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The following chapter: Use of Fungi Biodegradation by J. W. BENNET, K. G. WUNCH, AND B. D. FAISON Has been taken from the book: Manual of Environmental Microbiology Second Edition Editor in Chief Christon J. Hurst ASM Press Washington, D.C. 2002.

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Page 1: Use of Fungi Biodegradation Environmental Microbiology · Use of Fungi Biodegradation ... Environmental Microbiology Second Edition Editor in Chief Christon J. Hurst ... the perspective

The following chapter:

Use of Fungi Biodegradation by J. W. BENNET, K. G. WUNCH, AND B. D. FAISON

Has been taken from the book:

Manual of Environmental Microbiology

Second Edition Editor in Chief Christon J. Hurst

ASM Press Washington, D.C.

2002.

Page 2: Use of Fungi Biodegradation Environmental Microbiology · Use of Fungi Biodegradation ... Environmental Microbiology Second Edition Editor in Chief Christon J. Hurst ... the perspective

Use of Fungil. \7. BENNETI K. G.

in Biodeadation\yUNCH, AND B. D. FAISON

87In nature, fungi do much of the dirty work. Th"y are par-ticularly efficient at degrading the major plant polymers,cellulose and lignin, but they also decompose a huge arrayof other organic molecules including waxes, rubber, feath-ers, insect cuticles, and animal flesh. Although industrialmicrobiologists regularly hamess fungal metabolism forbrewing, baking, cheese preparation, and for production ofantibiotics, commercial enzymes, and a number of com-modity chemicals, fungi are best known for their dirrywork. They spoil our foods, blight our crops, rot our build-ings, contaminate our petri dishes, and cause some ratherloathsome diseases. Paradoxically, despite this notoriety,the use of fungi in bioremediation has been limited com-pared to that of bacteria. Here we present a brief intro-duction to fungal taxonomy and mycological techniques,introduce methods for isolating fungi and for growing themin the laboratory, define some important terms, review ex,amples of the successful applications of fungal organismsand enzymes for biodegradation, and point out the advan-tages and disadvantages of fungi as agents of bioremedia-t ion.

A LITTLE TAXONOMYLike rnany other higher-order raxonornic units, the term"fungus" is difficult to define. It embraces a large group ofnonphotosynthetic lower eukaryotes once considered partof the plant kingdom and later afforded srarus in their ownkingdom, the "Fifth Kingdom," on the basis of their char-acterist ic absorptive mode of nutr i t ion (102, 117, 168).taditionally, the Myxomycora, or slirne molds, and theEumycota, or "true fungi," comprised the two major sub-divisions within this fungal kingdom. A plasmodium orpseudoplasmodium characterized the Myxomycota, a grouprvhich included well-known senera such as Dict^tosieliumand Physarum, while in the Eumycora the assimilativephase was usually {ilamentous or yeasr-like. More recenrly,classification based on evolutionary relationships (i.e., phy-logenetic classification) has led to a realization rhar theorganisms that have traditionally been called fungi, on thebasis of shared nutritional modes and morphological char-acters, do not represenr a monophyletic lineage. Derivedprimarily from data on small-ribosomal-subunit (rDNA) se-quence analysis, the assemblage of traditional fungi is noivplaced in three groups: the kingdom Fungi, rhe kingdom

Stramenopila, and four protist phyla. ln this classification,the kingdom Fungi encompasses four phyla: Chytridiomy-cota, Zygomycota, Ascomycota, and Basidiomycota (18,26). The Stramenopila encompasses three phyia' Oomy-cota, Hyphochytriomycota, and Labyrinthulornycota. Fromthe perspective of research on fungal degradation, most ofthe species of interest are in the kingdom Fungi.

In filamentous forms, the individual thread-like cells arecalled hyphae. A fungal colony, or porrion of a colony,composed of many hyphae together is called a mycelium.The filamentous/mycelial growth form poses problems indetermining the size of a single organism and in measuringthe growth of fungi. In the older literarure, the term "thal-

lus" is often used to describe macroscopic mycelial forma-tions.

