the dead biomass of T. koningiopsis has been used in the production of Cu nanoparticles (Salvadori et al. 2014). Moreover, Trichoderma is capable of increasing plant tolerance in soils contaminated with high amounts of Cu and increasing its phytoaccumulation (Kacprzak et al. 2014; Vargas et al. 2017).

Chromium (Cr) is a very useful metal to many industries. In nature, it is found as Cr(III), without being harmful, but when oxidized to its Cr(VI) form due to anthropogenic activity, it presents high toxicity. The main damage to the environment and health of Cr(VI) is due to its corrosive nature, causing serious injuries when in contact with internal epithelia (ingestion or inhalation) or external (Coetzee et al. 2020). In Cr(VI) bioremediation by Trichoderma , a reduction to Cr(III) is necessary followed by a biosorption (Ray and Sur 2016; Saranya et al. 2020). In this sense , Trichoderma is capable of eliminating almost 100% of Cr(IV) in vitro (Vankar and Bajpai 2008; Shukla and Vankar 2014) and 30% in soil (Pehlivan et al. 2020).

Nickel (Ni) is a heavy metal considered an essential microelement for many plant physiological processes involved in its correct growth and development. However, excessive amounts of Ni in soils or waters cause serious toxicity symptoms in plants, such as chlorosis and growth inhibition, since their photosynthetic, respiratory, and water and nutrient transport activity are reduced. Ni environmental pollution is mainly a consequence of the metallurgical and electroplating industries. In animals, Ni easily accumulates in tissues, causing serious embryo-toxic, teratogenic, and carcinogenic damages (Shahzad et al. 2018). The ability of several Trichoderma species to bioaccumulate Ni by biosorption has been reported , reducing its presence in the soil by up to 78% (Hoseinzadeh et al. 2017; Tansengco et al. 2018). Furthermore, in interaction with plants, T. atroviride and T. asperellum , as examples, are capable of increasing the tolerance and phytoaccumulation of B. juncea and cacao, respectively, in Ni-contaminated soils (Cao et al. 2008; Rosmana et al. 2019).

Zinc (Zn) is an essential element for many biological processes in all organisms, such as protein synthesis or cell division. Its main toxicity problem due to excessive pollution of the environment has been observed in aquatic ecosystems, where it can be very harmful to life (Andarani et al. 2020). Although T. harzianum , T. atroviride , and T. virens are capable of eliminating the compound by biosorption, their capacity is very low, with removal percentages of 50% in vitro (Yazdani et al. 2010; Siddiquee et al. 2013; Tansengco et al. 2018) and 10% in soil (Pehlivan et al. 2020).

Arsenic (As) is the most widely distributed metalloid on the planet. The contamination of aquifers by As is the main sequence of natural geochemical mechanisms, but there are also minor anthropogenic sources, such as agrochemicals. Being present in aquifers, it quickly enters the food chain, causing serious damage to the vascular, nervous, and skin systems, as well as cancer (Alka et al. 2020). The removal of As by Trichoderma is performed through its reduction and methylation before its biosorption, transforming it into the nontoxic forms As(V) and As(III) (Su et al. 2011; Su et al. 2017), thus such as the formation of metal carbonates by the action of urease enzymes (Govarthanan et al. 2019). In this way, up to 70% of As is eliminated in vitro (Govarthanan et al. 2018) and percentages close to 10% in soil (Pehlivan et al. 2020). Due to this, the tolerance of water spinach (Ipomoea aquatic) and chickpea is increased in soils contaminated with As by Trichoderma application (Su et al. 2017; Tripathi et al. 2017).

6 Trichoderma and Other Pollutants

In relation to pesticides and heavy metals, Trichoderma has also been reported as an efficient mycoremediation agent against a great variety of pollutants of very varied origin, through mechanisms of action such as those already described.

