Professional Documents
Culture Documents
Singh 2020
Singh 2020
9
Fungi as potential candidates for
bioremediation
Rajesh Kumar Singh1, Ruchita Tripathi1, Amit Ranjan2,
Akhileshwar Kumar Srivastava3
1
Department of Dravyaguna, Institute of Medical Sciences, Banaras Hindu University,
Varanasi, India; 2Department of Kayachikitsa Institute of Medical Sciences, Banaras Hindu
University, Varanasi, India; 3The National Institute for Biotechnology in the Negev,
Ben-Gurion University of the Negev, Beer-Sheva, Israel
1. Introduction
The condition of environment directly influences the quality of life in the ecosystem on
earth. Human beings are most dominant animal on the earth, have developed the science
and technology for their comforts, and industrialized at large scale for the fulfillment of their
requirements, but unfortunately these produce adverse affect on environment, often resulting
to the extinction of several species of the earth. The civilization and industrialization produce
large amount of organic and inorganic pollutants, as well as nuclear wastes, which are
generally flushed into the river or dumped into the soil. The flushing and dumping of
such materials pollute to system, creating a serious problem for the survival of organisms.
Such pollutants are disposed by making a hole into land and filling it by waste material or
just filling the low-land areas just away from the cities, but continuous increases of the
pollutants need new place in near future, which develops other issues such as lack of water-
bodies, floods, etc. These methods of disposal are difficult to sustain because of limited space
and are also not economic and healthy (Karigar and Rao, 2011). Hence, bioremediation is
alternative, economical, and acceptable method to dispose these polluting materials.
Bioremediation is a process in which the waste and hazardous materials are transformed
into nonhazardous or less-hazardous substances by microbes such as bacteria, fungi, algae,
etc. The applications of fungal microbes in bioremediation have been well-known as fungal
bioremediation or mycoremediation. The fungi decompose the biomass residues and
chemical pollutants by producing several enzymes such as amylase, protease, lipase, nuclease,
etc., which degrade the cell walls, proteins, lipids, DNA, and other organic materials. These
microbes are used for biotransformation of organic waste materials and removal of pollutants
from environment (Balabanova et al., 2018). Fungi are capable to degrade the organic
chemicals, metals, metalloids, and radionuclides, by secreting enzymes and other chemicals
through chemical modification and/or influencing chemical bioavailability. It has also adopted
to survive in diverse condition continuously. Fungi are competent for metabolize various
environmental chemicals and utilize its product for survival without any additional need of
nutrition. It degrades pollutants through several extracellular oxidoreductases for decompos-
ing the lignocelluloses along with several pollutants. Fungi metabolize and immobilize the
metals, metalloids, and radionuclides in the mycosphere, store in various parts of the cell, or
translocate through fungal hyphae. It also degrades the compounds that are not intoxicated
by bacteria efficiently such as dioxins and 2,4,6-trinitrotoluene, drugs, etc. These features enable
fungi as potential candidate for removing organic or metal contaminants in the soils, water,
and air and can be used for bioremediation with cost-effective and nature friendly ways
(Harms et al., 2011). This chapter explains the diverse role of fungi group in overcoming the
pollutant toxicity through a robust technique bioremediation as summarized in Fig. 9.1.
FIGURE 9.1 Describing role of fungi in bioremediation and involvement of fungal enzymes in removal/
transformation of materials.
1. Introduction 179
polycyclic aromatic hydrocarbons (PAHs), nitroaromatic compounds, pesticides, synthetic
dyes, polychlorinated dibenzo-p-dioxins, and synthetic polymers simultaneously even in
mixture of all (Kues, 2015). The major groups of enzymes involved in the degradation of wastes
materials and pollutants include extracellular oxidoreductases, cell-bound enzymes, and other
transferase enzymes.
1.3 Transferases
Transferases include mainly aromatic nitroreductases, quinone reductases, etc., which
transfer the functional groups and convert the hazardous pollutants into nonhazardous
products. The transferase enzymes degrade the pollutants containing hydroxyl groups by
converting it into the conjugates. The conjugates are stored, fixed, or secreted into environment
in inactive conjugated forms (Morel et al., 2013). The different enzymes and components are
involved in remediation of contaminated materials as mentioned in Table 9.1.
TABLE 9.1 The details of enzymes producing fungal taxa and mechanism of action.