Fungal taxonomy is based on reproducrive morphology,which consists of both meiotic and mitotic spore-bearingstructures. Both sexual and asexual spores are typicallymade in vast numbers. Many fungi have more than onemorphologically distinct spore rype ar different phases intheir life cycles. Further complicating rhis fungal pleomor-phism is the fact that some fungi exist as either yeasr orfilamentous forms depending on the environmental milieu,a phenomenon called dimorphism, best known from med-ically important species.

Like other eukaryotes, fungi have nuclei, mitochondria,B0S ribosomes, and chromosomes. Fungal cells may be hap-loid or diploid; the nuclei within a mycelium rnay all begenetically identical (monokaryotic) or may be a mixtureof different genetic types (heterokaryotic). Basidiomycetesoften have a special form of heterokaryon called a dikar-yon. Although rnany fungi are microscopic, the best-knownspecies form macroscopic fruiting structures such as mush-rooms and truffles. Fungi are ubiquitous in terrestrial en-vironments, and many fungi are capable of growing inenvironments hostile ro mosr other forms of life (97). Forexample, fungi are the only eukaryotes that include mem-bers with thermophilic (60 to 62'C) oprimal growrh tem-peratures (158) .

In summary, the broadly understood concept of fungicomprises a polyphyletic group of eukaryotic, heterotrophicorganisms that absorb their food. Mycology texts such asthose by Alexopoulos, Mims, and Blackwell (10), Ross( 143), Moore-Landecker (124), and Carl i le and Watkinson(10) are helpful introductions ro this economically impor'

960

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rant group. Another useful tool is Ainsw,orth 6 Blsbi''sDictionary of ilrc Fungi (83). General trrx.rnonric principles,as rvell as a guicle to the sometimes arcllne principles offungal nomenclature, which are govcrned by the lnterna-tional Code of Botanical Nomenclature, are presented byHavyksworth (79). The last volumes ( in two parts) of theclassic series, The Fungl: an AduancedTreatise, provide com-prehensive taxonomic coverage (2,3), rvhi le the hrst vol-umes (4-0) give an almost encyclopedic revierv of theclassical mycological literature. Anotl-rer useful resource isthe multivolume series entitled The Mycot a, an Encyclopediaof Fungi (50). Volume VII addresses fungal classilicationand taxonomy (120) .

ACQUtSt i lON, CARE, AND FEEDINGOF FUNGIFilamentous fungi have more described species than anyother group of microorganisms, with :rbotrt 80,000 alreadynamed and approximately 1,800 new species publishedeach year. As with bacteria, it is believed that only a smallproportion of extant species are known tt-r science. Thetotal number of fungal species, both knorvn and unknorvn,has been estimated at more than 1.5 mil l ion (80, BZ).

About 170,000 pure strains of fungi are maintained inculture col lect ions international ly, representing an esti-mated 7,000 different species (Bi ). Information about theseresources can be accessed through the World l)irectory ofCoLlections of Cukure.s of Microorganisms (156). One of theoldest and largest fungal collections is the Centrarrlburearvoor Schemmelcultures in the Netherlands. The major col-lection in the United States is the Atnerican Type CultureCollect ion (98). In addit ion, the col lect ion at theNorthern Regional Research Laboratory of the U.S. De-partment of Agriculture in Peoria, lll., houses a large nLrm-ber of economically important fungi, ancl the ForestProducts Laboratory in Madison, Wis., holds a major col-lection of wood-rotting species. Major culture collectionsmaintain \Veb sites with information about holdings andinstructions about ordering. As with bacterial and viralstrains, a fee is usua[y charged for obtaining cultures.

ln the laboratory, fungi and bacteria are treated simi-larly. They can be grown on agar rnedia in petri plates orin liquid broths. Depending on the nutritional require-ments of the individual species, either a complex or definedmedium is used. Many fungi prefer media rvith acidic pH.On petri plates, molds are readily distinguished from mostbacteria because thev usuallv form drv aerial colonies thatmay be brightly colored due to the pigmentation of theirspores. With the naked eye, yeast colonies are nor so easilydistinguished from bacteria, but under the light micro-scope, their large size, compared to any run-of-the-mill pro-karyote, is easy to discern. Recipes for common andspecialty media for cultivating fungi are available in My-cology Guidpbook ( 155 ) and Handbook of Microbiologlcalltl.e-dia (15). ln isolating fungi from nature, antibiotics, such asstreptomycin, or other bacterial growth inhibitors, such asrose bengal, are frequently added to media, thereby selec-t ivcly enhancing the growth of fungi (119).

