• Vol. II, No. 1 • Enero-Abril 2008 •

Review of environmental

organopollutants degradation by white-

rot basidiomycete mushrooms

Revisión de degradación de contaminantes

ambientales por basidiomicetos de la pudrición

blanca

ORETO

OBLES

-H

ERNÁNDEZ

1,4

ECILIA

-G

ONZÁLEZ

- F

RANCO

, D

ONALD

L. C

RAWFORD

AND

ESLEY

W. C. C

HUN

Recibido:

Diciembre 14, 2007

Aceptado:

Abril 20, 2008

Abstract

White-rot fungi consist of a group of basidiomycetes that

are able to remove lignin, cellulose, and hemicellulose

concurrently at approximately equal rates. These fungi

produce three enzymes commonly known as lignin-modifying

enzymes (LMEs) that are responsible for the degradation of

wood components. These enzymes are produced during

the secondary metabolism under an obligatory aerobic

process and are induced by nutrient starvation, low pH, and

high concentrations of Mn. We focused this review on the

source of environmental organopollutants and the role that

these white-rot fungi play on the transformation or

mineralization of the environmental contaminants. These

recalcitrant compounds originate mainly from human

contamination. White-rot fungi or their enzymes showed

mineralization of many environmental contaminants such as

1,1,1-trichloro-2,2-bis(4-chlorophenyl) ethane (DDT), 2, 4,

6-Trinitrotoluene (TNT); polychlorinated biphenyls (PCB’s);

polycyclic aromatic hydrocarbons (PAH’s); wood

preservatives; some synthetic dyes; and bleach-derived

from paper producing plants.

Keywords: Bioremediation, environmental contaminants,

lignin modifying enzymes.

Resumen

Los hongos de la pudrición blanca de la madera pertenecen a un

grupo de basidiomicetos capaces de degradar lignina, celulosa y

hemicelulosa en proporciones más o menos equivalentes. Estos

hongos producen tres enzimas comúnmente conocidas como

enzimas modificadoras de la lignina (LME´s), las cuales son

producidas durante el metabolismo secundario bajo un proceso

estrictamente aerobio y son favorecidas por deficiencias

nutricionales, bajo pH, y exceso de Mn. En esta revisión nos

enfocamos en la fuente de los contaminantes ambientales más

comunes y el papel que juegan los hongos de la pudrición blanca

de la madera sobre la degradación de los diversos contaminantes

orgánicos que afectan el medio ambiente. Estos contaminantes

ambientales se originan principalmente por la acción del ser

humano. Los hongos de la pudrición blanca de la madera o sus

productos mostraron mineralización de varios de los contaminantes

ambientales como el 1,1,1-trichloro-2,2-bis(4-chlorophenyl) ethane

(DDT), el 2, 4, 6-Trinitrotolueno (TNT); bifenil policlorinados (PCB’s);

hidrocarburos policlínicos aromáticos (PAH’s); conservadores de

la madera; colorantes sintéticos; y blanqueadores derivados de

plantas productoras de papel.

Palabras clave: Biorremediación, contaminantes orgánicos,

enzimas modificadoras de la lignina.

_________________________________

1Facultad de Ciencias Agrotecnológicas, Universidad Autónoma de Chihuahua, Ciudad Universitaria S/N Campus 1, Chihuahua, Chih.,

31310, México. Phone and Fax: (614) 439-1844

2Department of Microbiology, Molecular Biology and Biochemistry, University of Idaho, Moscow, ID 83844-3052, USA.

3Department of Plant Soil and Entomological Sciences, University of Idaho. Moscow, ID 83843-2339, USA.

4Electronic address of author. Email: lrobles@uach.mx,.

Medio ambiente y desarrollo sustentable

Artículo arbitrado

• Vol. II, No. 1 • Enero-Abril 2008 •

Loreto Robles-Hernández, Ana Cecilia-González- Franco, Donald L. Crawford and W. W. C. Chun.: Review

of environmental organopollutants degradation by white-rot basidiomycete mushrooms

Introducción

White-rot fungi consist of a group of basidiomycetes that are able to remove lignin, cellulose,

and hemicellulose concurrently at approximately equal rates. Wood decay by white-rot fungi

maintains its fibrous nature and loses strength gradually until it is completely degraded.

