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Introduction
Xenobiotics are toxic chemicals that are exotic to living
organisms and have an anity to persist in the biosphere
(Sinha et al. 2009). ese compounds have synthetic
chemical composition, and species have not adapted to
these in evolution (Gren 2012). e residues of xenobiotic
substances persist in the ecosystem over a long period and
have negative eects on the microora and the fertility of
the soil (Gianfreda, Rao 2008). erefore, polluting the
environment with recalcitrant chemicals, which oen
are xenobiotics, is one of the major environmental issues
with global focus and recognition (Tišma et al. 2010).
e pollution created by xenobiotics disrupts natural
ecosystems, causes changes in climatic conditions, reduces
water levels and has other negative impacts (Gursahani,
Gupta 2011). e main sources of xenobiotics enter into the
environment from pharmaceutical industries (ibuprofen,
paracetamol), agriculture (pesticides, herbicides,
insecticides), the paper industry (paper and pulp euent),
food industry (food additives such as vinegar, lecithin),
plastic industry (polyvinyl chloride), consumer industry
(coatings, dyes) and petroleum industries (benzene, xylene)
(Mishra et al. 2019). Humans are exposed to xenobiotics
through inhalation, adsorption by skin (cosmetic
products) or ingestion (medicines, vegetables, fruits).
ey can cause severe health hazards such as heart defects,
neurodegeneration, defects in the central nervous system
and adverse reproductive problems. Hence, xenobiotic
degradation in the environment is essential (Phale et al.
2019).
Physico-chemical approaches involved in the
control of organic pollutants include ion exchange,
chemical occulation, adsorption, irradiation, oxidation,
precipitation and ozonation (Aksu 2005). e physico-
chemical approaches are very costly and oen yield adverse
intermediate metabolites that are harmful and need further
secondary treatment. To overcome these, several other
environmentally friendly processes have been described,
such as bioremediation, phytoremediation, etc. (Varsha
et al. 2011). Bioremediation is a technology in which
biological organisms (algae, bacteria, fungi and plants) are
employed to minimize the accumulation and harmfulness
of environmental contaminants (Gnanasalomi et al. 2013).
Xenobiotic microbial depletion is an eective strategy
for eliminating toxic pollutants from the environment.
Environmental and Experimental Biology (2021) 19: 103–119 Review
http://doi.org/10.22364/eeb.19.11
White-rot fungi-mediated bioremediation
as a sustainable method for xenobiotic
degradation
A. Kathiravan, J. Joel Gnanadoss*
Microbial and Environmental Biotechnology Research Unit, Department of Plant Biology and
Biotechnology, Loyola College, Chennai-600034, Tamil Nadu, India
*Corresponding author, E-mail: joelgna@gmail.com
ISSN 2255-9582
Abstract
Xenobiotics are hazardous compounds that are foreign to natural ecosystems. e production and use of xenobiotic compounds
continue to increase worldwide, which in turn causes environmental pollution and has adverse eects on humans. Degradation of
such compounds, therefore, needs urgent awareness and attention. e physicochemical approaches to treat the contaminants are
expensive. Bioremediation is a concept that exploits organisms to manage the environment with less manpower and time. White-rot
fungi-mediated bioremediation oers inexpensive, environmentally sustainable and potential degradation mechanisms for dierent
recalcitrant chemicals. White-rot fungi secrete lignolytic enzymes that have extensive substrate specicities and are involved in the
transformation and solubilization of lignin-like structural contaminants. e main lignolytic enzymes occurring in white-rot fungi are
laccases, lignin peroxidase, manganese peroxidase, and other peroxidases. Such lignolytic enzymes permit white-rot fungi to endure
high toxic levels. is review describes the opportunities to use white-rot fungi and their enzyme systems in the biodegradation of
multiple xenobiotic contaminants.
Key words: biodegradation, lignolytic enzymes, mycoremediation, white-rot fungi, xenobiotics.
Abbreviations: BTEX, benzene, toluene, ethylbenzene and xylene; DyP, dye-decolourizing peroxidase; LiP, lignin peroxidase; MnP,
manganese peroxidase; PAHs, polyaromatic hydrocarbons; PCBs, polychlorinated biphenyls; PCPs, pentachlorophenols; TNT,
2,4,6-trinitrotoluene; YMG, yeast-malt-glucose
104
e ability of microorganisms to break down xenobiotic
substances is considered an important means of removing
toxic materials (Sridevi et al. 2011). Some fungi are resilient
organisms compared to bacteria and are typically less
susceptible to high levels of pollutants. is is why fungi
were extensively studied regarding their bioremediation
capabilities in the mid-1980s (Ellouze, Sayadi 2016).
Fungi play a crucial role in all environments including
soil and marine habitats as decomposers and symbionts.
ey are especially suitable for bioremediation because
of their robust morphological structure and various
biochemical capabilities. Mycoremediation is a component
of bioremediation that employs fungus for intrinsic and
extrinsic management of polluted areas. Mycoremediation
is a cost-eective and environmentally reliable option
for removing, transporting and storing hazardous waste.
Mycelia may destroy these contaminants within the soil
before they move through food chains (Ramachandran,
Gnanadoss 2013). Further, attention has been given to the
distinct ability of fungi to remove these contaminants by
using a variety of extracellular and intracellular enzyme
systems for detoxication and bioremediation (Deshmukh
et al. 2016). e objective of this review paper is to
emphasize the signicant properties of white-rot fungi in
degrading dierent xenobiotic compounds like polymers,
polyaromatic hydrocarbons (PAHs), polychlorinated
biphenyls (PCBs), pentachlorophenols (PCPs),
antibiotics, 2,4,6-trinitrotoluene (TNT), benzene, toluene,
ethylbenzene and xylene (BTEX), pesticides and dyes.