When isolating cuiturable microorganisms from naturalsubstrates, it is relativcly easy tc-r obtain a colony countbased on the unicells of typical bacteria. Sampling for fungiis much harder due to their {ilarnentous growth habit.There may be a large mass of fungal m1'celium present, butthe methods adapted frr-rm bacteriology may not detect it.

87. Use of Funs i in B iodesradat ion I 961

Moreover, dormant ftrngal sp()res may prrlduce nlllnerouscolonies ri'hile thri'u'ing nonsporulating colonies may notbe recovered at al l . ln l ic luid shake culture, many f i lamen-tous ftrngi form pellets, thus rnaking direct turbidity assaysimpractical and making dry weights the most cornmonlyused measure. in batcl'r culture, the synthesis of m:rny fun-gal proclucts and en:ymes is not correlated with growth butis triggerecl by the lin-rit:rtion of an essential nutrient. Theterms "trophophase" and "idiophase," roughly comparableto bacterial log phase and stationary phase, respectively,havc been used to describe {ilamentous growth. Bothsecondary-metabolite production and the ligninolytic-enzyme production are correlated u'itl-r idiophase.

Enrichment cultures arc a classical microbiological tech-nique, commonly used ftrr hnding a specific microbe to de-grade a certain toxic waste. Enrichment cultures favor thegrowth of a particular species basecl on its nutritional re-quirements. h-r the most colnmon application of thismethod, aliquots of rvater, soil, leaf litter, or other mixedinocula arc placed into a medium containing the targetedcornpound as the sole carbon source. Only organisms withdegradative ability will grow. In liquid cttlture, competitionfor the substrate will leacl to enrichment of the microbialstrain that is able to grorv fastest. On petri plates, coloniesrepresenting many species are usually isolated; these arethen subcultured and tested further. With ferv exceptions,this approach leads to the isolation of bacteria. In general,fungi are slower growing and produce fewer propagules thando bacteria. In addition, fungi are less likely than bacteriato have the capracity to use xenobirttics as sole carbonsources. Many fungi need a supplemental carbon source tosustain growth, i.e., their tlegradative potential is cometa-bol ic.

Thus, the key to successftrl isolation of fungi for xeno-biotic clegradatic-rn is trvofcrld: (i) the recognition that fungiare easily outgrown by bacteria and (ii) the recognitionthat they produce many potent biodcgradative enzymes ca-pable of degrading toxic pollutants yet do not use thesebreakdon'n proJucts to sustain growth. To successful ly iso-late fungi with potential for bioremediation, it is necessaryto impose imaginative enrichment conditions, includingthe careful selection of supplementary carbon sources andbacteriostatic agents.

Serving as a manual to both methods and references,volume 4 of Method.s in Microbiologl Q4) is specilically de-voted to distinguishing mycological and bacteriologicalperspectives. Specialized techniques for collecting, isolat'ing, cultivating, manipulating, and preserving fungi aregiven. lndividual chapters are devoted to soil fungi, airs:rrnpling, and aquatic organisms. Although several decirdesold, this book is still a wonderful resource. See also Tech'niques in Microbictl Ecology (7 4), Mycology Guidebook (155),

and chapters 6, 35, and 49 for guidance on the specialhandling of fungi. Other valuable references concentratingon applied mycology are Arora et al. (13), Smith and Berry(151 , l 5 / ) and Smi th e t a l . ( 153 ) .

DEFINIT IONS AND DISTINCTIONSBiodegradation, mineralization, bioremediation, biodeter-ioration, biotransformation, cometabolism, and bioaccu'mulation are terrns not ah,vays used with appropriatesensitivity to their subtle diff-erences in meaning. The spe-cial role played by fungi in nature and in the human ex-ploitation of their often unique metabolism can be clarihed

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962 T BIOTRANSFORMATION AND BIODECRADATION

by thinking about the distinctions implied in this ecolog-ical lexicon.