Commonly a bleached and light color is observed as the wood is decomposed (Figure 1)

(Alexopolous et al., 1996). Although white-rot fungi can degrade lignin, it is extremely recalcitrant

and is mineralized in an obligatory aerobic process. The oxidation of lignin generates no net

energy gain; as lignin is not a substrate in the primary metabolism, and Instead, lignin is

degraded during secondary metabolism to access wood polysaccharides hidden within lignin-

carbohydrate structures, providing energy to

other organisms (Jefries, 1990).

These fungi secrete three chemically

distinct extra cellular enzymes; referred to as

lignin-modifying enzymes (LMEs), which are

critical for lignin degradation. Two of them are

glycosylated heme-containing peroxidases

[lignin peroxidase (LiP, E.C. 1.11.1.14) and

Mn dependant peroxidase (MnP,

E.C.1.11.1.13)] and the third one is a copper-

containing phenoloxidase [laccase (Lac, EC

1.10.3.2)]. The MnP enzyme catalyses an

H O -dependant oxidation of Mn2+ to Mn3+

in culture. Conversely, Lac production is

favored by agitation (Leonowicz et al. 1999).

A great deal of research has been

conducted on the role of white-rot fungal

LMEs in bioremediation of pesticides and

other organopollutants. White-rot fungi have

transformed or mineralized organochlorines,

organophosphates, munitions waste,

polychlorinated biphenils, polycyclic

aromatic hydrocarbons, wood

preservatives, synthetic dyes, bleach, and

pentachlorophenol (Bumpus and Aust, 1987;

Gramms et al., 1999; Hawari et al., 1999;

2 2

which oxidizes phenolic components of lignin

(Wariishi, Valli, and Gold, 1992). The Lac

enzyme generates radicals from a low-

molecular-mass re-dox mediator in an H2O2-

independent reaction. One mediator

compound has been identified as 3-

hydroxylanthranilate in the laccase-producing

white-rot fungus Pycnoporus cinnabarinus

(Bourbonnais et al., 1997), and others such

as 1-hydroxybenzotriazole (HBT) and 2,2’-

azino-bis-(3-ethylbenzothiazoline-6 sulfonic

acid) have been reported to be laccase

mediators in other fungi (Pointing, 2001). The

functioning of LiP, MnP, and Lac has been

studied in liquid cultures. Lignin-modifying

enzyme production occurs during secondary

metabolism and is induced by nutrient

starvation, primarily nitrogen. The production

of LiP and MnP is more efficient in high

oxygen levels, but is repressed by agitation

Limura et al., 1996; Lin et al.,1990; Pointing,

2001). In this review, we focus on the source

and degradation or mineralization of

environmental organopollutants by the white-

rot fungi.

Figure 1. White rotted wood of different plants with

young fruiting bodies of various species of white-rot

fungi, showing the typical wood decomposition by

this group of fungi (Alexopoulos et al., 1996).

Loreto Robles-Hernández, Ana Cecilia-González- Franco, Donald L. Crawford and W. W. C. Chun.: Review

of environmental organopollutants degradation by white-rot basidiomycete mushrooms

• Vol. II, No. 1 • Enero-Abril 2008 •

CO2

Pesticide Degradation.- Organochlorine

insecticides such as 1,1,1-trichloro-2,2-

compounds, such as methylcarbamate and

synthetic pyrethroid insecticides that were

developed to replace organochlorines were

toxic and persistent as well. Likewise, new

herbicides such as chlorophenoxyalkanoates,

triazines, and other hydrocarbons (PCBs)

have also caused toxicity and persistence in

the environment (Pointing, 2001).