White-rot fungi
White-rot fungi possess the remarkable ability to
biodegrade lignin and hence the name white-rot comes
from the white surface of timber invaded by white-
rot fungi, where the evacuation of lignin gives a faded
impression (Pointing 2001). Systematically, white-rot fungi
include specic basidiomycetes, and very few ascomycete
families like Xylariaceae are associated with white-rot decay
(Eaton, Hale 1993). e utilization of fungi for the cleaning
of contaminated soil was initially demonstrated during
the mid-1980s, when the white-rot fungus Phanerochaete
chrysosporium was found to degrade a high diversity of
natural contaminants (Bumpus, Aust 1987). is ability
was later exhibited for diverse species such as Trametes
versicolor and Pleurotus ostreatus (Ghani et al. 1996),
Lentinus subnudus (Adenipekun, Fasidi 2005), Psathyrella
candolleana LCJ 178 and Myrothecium gramineum
LCJ 177 (Gnanasalomi, Gnanadoss 2013), Porostereum
spadiceum (Tigini et al. 2013), Pleurotus floridanus LCJ155,
Leucocoprinus cretaceous LCJ164, and Agaricus sp. LCJ169
(Jebapriya, Gnanadoss 2014), Dentipellis sp. (Park et al.
2019), Ganoderma lucidium (Coelho-Moreira et al. 2018)
and Bjerkandera adusta (Dhiman et al. 2020). White-rot
fungi degrade all timber components, for example, cellulose,
hemicellulose and lignin, whereas other fungi destroy
lignin predominantly. e former is called a non-selective
white-rot degraders and the latter are known as specic
white-rot degraders. e specic white-rot degraders are
extremely intriguing from the biotechnology perspective as
they remove lignin leaving the lucrative cellulose unaltered
(Dashtban et al. 2010). Potential benets of using white-rot
fungi to remove ecological contaminants are due to their
ubiquitous existence, ability to break down assorted classes
of destructive foreign substances and to adjust the pH of
their characteristic substrate (Christian et al. 2005).
Enzyme systems in white-rot fungi
White-rot fungi usually produce one or multiple lignolytic
enzymes in various amounts, on the basis of which they
can be divided into four classes (Nerud, Misurcova
1996) namely: (a) laccase, manganese peroxidase (MnP)
and lignin peroxidase (LiP), (b) laccase and any of the
peroxidases, (c) laccases only, (d) peroxidases only. e
most widely recognized lignolytic enzymes present in
white-rot fungi incorporate laccases and MnP and the
least common are LiP and versatile peroxidase. ese
lignolytic enzymes can work together or independently,
yet additional enzymes like glyoxal oxidase, aryl alcohol
oxidase, cellobiose dehydrogenase, pyranose 2-oxidase,
and others are fundamental to accomplish the cycle of
lignocellulose or xenobiotic degradation. In addition, an
intracellular enzyme cytochrome P450 monooxygenase
and low molecular weight oxidants like hydroxyl radicals
and Mn3+ were demonstrated to be powerful in eliminating
lignocellulosic materials and various xenobiotics. Recently,
dye decolourising peroxidase (DyP), which is involved in
the decolouration of dyestus, and aromatic peroxygenases
has been found to be associated in catalysis of oxygen
transfer reactions that bring about the ester cleavage, is also
recognized as a lignolytic enzyme that corresponds with
white-rot fungi (Rodríguez-Couto, 2016).
Laccase
Laccase is a copper protein that has its position in blue
oxidases. Copper, which occurs at the dynamic site of
the enzyme, plays an integral role in catalytic reactions.
e catalytic center of the enzyme consists of four copper
atoms. Laccase catalyzes four single electron oxidations
of the substrate into four electron reductive bond
cleavages. Degradation of various aromatic mixtures
can be catalyzed by an associative reduction of oxygen
to water. Moreover, in the presence of key substrates
[2,20-azinobis-3-ethylbenzothiazoline-6-sulphonicacid
or 1-hydroxybenzotriazole] working as electron transfer
mediators, the substrate spectrum is further extended to
degrade non-phenolic mixtures (Kılıç et al. 2016). Laccase
was rst recognized in 1883 by Yoshida, when he separated
the exudates from Rhus vernicifera (urston 1994).
A. Kathiravan, J.J. Gnanadoss
105
ey are derived from natural sources and oen occur
in plants and microorganisms (Dwivedi et al. 2011) and
also in a few insects (Xu 1999). Fungal sources of laccase
have been isolated from dierent groups of fungi like
deuteromycetous, ascomycetous and basidiomycetous. Of
these, white-rot fungi and other litter degrading organisms
are the most prominent sources of the laccase enzyme. In
specic, laccase production by basidiomycetous taxa such as
Trametes, Pleurotus, Agaricus, Phanerochaete, Pycnoporus,
and Lentinus has been broadly explored as they are easy to
grow in in vitro (Rodríguez-Couto, 2019). White-rot fungal
species that synthesize laccase are Polyporus sanguineus,
Phlebia brevispora, Daedalea flavida and Phlebia radiata
(Arora, Gill 2001), Phanerochaete chrysosporium, Trametes
hirsuta, Marasmius sp. and Trametes versicolor (Risdianto et
al. 2012), Pleurotus florida, Pleurotus ostreatus and Pleurotus
sajor-caju (Radhika et al. 2013), Agaricus sp. LCJ262 (Jose,
Joel 2014), Trametes orientalis (Zheng et al. 2017), Cerrena
unicolor strain GSM-01 (Wang et al. 2017), and Myrothecium
gramineum LCJ 177 (Gnanasalomi, Gnanadoss 2019).
Laccases from white-rot fungi are associated with lignin
removal and are resilient at dierent pH and temperatures.
High purity of laccase can be obtained by suitable
optimizing parameters (Gnanasalomi, Gnanadoss 2013).
Laccase-mediator methods have enormous potential for
lignin removal, biosensor application, biofuel and organic
synthesis, bioremediation of some toxic chemical wastes,
pharmaceutical and nanobiotechnology applications
(Singh, Gupta 2020).