"Biodegradation" is the biologically mediated break-down of chemical compounds. It is an umbrella term, en-compassing most of the other jargon addressed in thissection, and generally implies a series of biochemical re-actions. \Vhen biodegradation is complere, the process iscalled "mineralization," i.e., the total breakdown of organicmolecules into water, CO2, and/or other inorganic endproducb. Not all authors are careful to disringuish betrveendegrees of biodegradation; some use the term to describealmost any biologically mediated change in a substrare, andothers use it to describe mineralization (9).

"Biotransformation," a rvord often used synonymouslyvi'ith "bioconversion," usually refers tc-r a single step in abiochemical pathway, in which a molecule (the precursor)is catalytically converted into a different molecule (theproduct). Many biotransformations in sequence constitutea metabolic pathway. Industrial processes frequently incor-porate biotransformation reactions. A famous example is inthe manufacture of steroids for birth control pills (141).When ecologists describe biotransformation, the environ-mental status of the transformed product is a primary con-sideration. Is it more water soluble and thus more easilyexcreted by the cell? Is it less toxic/ Is it more hazardousthan its precursor? \7hen relatively innocuous precursorsare converted into more toxic products, the process iscalled "activation." The metabolic activation of mercury isa il'ell-kno\,vn example of a biotransformation with malignenvironmental imnact.

"Biodeterioration" and "bioremec-liation" are the two as-

pects of biodegradation rvith an anthropomorphic empha-sis. Biodeterioration is the breakdorvn of economicallvuseful substances. Often the term is used narrowly to referto the deterioration of substances that are normally resis-tant to biological attack such as metals, plastics, drugs, cos-metics, paintings, sculpture, wood products, electricalequipment, fuels and oils, and other economically valuableobjects (147).

in bioremediation, biological systems are used to trans-form and/or degrade toxic compounds or otherwise renderthem harmless. Bioremediation can involve indigenousmicrobial populations with or withour nurrienr zupple-mentation, or it can involve inoculation of exogenousorganisms into the site. When exogenous organisms areadded, the process is called "bioaugmenrarion."

In eithercase, the goal is to disarm noxious chemicals without thefornration of ncw toxins.

"Bioaccumulation," sometimes used loosely synony-mously with "biosorption," is the concentration of sub-stances without any metabolic transformarion. Both livingand dead cells may be involved. Bioaccumulation tech-niques can be used to concentrate metals such as copper,lead, silver, uranium, and certain radionuclides from aqu.-ous environments, anJ the resultant loaded biomass can herecycled or contained.

The term "cornetabolism" is used in two senses. Usuallv.

it describes the situation where an organism is able to bio-transform a substrate but is un:rble ro qrow on it. As definedby Horvath, "Co-metabolisrn

refers toany oxidarion of sub-stances rvithout utilization of the energy derived from theoxidation to supporr microbial growrh" (BB). The phenom-enon has also been called "cooxidation"

and "qratuitous"

or "fortuitous" merabolisrn. Many biochemists disl ike the

term (67, 89). Nevertheless, i t has becone well entrenchetlin the l i terature.

A second meaning of cometabolism is to describe thedegradation of a given compound by the combined effortsof several organisms pooling their biochemical resources formutual efforts (41).

THE FUNGAL WAY OF DEGRADATIONThe organisms known as fungi, encompassing both Fungiand Stramenopila, share a unique nutritional strategy, i.e.,their cells secrete extracellular enzymes which break downpotential food sources, which are rhen absorbed back intothe fungal colony. This way of life means that any discus-sion of fungal biodegradation must cover an extraordinarvamount of catalytic capability. The decomposition of lig-nocellulose is probably the single mosr imporranr degra-dative event in the Earth's carbon cycle. The utilizationand transformation of the dead remains of other organismsis essential to the Earth's economy. An enormous ecologicalliterature exists on the role of fungi as primary and sec-ondary decomposers in these classic "cycles" of nature (see,for example, references 8, 3I,36, and 60).