Although DDT is a persistent

environmental pollutant, it does appear to

undergo slight degradation in the

environment. A general pathway for DDT

degradation involves reductive

dechlorination, followed by further

dechlorination, oxidation, and decarboxilation

prior to ring cleavage (Figure 2) (Bumpus and

Aust, 1987).

Figure 2. Proposed degradation of DDT by the white-

rot fungus Phanerochaete chrysosporium. Adapted

from Bumpus and Aust (1987).

CL CL

CCL

bis(4-chlorophenyl) ethane (DDT), lindane

and aldrins have been used in enormous

quantities for many decades in agriculture

and for public health. The organochlorine

herbicides 2,4-dichlorophenoxy-acetic acid

(2,4-D), 2,4,5-trichlorophenoxiacetic acid

(2,4,5-T) and 2-methyl-4, 6-

dichlorophenoxyacetic acid (MCPA) have

also been widely used in agriculture with the

CL CL

CCL

CL CL

HCCL

CL CL

HCCL

concomitant generation of dioxins. Dioxins

were components of «Agent Orange,» used

extensively as defoliants during the Vietnam

War and now are groundwater and soil

contaminants. Although organochlorines are

not being used in developed countries, their

use continues in developing nations

(Pointing, 2001). The organophosphorous

C CL

Species of Pleurotus ostreatus, Phelinus

weirii, and Polyporus versicolor have been

shown to degrade DDT. They were able to

mineralize 5.3-13.5% of added 14C-

RING CLEAVAGE PRODUCT

DBP

FW-152

DDD

DICOFOL

DDT

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Loreto Robles-Hernández, Ana Cecilia-González- Franco, Donald L. Crawford and W. W. C. Chun.: Review

of environmental organopollutants degradation by white-rot basidiomycete mushrooms

radiolabeled DDT, dicofol, and

methoxychlor over 30 days under ligninolytic

growth conditions (Bumpus and Aust, 1987).

During DDT biodegradation, intermediate

products are generated which later are

degraded. It has been shown that 14C-

radiolabeled 1,1-dichloro-2,2-

bis(4chlorophenil) ethane (DDE), a sub

product of DDT, is mineralized to

CO and

H2O by Phanaerochate chrysosporium

(Bumpus and Aust, 1987). Phanerochaete

chrysosporium has also shown to degrade

up to 23.4% of 14C-radiolabeled aldrin,

dieldrin, chloridane, lindane, and mirex

during 30 days of incubation (Kennedy et

al., 1990). Organophosphate insecticides

are not usually persistent in the environment,

and are easily degraded. Phanerochaete

chrysosporium mineralized up to 27.5% of

C-radiolabeled chloropyrifos, fonofos, and

terbufos in 18 days of incubation (Bumpus

and Aust, 1987). The organophosphate

insecticides are less persistent in the

environment than organochlorine

insecticides and P. chrysosporium has

been demonstrated to mineralize 12.2-

27.5% of 14C-radiolabeled chloropyrifos,

fonofos, and turbofos in 18-day incubation

(Bumpus et al., 1993 cited in Pointing,

2001). The chlorinated triazine herbicide 2-

chloro-4-ethylamine-6-isopropyl-amino-1, 2,

4-triazine (atrazine), which is recalcitrant in the

environment has also been transformed by P.

chysosporium (Mougin et al., 1994 cited in

Pointing, 2001) and Pleurotus pulmonarius

(Masaphy et al., 1993 cited in Pointing, 2001)

into less recalcitrant hydroxylated and N-

dealkylated metabolites.

2, 4, 6-Trinitrotoluene (TNT)

At military sites, TNT wastes from

munitions production and storage have been

found to contaminate water, soil, and

sediments. TNT has been shown to cause liver

damage and anemia in humans (Pointing,

2001; Spiker et al., 1992). Currently, methods

for remediation of TNT-contaminated soils are

being studied. Some anaerobic bacteria can

transform but not mineralize TNT (Pointing,

2001). However, recent studies have

demonstrated the ability of white-rot fungi to

mineralize TNT. The transformation of TNT

results in the formation of the dinitrotoluenes

(DNTs), which are generally not degraded

immediately. Many microorganisms are able

to transform TNT into DNTs, but only white-rot

fungi degrade and mineralize the DNTs to

CO2 and H2O (Hawari et al., 1999; Hodson et

al., 2000). The transformation and

mineralization of TNT by white-rot fungi is

illustrated in Figure 3.