Lignin peroxidase
LiP is a heme enzyme from the oxidoreductase family, which
is primarily secreted by white-rot basidiomycetes during
the formation of secondary metabolites. LiP plays a key part
in removing the lignin portion of the plant cell wall. LiP
assists in the biodegradation of lignin and other phenolic
molecules with H2O2 as a substrate and veratryl alcohol
as a mediator (Singh et al. 2019). LiP has been reported in
various white-rot fungi like Coriolus versicolor f. antarcticus
(Levin et al. 2004), Phanerochaete chrysosporium (Wang
et al. 2008), Ganoderma lucidium (Sasidhara et al. 2014),
Pleurotus ostreatus, Pleurotus sapidus, Pleurotus florida
(Kunjadia et al. 2016), Porodaedalea pini (Tanabe et al.
2016), Podoscypha elegans (Agarwal et al. 2017), Coriolopsis
gallica, Pleurotus sajor-caju and Lentinula edodes (Ding et
al. 2019). LiP is exploited for numerous industrial uses and
bioremediation processes due to its immense substrate
specicity and high redox potential (Erden et al. 2009).
Manganese peroxidase
As LiP, MnP is also placed under the same family of
oxidoreductases described in Phanerochaete chrysoporium
as another lignolytic enzyme (Paszczyńskib et al. 1985).
MnP seems to more prevalent in white-rot fungi than
LiP (Hammel, Cullen 2008). In contrast to LiP, MnP has
a low redox potential and oxidizes the compounds with
H2O2 performing as oxidant and manganese performing
as a mediator in the MnP catalytic process. e function
of MnP is the conversion of Mn2+ ions to Mn3+. Mn3+ is
extremely reactive and chelates with biomolecules such as
oxalate and malate formed by the fungus (Shanmugapriya
et al. 2019). Chelated Mn3+ stimulates the degradation
of phenolic compounds to phenoxy radicals (Hofrichter
2002). A few examples of MnP from white-rot fungi are
Bjerkandera sp. (Mester, Field 1997), Irpex flavus, Polyporus
sanguineus and Dichomitus squalens (Gill, Arora 2003),
Physisporinus rivulosus (Hakala et al. 2005), Pleurotus
ostreatus, Coriolus versicolor and Phlebia tremellosa
(Robinson et al. 2011), Cerrena unicolor (Zhang et al. 2018)
and Pseudolagarobasidium sp. (amvithayakorn et al.
2019). MnP nds wide applications in the industries such
as food, textile, paper and pulp industries, pharmaceutical
and bioremediation (Singh et al. 2019).
Versatile peroxidase
Versatile peroxidase is a hybrid peroxidase that comprises
the catalytic activities of MnP and LiP (Dosoretz, Reddy
2007). Similar to MnP, it have a strong anity for Mn2+
and initiates the conversion of Mn2+ to Mn3+ and it also
metabolizes non-phenolic and phenolic molecules without
Mn2+ like LiP. is enzyme seems to be expressed mostly in
fungal genera such as Pleurotus, Bjerkandera, and Lepista
and may also be present in Panus and Trametes (Yadav,
Yadav 2015). Versatile peroxidase has distinctive characters
compared to other lignolytic peroxidases and is suitable
for utilization in various applications like the paper and
pulp industry, biofuel production, ruminant nutrition,
bioremediation, and the textile industry (Ravichandran,
Sridhar 2016).
Dye-decolourising peroxidase
DyP is a novel group of heme peroxidases that were
molecularly identied and are well-known in bacteria and
fungi. ey lack structural and sequence resemblances
with traditional ora and fauna peroxidases. As the name
species, DyP can use H2O2 to detoxify dierent groups
of azo and anthraquinone-based articial dyes, substrates
that are less susceptible to oxidation by members of
other classical heme peroxidases. Also, specic DyP were
described to oxidize compounds of the phenol lignin type,
thus providing the enzymatic ability for this category
of heme peroxidase to support the transformation of
lignocellulosic materials for downstream production of
biofuel (Chaplin et al. 2019). DyP was initially identied
from Bjerkandera adusta culture (formerly reported as
Geotrichum candidum) (Fernández-Fueyo et al. 2015).
DyP producing white-rot fungi include Termitomyces
albuminosus (Johjima et al. 2003), Pleurotus ostreatus
(Faraco et al. 2007), Marasmius scorodonius (Pühse et
al. 2009), Auricularia auricula-judae (Liers et al. 2010),
White-rot fungi mediated bioremediation for xenobiotic degradation
106
Exidia glandulosa, Mycena epipterygia (Liers et al. 2013),
Irpex lacteus (Salvachúa et al. 2013), Funalia trogii (Kolwek
et al. 2018), Trametes versicolor (Amara et al. 2018), and
Pleurotus sapidus (Krahe et al. 2020).
Cytochrome P450 monooxygenase
Cytochrome P450 monooxygenase is a main intracellular
enzyme that ts the class of oxygenases that helps in the
degradation of xenobiotics via oxygen. ey also have
heme-comprising enzymes that incorporate one or several
oxygen molecules to break down aromatic rings and even
stabilize the compound (Baker et al. 2019). e importance
of cytochrome P450 monooxygenase mechanisms in
detoxication of endogenous and exogenous molecules has
been shown (Ichinose et al. 2013). Increased removal of
PAHs was achieved by the initial application of cytochrome
P450 monooxygenase in degradation experiments.
Improved elimination of contaminants was obtained
through molecular methods for ecient and oversupply of
cytochrome P450 enzyme (Deshmukh et al. 2016).
Xenobiotic degradation process by white-rot fungi
e capability of white-rot fungal species in eliminating
xenobiotic compounds from ecosystems is dependent
on their ability to biodegrade lignin, as it is close to the
structure of dierent xenobiotics (Fig. 1). erefore, the
identical methodologies that provide white-rot fungi the
potential to degrade lignin are being used to remove a large
range of xenobiotic contaminants. Most of the xenobiotics
are oxidized and mineralized to various sizes using white-
rot fungi under the lignolytic conditions (Field et al. 1993).
e xenobiotic degradation process is shown in Fig. 2.
Fig . 1. Structure of lignin in comparison with the chemical
structure of diverse xenobiotic compounds.