The main group of hydrocarbons polluting the environment are the polycyclic aromatic hydrocarbons (PAHs), whose adverse effects have already been described. The ability of Trichoderma to eliminate the toxicity of PAHs in different soils has been widely reported, due to its use as a carbon resource (Daccò et al. 2020b) by the action of various enzymes (dehydrogenase, catechol 1,2 dioxygenase, laccase , and peroxidase ) (Yao et al. 2015; Zafra et al. 2015). In this way, it has been possible to eliminate up to 75% of the phenanthrene (Cobas et al. 2013; Zafra et al. 2015), 80% of the pyrene (Zafra et al. 2015; Al Farraj et al. 2020) and benzo[a]pyrene (Yao et al. 2015; Zafra et al. 2015), or 50% of naphthalene (Miles et al. 2020). In the same way, Trichoderma is capable of eliminating diesel present as a pollutant in different soils. In vitro, T. reesei eliminates up to 95% of the diesel in 40 days (Nazifa et al. 2018), while in soil the percentage is reduced to 70% by T. harzianum (Elshafie et al. 2020). Diesel degradation occurs through dehydrogenase and phenoloxidase enzymes (Mishra and Nautiyal 2009; Andreolli et al. 2016).

The main source of contamination by dyes comes from the widely distributed worldwide coloring industry, specifically from its wastewaters. The dyes present a great potential of damage to the environment, due to their mutagenic and carcinogenic capacity, and their direct damage to kidney, liver, brain, reproductive system, and central nervous system (Kaykhaii et al. 2018). The main mechanism of action of Trichoderma in the mycoremediation of dyes is through its enzymatic degradation. In vitro, T. asperellum and T. harzianum are capable of degrading by the action of laccase enzymes up to 98% of methylene blue (Ranimol et al. 2018) and malachite green (Shanmugam et al. 2017b; Ranimol et al. 2018), 96% of Congo red (Ranimol et al. 2018), or 60% of crystal violet (Shanmugam et al. 2017a; Ranimol et al. 2018). Although in the degradation of up to 88% of creson red in 30 days by T. harzianum , the activity of the enzymes manganese peroxidase, lignin peroxidase, and 1,2- and 2,3-dioxygenase has also been reported (Nor et al. 2015).

There are many other pollutants against which Trichoderma ’s ability as a mycoremediation agent has been reported, which are listed in Table 1. Some of them include the degradation of detergents by invertase and protease enzymes from T. harzianum (Jakovljević et al. 2015), phenolic compounds or plastics by laccase enzymes (Balcázar-López et al. 2016; Lawrance et al. 2019), cyanide by cyanide hydratase and rhodanese enzymes (Ezzi and Lynch 2002; Zhou et al. 2007), and even 2,4,6-trinitrotoluene (TNT ) (Alothman et al. 2020).

7 Conclusions

Soils and waters around the world present, to a greater or lesser extent, some pollutant that is seriously harmful to the environment and health. Due to their presence in soils and waters and their toxicity, pesticides and heavy metals represent the main pollutants in the agricultural system. In this sense, bioremediation is an effective strategy for the elimination of these contaminants, highlighting the role played by fungal enzymes in mycoremediation, which allows the degradation and/or conjugation of these harmful elements.

The use of fungi in the bioremediation of pollutants in soils and waters presents a series of limitations and drawbacks. The process can be very slow and incomplete, since the fungi need a period of adaptation to the new environment once they are inoculated, and have access to the contaminant of interest. Moreover, the transformation of pollutants to more toxic forms by fungal action can occur. However, mycoremediation is an innovative, cost-effective, and ecologically beneficial technology in removing contaminants such as pesticides and heavy metals.

Due to their ability to survive in highly polluted extreme environments and the extensive enzymatic library they possess, there are numerous species of the genus Trichoderma capable of effectively bioremediating a wide range of different contaminants. Thanks to its enzymatic activity, Trichoderma is capable of degrading in percentages close to 100% such polluting pesticides as glyphosate or pentachlorophenol. In addition, its mycoremediation capacity can have derived benefits, as is the case with the broad spectrum pesticide 3-chloropropionic acid, transformed by Trichoderma into propionic acid.

As far as heavy metals are concerned, in vitro it has been proven that Trichoderma is capable of effectively eliminating almost all of the contaminant by biosorption, although in its application on soils the elimination percentages are even reduced to one-tenth. Despite the wide variety of heavy metals that Trichoderma is capable of bioaccumulating, its low efficiency in natural environments represents a difficulty for its widespread use.

Furthermore, various species of Trichoderma have been described with the ability to remove many other pollutants from soils and waters, thanks to mechanisms similar to those used against pesticides and heavy metals. These include hydrocarbons, dyes, detergents, phenolic compounds, or cyanide. Therefore, Trichoderma is a powerful mycoremediation agent for the main current environmental pollutants, although even more studies are necessary on its application in natural environments, in order to obtain efficient elimination processes.