Figure 3. Bioremediation of 2,4,6-trinitrotoluene (TNT) contaminated soil by white-rot fungi. Adapted from

Hawari et al (1999); Hodson et al. (2000).

• Vol. II, No. 1 • Enero-Abril 2008 •

Loreto Robles-Hernández, Ana Cecilia-González- Franco, Donald L. Crawford and W. W. C. Chun.: Review

of environmental organopollutants degradation by white-rot basidiomycete mushrooms

important role in the degradation of DNTs.

Addition of surfactant to ligninolytic cultures

of P. chrysosporium significantly enhanced

TNT mineralization (Hodson et al., 2000).

Many studies related to TNT degradation

have employed relatively low TNT

concentrations. Phanerochaete

chrysosporium could germinate from

spores, grow and transform at 20 ppm, but

not at 100 ppm of TNT (Spiker, et al., 1992).

Polychlorinated Biphenyls (PCB’s) PCBs

are produced through chlorination of the

biphenyl group. PCBs are a family of

compounds with a wide range of industrial

applications in heat transfer fluids, dielectric

fluids, hydraulic fluids, flame-retardants,

solvent extenders and organic diluents.

PCBs have entered into soil and sediment

environments as a result of improper

disposal of industrial PCB wastes and

leakage of PCBs from electric transformers

(Pointing, 2001; Yadav et al., 1995).

Numerous studies have shown that white-rot

fungi including Coriolopsis polyzona, P.

chrysosporium, Pleurotus ostreatus, and

Trametes versicolor were capable of PCB

removal in-vivo (Figure 4) (Yadav et al.,

1995). Studies using

C-radiolabeled PCBs

showed that C. polyzona, P. chrysosporium

and T. versicolor were capable of PCBs

elimination but the exact role of LME in this

process still is not clear (Baudette et al.,

2000).

Figure 4. Degradation of PCBs (Pentachlorophenol Aroclors) by Coriolopsis polyzona, P. chrysosporium,

Pleurotus ostreatus, and Trametes versicolor. Adapted from Yadav et al. (1995).

Polycyclic Aromatic Hydrocarbons

(PAH’s).- PAHs are benzene homologues

generated from the fusion of four or more

benzene rings. PAHs are highly toxic

organopollutants, which are widely

distributed in industrial and terrestrial

environments. They originate from natural oil

deposits, wood burning, vegetation

decomposition, vehicle transport, waste

incineration and industrial processes. Due

to their toxic effects, PAHs pose a serious

health risk to animals, including humans.

Many of these compounds are known to be

mutagenic and carcinogenic (Collins and Ng,

1997). Several reports have shown that the

white-rot fungi are the only organisms capable

of PAHs degradation and that the rates of

mineralization are correlated with the

production of LMEs (Field et al., 1992). Extra-

cellular preparations of LiP from P.

• Vol. II, No. 1 • Enero-Abril 2008 •

Loreto Robles-Hernández, Ana Cecilia-González- Franco, Donald L. Crawford and W. W. C. Chun.: Review

of environmental organopollutants degradation by white-rot basidiomycete mushrooms

chrysosporium was one of the first LMEs

capable of PAH degradation (Bumpus and

Aust, 1987). Because MnP and Lac have

been shown to be the most predominant

LMEs during the PAHs metabolism, most

research has focused on those enzymes.

The MnP of P. chrysosporium showed

activity in the oxidation of twelve 3-6 ring

PAH. In some cases the enzyme was limited

by Mn2+ availability (Bogan et al., 1996).

Results differ between investigators and

fungal species. For instance, Collins et al.