Fig . 2. Schematic diagram representing the degradation mechanism of xenobiotic compounds using white-rot fungi.
A. Kathiravan, J.J. Gnanadoss
107
Applications of white-rot fungi in xenobiotic
degradation
Degradation of polymers using white-rot fungi
Plastic is typically a polymer that is composed of various
elements such as carbon, hydrogen, silicon, oxygen, chloride
and nitrogen (Seymour 1989). Linking the monomers
using chemical bonds forms plastic. Polythene contains
about 64% of plastic, a continuous hydrocarbon polymer
comprising elongated strands of ethylene monomers.
e overall equation for polyethylene is CnH2n, where n,
represents the total number of carbon molecules (Sangale et
al. 2012). e worldwide usage of plastic is rising rapidly at
a rate of 12% per year and approximately 0.15 billion units
of synthetic materials are developed globally every year
(Das, Kumar 2014). Every year, the ecosystem accumulates
25 million metric tons of polymer waste (Kaseem et al.
2012).
Biodegradation of many synthetic polymers with
dierent chemical compositions has been reported, but
several of them involved degradation using white-rot
fungi-mediated lignin enzymes (Pointing 2001). Nylon-6
polymer degradation initially using white-rot fungus
Bjerkandera adusta has been described (Friedrich et al.
2007). Synthetic materials including polyvinyl chloride,
nylon, acrylamide, etc. that are degraded by dierent
white-rot fungi have been documented (Kale et al. 2015).
Removal of biopolymers like lignin, hemicellulose and
cellulose is also possible by white-rot fungi. In comparison
to other groups of microorganisms, lignin removal through
white-rot fungi is more promising (Woiciechowski et al.
2013). Phellinus pini, Phanerochaete chrysosporium, Phlebia
sp., Pleurotus sp., Heterobasidion annosum, Ceriporiopsis
subvermispora, Irpex lacteus and Trametes veriscolor are
specic white-rot fungi that preferably invade lignin more
eectively than cellulose and hemicellulose. ey secrete
dierent classes of lignolytic enzymes that facilitate the
degradation of aromatic organic compounds, producing
aromatic radicals, and modify the structure of lignin-
and lignocellulose-derived products (Andlar et al. 2018).
Study on the oxidation of the biopolymer lignin from the
paper industry was conducted to determine the capacity
for degradation by ve white-rot fungi (Lentinus edodes,
Pleurotus ostreatus, Trametes versicolor, Phanerochaete
chrysosporium and S22). Among these ve isolates, three
white-rot fungi (Phanerochaete chrysosporium, Pleurotus
ostreatus and S22) showed a high level of lignin degradation
at pH 9.0 to 11.0 (Wu et al. 2005).
Degradation of PAHs using white-rot fungi
PAHs are organic substances that mostly lack colour or
are pale yellow solids. ey are an omnipresent class
of many chemically related compounds that persist in
the environment with complex structures and toxicity
(Abdel Shafy et al. 2016). Some white-rot fungi including
BKM-F-1767, Bjerkandera adusta CBS 595.78, Trametes
versicolor Paprican 52, Phanerochaete chrysosporium and
Trametes versicolor has been tested for ability to degrade
hydrocarbons (Field et al. 1992). All white-rot fungi
signicantly degraded anthracene, as well as nine of the
strains eectively degraded benzo(a)pyrene. Of those,
Bjerkandera sp. Bos 55 seems to be new species and was
deemed an eective degrader of anthracene (99.2 %)
and benzo(a)pyrene (83.1%) molecules within 28 days
respectively. e genus Phanerochaete and Bjerkandera
transformed anthracene into anthraquinone, which is an
end metabolite. Further, this analysis showed Trametes sp.
degraded anthracene with no substantial accumulation of
quinone (Field et al. 1992).
e removal of PAHs by means of white-rot fungi
is aected by temperature, the composition of the
medium, dissolved oxygen and soil moisture content
(Chen et al. 2005). e biological removal of PAHs such
as phenanthrene, uorine and pyrene was achieved using
thermotolerant Trametes polyzona RYNF13. is fungus
exhibited PAH degradation at 100 mg L–1. Complete
removal of phenanthrene was detected in mineral salt
glucose medium at 30 °C aer an incubation period of
18 days while 52% of pyrene and 90% of uorine could
be removed under similar conditions. is fungus is still
capable of surviving at a high temperature of about 42
°C and degrades phenanthrene (68%), uorine (48%)
and pyrene (30%) respectively within 32 days. us, this
strain has potential for PAH degradation specically in
the tropical area where even air temperature can be more
than 40 °C (Teerapatsakul et al. 2016). It was shown that
the most ecient laccase-producing white-rot fungi
Pycnoporus sanguineus can remove phenanthrene (45.6%)
and benz(a)anthracene (90.1%) in in vivo conditions (Li
et al. 2018). ey also transformed phenanthrene into
2-dibenzofuranol by the cytochrome P450 monooxygenase
enzyme or 9,10-phenanthrenedione through extracellular
laccase and benz(a)anthracene into benz(a)anthracene-
7,12-dione through extracellular laccase. Various PAHs
that are degraded by diverse white-rot fungi are represented
in Table 1.
Degradation of PCBs using white-rot fungi
PCBs are widespread organic molecules that were used as
coolant liquids in transformers and electric motors during
the 20th century (Borja et al. 2005). Although their application
and production were prohibited in the last decade, they
survive in ecosystems and lead to severe consequences for
living organisms (Colvin, Nelson 1990). Eaton (1985) was
the rst researcher to study PCBs (Aroclor® 1254 mixture)
degradation using Phanerochaete chrysosporium. In this
experiment, Aroclor® 1254 was mineralized into CO2 with
the removal of water-soluble organic compounds and
irreversible attachment to cells. e results obtained have
been validated by the absence of gas chromatographic peaks.