180
S.No. Enzymes Fungal taxa Enzyme occurrence Mechanism of action References
1 Laccases Ascomycota and Extracellular O2-dependent one-electron oxidation of (Baldrian, n.d.; Majeau
Basidiomycota organic compounds. et al., 2010)
2 Tyrosinases Ascomycota, Intracellular (but O2-dependent hydroxylation of monophenols (Halaouli et al., n.d.;
Basidiomycota, and sometimes to o-diphenols (cresolase activity) Ullrich and Hofrichter,
Mucoromycotina extracellular) Oxidation of o-diphenols to catechols 2007)
(catecholase activity).
1. Introduction
12 Nitroreductases Ascomycota, Cell bound NADPH-dependent reduction of (Bhushan et al., 2002;
Basidiomycota, and nitroaromatics to hydroxylamino and Crocker et al., 2006;
Mucoromycotina amino(nitro) compounds and of nitro Esteve-Núñez et al., 2001;
functional groups of N-containing Fournier et al., 2004;
heterocycles. Scheibner et al., 1997)
13 Reductive Basidiomycota and Cell bound Two-component system comprising a (Jensen et al., 2001;
dehalogenases perhaps membrane-bound glutathione S-transferase Nakamiya et al., 2005)
Ascomycota that produces glutathionyl conjugates with
concomitant chlorine removal and a soluble
glutathione conjugate reductase that releases
reductively dechlorinated compounds.
14 Miscellaneous Ascomycota, Cell bound Formation of glucoside, glucuronide, xyloside, Kasai et al. (2010)
transferases Basidiomycota, and sulfate, or methyl conjugates from
Mucoromycotina hydroxylated compounds.
181
182 9. Fungi as potential candidates for bioremediation
2. Fungal bioremediation
2.1 Toxic recalcitrant compound
The poor electron donor compounds such as polychlorinated dibenzo-p-dioxins (PCDDs)
and polychlorinated dibenzofurans (PCDFs) occurring at very low concentration are oxidized
to the electronegativity of the chlorine atoms by accepting the electrons from the aromatic
rings (Hammel, 1995). The compounds with more than one chlorine atom are not employed
as a source of carbon and energy by bacteria. Therefore, the biotransformation of the toxic
compounds, PCDD 2,3,7,8-tetrachlorodibenzo-p-dioxin (2,3,7,8-TCDD), through aerobic
and anaerobic bacteria is slow process ranging to months; however, it is not completely
biotransformed and finally halted at the stage of less chlorinated aromatic products. Compar-
atively, the white-rot fungus Phanerochaete sordid converts the compound 2,3,7,8-TCDD into
chlorocatechols within 10 days and other fungus of same species P. chrysosporium mineralizes
the intermediate products. The fungus P. sordida has no specific to particular compound and
it transforms compounds containing different chlorine atoms, namely PCDDs (6e8 chlorines)
and PCDFs (4e8 chlorines) (Lipnick et al., 2000). The ascomycete Cordyceps sinensis has great
potential to remove the highly chlorinated dioxins at fast rate similar to white-rot fungi. The
2,4,6-trinitrotoluene (TNT) is also highly oxidized to the electronegativity of its nitro groups.
The transformation of TNT is accomplished mostly through aerobic bacteria into
monoamino-dinitrotoluenes, diamino-nitrotoluenes, and hydroxylamino-dinitrotoluenes that
acquire to produce mutagenic azoxy-tetranitrotoluenes, although the transformation of TNT
through anaerobic bacteria mostly halts at the stage of triaminotoluene, whereas white-rot
and litter-decaying basidiomycetes mineralize TNT rapidly (Esteve-Núñez et al., 2001).
Researches into use of nonspecific enzymes through biotechnological approaches must eluci-
date the problems generated during the reactions. The specific fungal transformation products
of PAHs have less concentration of mutagenic and carcinogenic metabolites in which most
transformed products are lower toxic than its parent compounds. The formations of PCDDs
and PCDFs on enzymatic oxidative coupling of chlorophenols are required to assess the
structure, biological activity, stability, and environmental behavior (Lamar et al., 2003). The
laccase-catalyzed transformation of 1-ethyl-3-(3-dimethylaminopropyl) carbodiimide hydro-
chloride (EDCs) to oligomeric coupling products reduces the endocrine-disrupting activity of
such compounds. Similarly, the toxicity is reduced by laccases and other phenoloxidases for
covalently linked chlorophenols, other phenols, and TNT metabolites to components of soil
humic substances.