(1996) found that Lac of T. versicolor could

not oxidize phenanthrene (Figure 5), but Lac

of Coriolopsis gallica could (Pickard et al.,

1999).

Figure 5. Anthracene transformation in the presence of either Lac I or Lac II enzymes purified from Tramites

versicolor. Adapted from Collins et al. (1996).

Wood Preservatives.- The organic wood

preservatives creosote and

pentachlorophenol (PCP) have been used

extensively, although their use has been

discontinued as a result of soil and

groundwater contamination. Creosote is a

coal-tar distillation product consisting of a

highly heterogeneous PAH mixture, which

includes 16 of the United States EPA priority-

listed pollutants. PCP is a benzene ring with

five chloride substitutions, and is listed as a

priority pollutant by the United States EPA

(Pointing, 2001). Decomposition of creosote

by white-rot fungi is very similar to PAH

degradation. However, creosote is more

complex and therefore can be more toxic to

fungi than PAH during degradation (Pointing,

2001). Phanerochaete chrysosporium

mineralized up to 50% of 14C-radiolabeled

PCP when grown under ligninolytic

conditions. Not all species of the genus were

able to mineralize PCP. Some of them were

inhibited in the presence of 5 ppm of PCP;

however, Phanerochaete chrysosporium

and P. sordida grew in the presence of 25

ppm of PCP. A rapid reduction of PCP

resulted in accumulation of the product

pentachloroanisole (PCA), a quinone

intermediate expected for LME-mediated

oxidation (Lin et al., 1990).

Synthetic Dyes.- Synthetic dyes are

chemically diverse, with those commonly

used in industry divided into those of azo,

triphenylmethane or heterocyclic/polymeric

structures. They are used extensively in

biomedical, food, plastic,

• Vol. II, No. 1 • Enero-Abril 2008 •

Loreto Robles-Hernández, Ana Cecilia-González- Franco, Donald L. Crawford and W. W. C. Chun.: Review

of environmental organopollutants degradation by white-rot basidiomycete mushrooms

and textile industries. Synthetic dyes are

not biodegradable and when discharged

into the environment, they are persistent and

many are also toxic (Pointing, 2001). Early

studies have shown that polymeric dyes were

decolorized by ligninolytic cultures of P.

chrysosporium and that inhibitors of lignin

degradation also repressed dye

decolorization (Glenn and Gold, 1983). Other

studies have also reported decolorization of

an extensive number of azo,

triphenylmethane and heterocyclic dyes by

white-rot fungi (Pointing, 2001). The role of

sorption in dye decolorization appears to be

influenced by ligninolytic compounds. A non-

ligninolytic culture of P. chrysosporium was

found to have about 49% of total azo and

heterocyclic dye bound to the mycelium

(Cripps et al., 1990). Conversely, a

ligninolytic culture of P. sanguineu

accounted for less than 3% of azo and

triphenylmethane dye removal (Pointing,

2001). The action of LMEs in dye

decolorization has been demonstrated in

several studies using purified cell-free

enzymes. LiP of P. chrysosporium

decolorized azo, triphenilmethanen and

heterocyclic dyes in the presence of veratryl

alcohol and H2O2 (Cripps et al. , 1990).

Bleach-Derived from Paper Producing

Plants.- Billions of gallons or sometimes

intensely colored waste effluents are

released into the environment annually by the

pulp and paper industry (Michael et al.,

1991). The primary contributor to the color

and toxicity of these streams is the pulp

bleach plant effluent, which contains largely

high molecular, modified and chlorinated

lignin and its degradation products, including

chlorolignins, chloro-phenols, chloro-

catechols, and chloro-aliphatics (Michael et

al., 1991; Pointing, 2001). There are a few

reports that describe the role of white-rot

fungi in the mineralization of those pollutants.

It has been shown that P. chrysosporium can

oxidize, demethylate and dechlorinate bleach-

plant effluents. Among the LMEs, MnP has

been the most effective in these processes

(Michael et al., 1991). It has also been

demonstrated that Lac of T. versicolor has

high activity in dechlorinating the bleach-plant

effluents (Limura et al.,1996).