White-rot fungi mediated bioremediation for xenobiotic degradation
108
PCB congener degradation by Ceriporia sp. was carried out
by Hong et al. (2012). In this analysis, four PCB congeners
(4,4’-dichlorobiphenyl, 2,2’,4,4’,5,5’-hexachloro-biphenyl,
2,3’,4’,5-tetrachlorobiphenyl and 2,2’,4,5,5’-pentachloro-
biphenyl) were examined. e biodegradation rate of
4,4’-dichlorobiphenyl on the 13th day was reported to
be around 34.03% whereas the biodegradation rate of
2,2’,4,4’,5,5’-hexachlorobiphenyl on the 17th day was nearly
40.05%. is shows that extremely chlorinated biphenyls
can be reduced by Ceriporia sp. e immobilized laccase
obtained from Coprinus comatus on wood biochar from
diverse species can degrade chlorinated biphenyl in
wastewater (Li et al. 2018). Pleurotus ostreatus, Trametes
versicolor, Phlebia brevispora, Pycnoporus cinnabarinus, and
Pleurotus sajor-caju are few other white-rot fungi explored
for PCBs degradation.
Degradation of PCPs using white-rot fungi
PCPs are lethal compounds that extensively occur in the
industrial output of pesticides and wood preservatives
(Czaplicka 2004). e usage of PCPs was forbidden
in several countries owing to their high toxicity in the
late 1980s but still, they are used in a few countries. e
harmfulness of pentachlorophenol has been broadly
reported as a recalcitrant and global pollutant in the soil
and water (Varela et al. 2017). Degradation of PCPs is
Tab le 1. Degradation of various PAHs by dierent white-rot fungi
PAH compounds White-rot fungi Reference
Acenapthene Phanerochaete chrysoporium Bishnoi et al. 2008
Anthracene Pleurotus ostreatus, Coriolopsis polyzona, Phanerochaete
chrysosporium, Trametes versicolor
Vyas et al. 1994
Trametes pocas, Trametes cingulate Tekere et al. 2005
Irpex lacteus Baborová et al. 2006
Anthracophyllum discolor Acevedo et al. 2011
Chrysene Bjerkandera sp. Valentin et al. 2007
Polyporus sp. Hadibarata et al. 2009
Pleurotus ostreatus Nikiforova et al. 2010
Pleurotus sajor-caju Saiu et al. 2018
Dibenzothiophene Coriolopsis gallica Bressler et al. 2000
Bjerkandera sp. Valentin et al. 2007
Agrocybe aegerita, Coprinellus radians Aranda et al. 2009
Fluoranthene Bjerkandera sp. Valentin et al. 2007
Phanerochaete chrysosporium Bishnoi et al. 2008
Pleurotus pulmonarius Wirasnita, Hadibarata 2016
Fluorene Agrocybe sp. Chupungars et al. 2009
Pleurotus eryngii Hadibarata, Kristanti 2014
Polyporus sp. Lazim, Hadibarata 2016
Trametes sp. Zhang et al. 2016
Ganoderma sp. Torres-Farradá et al. 2019
Napthalene Phlebia lindtneri Mori et al. 2003
Trametes versicolor Bautista et al. 2010
Armillaria sp. Hadibarata et al. 2012
Pleurotus ostreatus Sukor et al. 2012
Pleurotus eryngii Hadibarata et al. 2013
Ganoderma sp. Torres-Farradá et al. 2019
Phenanthrene Trametes versicolor Han et al. 2004
Bjerkandera sp..Terrazas-Siles et al. 2005
Phanerochaete chrysoporium Bishnoi et al. 2008
Anthracophyllum discolor Acevedo et al. 2011
Ganoderma lucidum Agarwal et al. 2018
Pycnoporus sanguineus Li et al. 2018
Pyrene Dichomitus squalens, Pleurotus sp..Martenz, Zadrazil 1996
Phlebia brevispora Lee et al. 2016
Coriolopsis brysina Agarwal, Shahi 2017
Pleurotus sajor-caju Saju et al. 2018
Quinoloine Pleurotus ostreatus Zhang et al. 2007
A. Kathiravan, J.J. Gnanadoss
109
achieved in three ways: via oxygenolysis, hydroxylation
or reductive dehalogenation (Field, Sierra-Alvarez 2008).
Fungal remediation of PCPs gained interest in the last forty
years. White-rot fungi can degrade PCPs and transform
the respective PCPs compounds through methylation and
dechlorination reactions. PCPs degradation under both
lignolytic and non-lignolytic conditions using three white-
rot fungi (Trametes sp., Pleurotus sp., and Phanerochaete
chrysosporium) were studied (Ryu et al. 2000). e activity
of lignolytic enzymes was detected in Pleurotus and
Trametes cultures, but not in Phanerochaete chrysosporium.
is proves that PCP degradation can be carried out
in two conditions (lignolytic and non-lignolytic) using
white-rot fungi. Phlebia acanthocystis, a white-rot fungus,
was capable of degrading 100% and 76% of PCPs (25 μM
concentration) in low nitrogen as well as potato dextrose
broth culture media, respectively, during incubation for
approximately 10 days (Xiao, Kondo 2020).
e reduction of PCPs in Phlebia acanthocystis
culture is followed by the production of two metabolites
(p-tetrachlorohydroquinone and pentachloroanisole)
through oxidative metabolism. e metabolism of both
molecules is closely linked to Phlebia acanthocystis
extracellular enzymes. Further, the breakdown of PCPs to
p-tetrachlorohydroquinone is carried out by cytochrome
P450 monooxygenase (Xiao, Kondo 2020). e white-rot
fungi with ability to degrade PCPs are Trametes versicolor
(Walter et al. 2004), Anthracophyllum discolor (Rubilar et al.
2007), Bjerkandera adusta, Fomes fomentarius, Ganoderma
applantum, Pleurotus ostreatus, and Laetiporus cincinnatus
(Ramesh, Pattar 2009) and Phlebia acanthocystis (Xiao,
Kondo 2020).
Degradation of TNT using white-rot fungi
TNT is oen utilized as an explosive by the military and
can cause pollution to soil and water at TNT production
and storage sites. It is mutagenic and harmful to many
organisms in that environment. Based on animal studies,
TNT can be a carcinogen for humans (Honeycutt et al.