PAHs as good substrates in respect to energetic perspective and its low molecular mass
PAHs are commonly used by bacteria. The bioavailability decreases inverse to molecular
mass, only a few bacteria grow at high molecular mass PAHs with five or more aromatic
rings. The fungal species of Ascomycota, Basidiomycota, and Mucoromycotina having a
nonspecific mechanism to detoxify the compounds hydroxylate to PAHs intracellularly
and then transfer to water-soluble compounds that could be excreted out. In addition,
different fungi utilize the extracellular oxidoreductases in PAH degradation and mineralize
to high molecular mass PAHs, such as highly carcinogenic benzo[a]pyrene and others
(Mao and Guan, 2016).
2. Fungal bioremediation 183
wood-rotting fungi Antrodia xanthan and Fomitopsis palustris (Deshmukh et al., 2016;
Voberkova et al., 2017). Trichoderma viride is one of the promising fungi for conversion of
organic municipal solid waste to harmless substances. The main factors such as pH and
temperature are good indicator for the end of the bioconversion of municipal solid waste
(Gautam et al., 2012).
3. Fungi in bioremediation
Fungi could survive in different habitats that colonize in soil matrix along with freshwater
and also in marine habitats. Fungi also grow in different climatic conditions including the
stress condition and inseminate the spores through air that aid in balancing of ecosystem.
It has been reported that the fungi can also survive in effluent treatment plants (ETPs) during
treatment of wastewaters. The surviving ability in diverse habitats and potential for produc-
ing the diverse enzymes indicates fungi as potential candidates for bioremediation.
4. Technology advancement
Bioremediation of toxic substances is one of reliable methods for cleanup of polluted sites
and fungi play important role in remediation of hazardous substances containing different
constituents in ecosystem with multiple modes for overcoming the problems of contamina-
tion. Nonetheless, their implications are mainly associated with environmental factors and
long lag phase, sludge generation, and difficult methods, which may have direct impact
on application of fungal biomass in bioremediation. Many advance technologies have been
developed in field of fungal bioremediation to reduce the associated problems. One such
advance processes associated with enzymes of the fungal biomass reduces bioremediation
time, no lag phase, minimal sludge generation, and easy process control. Though enzymes
create itself other problems of high cost and less shelf life due to lower stability, although
enzymes production in whole cell and its immobilization have been enhanced their stability
by increasing shelf life and achieved for reusing the enzyme with affordable costs. To date,
the various bioreactors; fluidized beds and rotating biological contactors have been developed
for remediating of contaminants with fungi (Gautam et al., 2012). However, novel bioreactor
systems are being constructed for elimination of dyes, e.g., Reactive Green 19 by white-rot
fungi (Sari et al., 2016). A two-stage reactor have been succeed in remediation of azo dye
Reactive Blue 222 along with Photo-Fenton’s and aerobic treatment through two white-rot
fungi P. ostreatus IBL-02 and P. chrysosporium IBL-03 (Kiran et al., 2013). A white-rot fungus,
T. versicolor, revealed potential removal of TrOCs through fungal membrane bioreactor in
non-sterile condition at 2 days hydraulic retention time (HRT) (Yang et al., 2013). Bhattacharya
et al. have developed a novel approach for degradation of HMW-PAHs using white-rot fungus
P. chrysosporium. The remediation of benzo[a]pyrene under ligninolytic culture medium in-
creases the PAH oxidizing monooxygeneses with formation of P450-hydroxylated metabolite
that is eliminated through non-ligninolytic phase (Bhattacharya et al., 2014). The other
significant strategy associated with biopurification systems in stimulating bioremediation of
pesticides having wastewaters through highly active biological mixture of particular white-
rot fungi has been explained by Rodrı’guez-Rodrıguez et al. (Rodríguez-Rodríguez et al.,
n.d.). The sustainability and eco-friendly nature of bioremediation has been displayed for
the remediation of sewage sludge containing filamentous inoculum in a large-scale bioreactor
by implying a continuous process (Rahman et al., 2014). In spite of the fungi alone, its
co-cultures with bacteria playing as a synergistic degradation system containing Fusarium
sp. PY3, Bacillus sp. PY1, and Sphingomonas sp. PY2 remove pyrene by 96.0% and volatilized
arsenic by 84.1% (Liu et al., 2013). Other significant and innovative approach for remediation
of PAHs have been initiated by Cobas et al. (2013) in which 90% phenanthrene has been
removed within 14 days by formation of permeable novel reactive biobarriers of Trichoderma
longibrachiatum on nylon sponge. Fungal biocatalysis is employed in all cell systems associated
with textile wastewater treatment (Spina et al., 2015).
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