Conclusions

White-rot fungi are able to degrade lignin,

cellulose, and hemicellulose concurrently at

approximately equal rates. These fungi

secrete three extra cellular enzymes (LMEs)

that are critical for wood degradation.

Because of their ability to biodegradate

natural lignocellulosic materials and humic

substances to CO2 and H2O, the white-rot

basidiomycete mushrooms or their products

are able to transform and mineralize, in-vitro

or in-vivo, many environmental

organopollutants, including pesticides,

munitions waste, polychlorinated biphenyls,

polycyclic aromatic hydrocarbons, wood

preservatives, synthetic dyes, and waste

materials from paper producing plants.

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Loreto Robles-Hernández, Ana Cecilia-González- Franco, Donald L. Crawford and W. W. C. Chun.: Review

of environmental organopollutants degradation by white-rot basidiomycete mushrooms

Resúmenes curriculares de autor y coautores

LORETO ROBLES-HERNÁNDEZ. He is Titular Academic B in the department of Agrotecnological Sciences of the Autonomous University

of Chihuahua. He obtained his Ph.D. at the University of Idaho and his Masters and Bachelors degree at the Autonomous

University of Chihuahua. His experience lies in bacterial and viral diseases, biological control, and plant diagnosis. He teaches

Plant pathology, Microbiology, Biological control, and Postharvest Physiology. He is advisor of Graduate students and is

member of the graduate advising committee.

WESLEY W.C. CHUN. Is an Associate Professor in the Department of Plant Soil and Entomological Sciences of the University of

Idaho, USA. He obtained his Ph.D. at the University of California, Riverside; his M.S. at the University of Hawaii; and his B.S.at

the University of Hawaii. Recently, he conducts research on bacterial diseases of plants, disease diagnosis, biological control,

host range and pathogenicity determinants of phytopathogenic bacteria, and seed pathology. Dr. Chun teaches Biological

control, Biotechnology, and Plant Pathology. He performs disease identification and diagnosis of field, greenhouse, and home

garden/landscape problems. He is advisor of Graduate students and is member of the graduate advising committee.

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Este artículo es citado así:

ROBLES-Hernández L. , A. C. González- Franco, D. L. Crawford and W. W. C. Chun. 2008. Review of environmental organopollutants

degradation by white-rot basidiomycete mushrooms. TECNOCIENCIA Chihuahua 2(1): 32-39.

• Vol. II, No. 1 • Enero-Abril 2008 •

Loreto Robles-Hernández, Ana Cecilia-González- Franco, Donald L. Crawford and W. W. C. Chun.: Review

of environmental organopollutants degradation by white-rot basidiomycete mushrooms

DOI: https://doi.org/10.54167/tecnociencia.v2i2.64

ANA CECILIA GONZÁLEZ. Franco. Dra. Gonzélez is Titular Academic B in the department of Agrotecnological Sciences of the Autonomous

University of Chihuahua. She obtained her Ph.D. at the University of Idaho and his Masters and Bachelors degree at the

Autonomous University of Chihuahua. Her experience lies in fungal and viral diseases, and biological control. She teaches Plant

microbe interactions, Biochemistry, Chemistry, and Biotechnology. She is advisor of graduate students and is a member of the

graduate advising committee. She is member of the National System of Researchers.

DON CRAWFORD. Dr. Don Crawford is Professor of Microbiology, Molecular Biology & Biochemistry and Director of the Environmental

Science Program at the University of Idaho. He obtained his B.A. degree (Biology) from Oklahoma City University, and his M.S. and

Ph.D. degrees (Bacteriology) from the University of Wisconsin, Madison. He spent four years on the faculty of George Mason

University in Fairfax, VA before coming to the University of Idaho in 1975. His expertise lies in microbial physiology and genetics,

especially of soil actinomycetes. He has published 158 papers regarding characterization of microbial enzymes and the use of

actinomycetes as biocontrol agents.