1996). Most of the white-rot fungi can convert TNT to
dinitrotoluenes and further, result in mineralization to CO2
(Pointing 2001). TNT degradation (50 mg L–1) was studied
using seven white-rot species in two dierent media: yeast-
malt-glucose (YMG) medium and nutrient-rich YMG
medium (Kim, Song 2000). e degradation rate was
higher in nutrient-rich YMG medium than in the limited
nutrient YMG medium. Hydroxylamino-dinitrotoluene
isomers have been recognized as the rst TNT metabolites
to be detected and these compounds are converted into
amino-dinitrotoluenes during further incubation. It was
observed that TNT (90 mg L–1) was degraded in nutrient
broth during 21 days by four white-rot fungal species:
Phanerochaete chrysosporium (67%), Phanerochaete sordida
(87%), Phlebia brevispora (90%), and Cyathus stercoreus
(94%). e TNT degradation from culture was evaluated
by high-performance liquid chromatography and the
cytotoxicity of pollutants in the medium was calculated by
Salmonella/microsome bioassay. is study showed that
white-rot fungi can degrade and detoxify TNT compounds
in aerobic conditions in non-lignolytic nutrient broth
(Donnelly et al. 1997). TNT degradation was examined by
several other white-rot fungi like Irpex lacteus (Kim, Song
2003), Hypholoma fasciculare (Perkins et al. 2005), Trametes
versicolor (Cheong et al. 2006), Kuehneromyces mutabilis,
and Stropharia sp. (Serrano-González et al. 2018).
Degradation of BTEX compounds using white-rot fungi
BTEX compounds like benzene, toluene, ethylbenzene,
and xylenes are a vital class of organic contaminants that
are constituents of petroleum fuels and they are oen
used in various industries as industrial solvents (Smith
1990). e rst study of white-rot fungi degradation
of BTEX compounds was reported by Yaddav, Reddy
(1993). Waste mushroom biomass from Ganoderma
lucidum and Pleurotus ostreatus was used as a substrate
(10%) to decontaminate Esfahan Oil Renery’s petroleum
hydrocarbon contaminated soil (Mohammadi-Sichani et
al. 2019). Petroleum hydrocarbons at the contamination
site were oxidized by waste mushroom biomass of Pleurotus
ostreatus (69.5%) as well as Ganoderma lucidum (57.7%)
and also reduced the soil toxicity in 3rd month respectively.
BTEX compound degradation using white-rot fungi has
been less explored.
Degradation of antibiotics using white-rot fungi
Antibiotics are substances that help to treat communicable
diseases in animals, humans, cattle and aquacultures around
the globe. e discharge of a high proportion of vaccines
into water sources and soil creates a potential threat to all
microbes in these surroundings (Cycoń et al. 2019). e
production of antibiotics is continuously increasing and
their usage has extended from 100 000 to 200 000 tons
worldwide (Gelband et al. 2015). Almost all antibiotics are
not entirely processed in humans and animal bodies. A large
number of therapeutic drugs are discharged into soil and
water bodies by community wastewater, livestock manure,
sludge from sewage and nitrogenous wastes that are oen
used to irrigate and enhance farmlands (Bouki et al. 2013).
Usually, the traditional treatment process is not eective in
treating many pharmaceutical products (Heberer 2002).
e white-rot fungi-mediated bioremediation technique
is therefore a simple and economical method to eliminate
antibiotics.
An in vitro study was conducted on use of LiP obtained
from Phanerochaete chrysosporium for the removal of two
drugs (carbamazepine and diclofenac) that are commonly
found in water bodies. It showed that the LiP entirely
removed diclofenac at pH 3.0 to 4.5 and 3 to 24 ppm H2O2.
e ecacy of carbamazepine degradation is generally
below 10% (Zhang, Geißen 2010). A study on ciprooxacin
degradation using Pleurotus ostreatus (Singh et al. 2017)
showed that the highest degradation rate occurred at
White-rot fungi mediated bioremediation for xenobiotic degradation
110
a concentration of 500 ppm due to maximum enzyme
production. e degradation rate of ciprooxacin aer
14 days of culture at this concentration was evaluated by
three assays: titrimetric (68.8%), indigo carmine (94.25%)
and methyl orange (91.34%). Elimination of ciprooxacin
was additionally demonstrated by high-performance liquid
chromatography, which showed 95.07% degradation and the
microbiological experiment exhibited reduced biological
activities of degraded products against pathogenic bacteria
i.e. Staphylococcus aureus, Escherichia coli and Streptococcus
pyogenes. Trametes hirsuta eciently degraded higher
concentrations of chloramphenicol (10 mg L–1) in the
existence of a laccase mediator system like syringaldehyde,
vanillin, 2,20-azinobis-3-ethylbenzothiazoline-6-sulpho-
nic acid and α-naphthol. e availability of mediators
enhanced the degradation percentage from 10 to 100%
during 48 h. Liquid chromatography mass spectrometry
conrmed the chloramphenicol degradation. e produc-
tion of chloramphenicol aldehyde aer the breakdown
was non-pathogenic to microorganisms (Navada, Kulal
2019). Magnetic cross-linked enzyme aggregates of
Cerrena laccase have been demonstrated to be eective
in the biodegradation of antibiotics such as tetracycline,
oxytetracycline, ampicillin, sulfamethoxazole and erythro-
mycin (Yang et al. 2017). For example, at 40 U mL–1 Cerrena
laccase removed tetracycline antibiotic (100 μg mL–1) at
pH 6 and temperature at 25 °C during 48 h without redox
mediators. Numerous studies revealed that white-rot fungi
have the potential to degrade antibiotics (Table 2).
Degradation of pesticides using white-rot fungi
In modern-day farming, pesticide application is more
common to increase crop produce and reduce post-harvest
losses (Hai et al. 2012). About 5% of applied pesticides
exterminate the specic pest organisms whereas the
remnants pass through surface and groundwater (Nawaz et
Tab le 2. Degradation of dierent antibiotics by various white-rot fungi
Antibiotics White-rot fungi Reference
Amoxicillin Trametes polyzona Lueangjaroenkit et al. 2019
Ampicillin Verticillium leptobactrum Kumar et al. 2013
Carbamazepine Trametes versicolor Hata et al. 2010a
Phanerochaete chrysosporium Zhang, Geißen 2010
Stropharia rugosoannulata, Gymnopilus luteofolius, Ganoderma lucidum,
Irpex lacteus, Agrocybe erebia
Castellet-Rovira et al. 2018
Chloramphenicol Trametes hirsuta Navada, Kulal 2019
Ciprooxacin Trametes versicolor Prieto et al. 2011
Pleurotus ostreatus Singh et al. 2017
Ganoderma lucidum Chakraborty, Abraham 2017
Pycnoporus sanguineus, Phanerochaete chrysosporium Gao et al. 2018
Xylaria longipes Rusch et al. 2018
Dichlofenac Phanerochaete sordida Hata et al. 2010b
Trametes trogii, Phanerochaete chrysosporium Aracagök et al. 2018
Pleurotus ostreatus Chapple et al. 2019
Erythromycin Trametes versicolor, Bjerkandera adusta Aydin et al. 2016
Ibuprofen Trametes versicolor, Irpex lacteus, Ganoderma lucidum, Phanerochaete
chrysosporium
Marco-Urrea et al. 2009
Lamotrigine Pleurotus ostreatus Chefetz et al. 2019
Naproxen Trametes versicolor Borràs et al. 2011
Noroxacin Trametes versicolor Prieto et al. 2011
Irpex lacteus, Panus tigrinus, Dichomitus squalens, Pleurotus ostreatus Čvančarová et al. 2015
Ganoderma lucidum Chakraborty, Abraham 2017
Ooxacin Trametes hirsute Haroune et al. 2014
Trametes versicolor, Irpex lacteus, Panus tigrinus, Dichomitus squalens,
Pleurotus ostreatus
Čvančarová et al. 2015
Sulfamethoxazole Phanerochaete chrysosporium Guo et al. 2014
Pleurotus ostreatus, Pleurotus pulmonarius, Trametes sp.de Araujo et al. 2017
Trametes versicolor Alharbi et al. 2019
Tetracycline Phanerochaete chrysosporium Wen et al. 2009
Trametes versicolor Suda et al. 2012
Cerrena sp. Yang et al. 2017
Pycnoporus sp. Tian et al. 2020
A. Kathiravan, J.J. Gnanadoss
111
al. 2011). e existence of agropesticides in the biosphere
has becomes a threat to ora, fauna, microbes and humans
(Hussain et al. 2015). e removal of lindane pesticides was
accomplished by Cyathus bulleri and Phanerochaete sordida.
Among these two species, Cyathus bulleri degraded more
eectively than Phanerochaete sordida. During the time
of degradation, two degradable intermediate metabolites
(tetrachlorocyclohexene and tetrachlorocyclohexanol)
were observed in Phanerochaete sordida culture.
Tetrachlorocyclohexanol was the rst detected degradation
product in Cyathus bulleri culture (Singh, Kuhad 2000).
Bending et al. (2002) studied the degradation potential
of nine white-rot fungi against monoaromatic pesticides
like diuron, metalaxyl, atrazine or terbuthylazine in liquid
culture. e highest level of pesticide degradation was
reported in Hypholoma fasciculare, Stereum hirsutum and
Coriolus ver sicolor. e rate of degradation of terbuthylazine,
diuron and atrazine was 86% while for metalaxyl the
degradation rate was below 44%. e capability of three
Phlebia species to degrade dieldrin and aldrin was also
examined (Xiao et al. 2011). Aer 42 days of treatment,
the three Phlebia sp. could degrade approximately 50% of
dieldrin in a low nitrogen medium. ree oxidized products
were identied as dieldrin metabolites in Phlebia species;
oxidation reactions might play an eective role in removing
dieldrin. Further, aldrin showed high degradation activity
and aer 28 days of culture, 90% of aldrin was degraded.
Transformed metabolites (two carboxylic acid products
and 9-hydroxyaldrin) were identied in the fungal cultures.
is showed that the methyl group of pesticides such as
aldrin and dieldrin might be susceptible to oxidative attack
by white-rot fungi. Clothianidin pesticide degradation
was tested using Phanerochaete sordida in nitrogen-
limited broth. Approximately 37% of clothianidin was
degraded at 30 °C aer an incubation period of 20 days.
N-(2-chlorothiazol-5-yl-methyl)-N’-methylurea was the
transformed metabolite during clothianidin degradation,
identied by analyzing the supernatant culture with high-
resolution electrospray ionisation mass spectrometry
and nuclear magnetic resonance (Mori et al. 2017). Some
common pesticides that are degraded by various white-rot
fungi are shown in Table 3.
Degradation of dyes using white-rot fungi
Articial dyes are broadly exploited in various industries
like food, cosmetics, pharmaceutical, textiles and leather,
etc. (Couto 2009). From 1856, over 105 dierent dyes
have been produced globally with a yearly production
of about 7 × 105 metric tons (Chen et al. 2003). Globally,
approximately 28 000 tons of textile dyestus are released
into textile industrial euent each year (Jin et al. 2007).
Unprocessed dye euents in water bodies cause severe
environmental and health threats (Shedbalkar et al. 2008).
Developing a cost-eective biological method to remove
synthetic colours is essential.
White-rot fungi are a class of fungi that synthesize
Tab le 3. Degradation of dierent pesticides by various white-rot fungi
Pesticide White-rot fungi Reference
Atrazine Pleurotus pulmonarius Masaphy et al. 1996
Anthracophyllum discolor Elgueta et al. 2016
Carbofuran Phlebia sp., Irpex lac teus Li et al. 2020
Chlorpyrifos Phlebia sp., Lenzites betulinus, Irpex lacteus Wang et al. 2020
Clothianidin Phanerochaete sordida Mori et al. 2017
Dichlorophen Bjerkandera adusta Davila-Vazquez et al. 2005
Dichlorophenoyacetcid Lentinula edodes Tsujiyama et al. 2013
Lentinus crinitus Serbent et al. 2020
Diuron Agrocybe semiorbicularis, Auricularia auricola, Flammulina
velupites, Dichotomitus squalens, Coriolus veriscolor, Hypholoma
fasciculare, Phanerochaete velutina, Pleurotus ostreatus, Stereum
hirsutum
Bending et al. 2002
Ceriporia lacerata, Phanerochaete chrysosporium,
Phanerochaete sordida, Trametes versicolor
Mori et al. 2018
Endrin Phlebia acanthocystis, Phlebia brevispora Xiao, Kondo 2019
Fipronil Trametes versicolor Wolfand et al. 2016
Lindane Cyathus bulleri, Phanerochaete sordida Singh, Kuhad 2000
Ganoderma australe Dritsa et al. 2005
Pleurotus ostreatus Papadopoulou et al. 2006
Ganoderma lucidum Kaur et al. 2016
Parathion Bjerkandera adusta, Pleurotus ostreatus, Phanerochaete
chrysosporium
Jauregui et al. 2003
1,1’-(2,2,2-Trichloroethane-1,1-
diyl)bis(4-chlorobenzene) (DDT)
Phlebia lindineri, Phlebia brevispora Xiao et al. 2011
White-rot fungi mediated bioremediation for xenobiotic degradation
112
enzymes able to decompose dyes in aerobic conditions
(Nozaki et al. 2008). ey produce several oxidoreductases
that can biodegrade lignin and their associated aromatic
compounds. e capacity for dye degradation diers for
fungal species and enzymes (Nyanhongo et al. 2002). Four
dierent mechanisms are involved in the decolouration of
dye using white-rot fungi: biodegradation, biosorption,
bioreactor and immobilized lignin modied enzymes
(Jebapriya, Gnanadoss 2013). e biosorption mechanism
involves the adsorption of dyes by fungal biomass. However,
dye removal by adsorption was found to be restricted to
50% (Knapp et al. 2001). Biodegradation has a key role in
dye decolourization, as it secretes extracellular lignolytic
enzymes to oxidize the dyes (Jayasinghe et al. 2008).
Laccase producing white-rot fungi Pleurotus floridanus
LCJ155, Leucocoprinus cretaceous LCJ164, and Agaricus sp.
LCJ169 were eective in degrading synthetic dyes such as
bromophenol blue, methyl red, phenol red, Congo red and
brilliant green (Jebapriya, Gnanadoss 2014). Bjerkandera
adusta cultured in potato dextrose broth medium in an
airli bioreactor. Aer 10- to 15-h treatment, there was 90%
of dye decolourization for both acid and reactive colourants.
ese results suggested that a bioreactor employed with a
white-rot fungal strain is promising for dye euent removal
(Sodaneath et al. 2017). e decolourization of erichrome
black T and Congo red dyes by Pleurotus ostreatus was
studied (Gnanadoss et al. 2013). e highest degradation
rate of dyes was observed when Pleurotus ostreatus culture
was immobilized on polyurethane foam.
e LiP enzyme obtained from Ganoderma lucidum
(GRM117) and Pleurotus ostreatus (PLO9) immobilized
on carbon nanotubes is a promising biocatalyst for dye
removal (Oliveira et al. 2018). Biosorption of remazol
brilliant blue R and indigo carmine dyes was studied using
immobilized biomass of white-rot fungus Psathyrella
candolleana LCJ178. Polyurethane foam, stainless steel
sponge, lua sponge, scotch brite and white nylon sponge
were used as supporting materials for immobilization
of Psathyrella candolleana LCJ178 biomass. Of these,
stainless steel sponge was found eective in binding to
the culture without causing any operational diculties.
is study revealed that the selection of suitable support
material, culture condition (shaking) and other physical
aspects were critical for enhancing the process of dye
removal (Gnanasalomi et al. 2016). Several reviews on
the dye removal by means of white-rot fungi have already
been published (Shah, Nerud 2002; Wesenberg et al. 2003;
Asgher et al. 2008; Tišma et al. 2010; Jebapriya, Gnanadoss
2013; Sen et al. 2016; Chaturvedi et al. 2019; Periasamy et
al. 2019).
Conclusions
Xenobiotic compounds are anthropogenic substances
generated from multiple industries that have negative
environmental consequences if they are released without
proper pretreatment. Xenobiotics are noxious to living
organisms; therefore they need to be removed quickly
before entering into the environment. However, the
physical and chemical methodologies are not feasible
enough to degrade xenobiotic compounds. Subsequently,
an alternative remediation technology is needed to combat
xenobiotic compounds. Bioremediation technology is
more promising in xenobiotic degradation owing to its
cost-eective and eco-friendly approach.
White-rot fungi are thought to be ecient bio-degraders
of organic pollutants probably owing to their metabolic
enzymes with extensive substrate specicities. Dierent
white-rot fungi have dierent biodegradation abilities for
dierent xenobiotic compounds primarily due to their
unique morphology, culture and environmental aspects as
well as the nature of the enzymes produced. e characteristic
features of lignolytic enzymes dier between taxa of white-
rot fungi. ey are well explored in the biodegradation of
diverse xenobiotics like dyes, hydrocarbons, and phenolic
compounds on a laboratory scale. Still, many studies are
required to explore the scope of white-rot fungi at the
industrial level. Additionally, screening of new white-rot
fungal isolates oen with promising enzyme activity is
required for the bioremediation of new toxic chemicals due
to increased industrial contamination. White-rot fungi in
combination with biotechnological tools such as genetic
engineering can produce novel strains with ideal properties
for the disintegration of numerous xenobiotic pollutants.
Acknowledgements
e authors are grateful to the management of Loyola College,
Chennai for providing necessary facilities and encouragement.
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White-rot fungi mediated bioremediation for xenobiotic degradation
Received 28 May 2021; received in revised form 26 June 2021; accepted 10 September 2021