From the human perspective, the power of fungal en-zymes is Janus-faced. Molds destroy more food than anyother group of microorganisms. They damage standing tim-ber, finished wood products, fibers, and a wide range ofnoncellulosic products such as plastics, fuels, paints, glues,drugs, and other human arrifacrs (48, l4Z). On the otherhand, many of the oldest biotechnological pracrices arealso based on fungal catalytic power: baking, brewing, winefermentation, production of certain cheeses, and the kojiprocess are ancient examples of the way humans have em-ployed fungi for their own benefit. In the 20th century,numerous hydrolytic enzymes involved in the degradationof relatively simple biopolymers such as starch and proternhave been purilied, characterized, and utilized within in-dustrial settings. These include fungal amylases, gluco-amylases, lipases, pectinases, and proteases (see references19 and 72 for reviews). Fungal cellulases provide a goodexample of the contrasting faces of a single enzymatic ca-pability. During World War ll, research by the U.S. Armyon the rnicrobial destruction of military clothing and tentsled to the characterization of the cellulolytic mold Tricho-derma reesei. Continuing research on T. reesei identified acomplete set of cellulase enzymes required for the break-down of cel lulose to glucose (128, 139). These enzymesnow prornise the potenrial of converting waste cellulosicsinto foods for our burgeoning population and have beenthe subject of intense molecular biology research (51,173).Although cellulase-produced glucose is not yet economi-cally competitive, anorher traditional fungal process rs:mushroom cult ivat ion on l ignocel lulose (34, 154). Theseand some other examples of economically advantageoususes of fungal biodegradation are displayed in Th-b le 1 .

Fungi are also good at bioaccumulation of metals. Manyspecies can adsorb cadmium, copper, lead, mercury, andzinc clnto their rnycelium and spores. Sometimes the wallsof dead fungi bind better than living ones. Systems usingRhiloprzs arrhizus have been developed for treating uraniumand thorium (161). Spent fungal biomass from industrialfermentations is an available resource for the concentrationof heavy-rnetal conramination (62, 63, I44).

What about fungal degradation of pollutants and toxicwastes? In some cases, traditional methods are beineadopted for contemporary needs. For example, compostinghas been used to rrear borh pesricides (59) and munit ions

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BZ. Use of Fungi in B iodegradat ion t 963

TABLE 1 Econonrically benehcial examples of fungal degradation

Process Substrate Species Rerrresentative citations

Composting

Mushroom cultivation

Single-cell proteinproduction

Sol id-rvaste treatrnenr

\Tastervater treatment

Straw, rnAnure, agricultural waste,bark

Lignocellulose, anirnal manure

Strarv, sawdust

Wood logs

Alkanes

Brewery wastes, molasses

Sulfite rvaste liquid

Sludge/sewage

Pulp and paper mill e{lluent

Disti l lery waste

Kraft bleaching effluent

Tannery effluent

Consortia of bacteria and fungi, usuallyuncharacterized

Agaricus bisporus

Pleurotus ostreatus (oyster mushroom )

Itntinus odoide s ( shiitake )

Yeasts, e.g., Candi&t tropicalis

Saccharomy ces cerevisiae, S. carlsbergensis

Candidn wilis, P aecilom)ces varioti

Consortia of bacteria and fungi, usuallyuncharacterized

Coriolus ver sicolor, Phrtnerochaetechrysosporium

Yeasts, especially Candi&t utilis

P hnner o chne te chr y s o s p orium

A-spergllas, P enicillium

z l , 55

3 4 , 8 4r54154

42, 100rr4rr4

7'7 lO

106, 107

6 l49rz7

wastes (169). There is also rather a lot of descriptive bio-chemistry concerning the ability of various fungi and theirenzymes to biotransform pesticides (see reference 138 forenzymes ancl reference 150 for lists of speci{rc compoundsand organisms), but, to date, the most sophisticated fungalapproaches to environmental clean-up have grown out ofprior research on degradation of petroleum hydrocarbons(16, 37, 66) and on the adaptation of research on fungaltreatment of lignocellulytic wastes in the pulp and paperindust ry ( i06, 107, 109) .

The ability to grow on petroleum hydrocarbons is rvide-spread among the fungi (14,33,66). Jet crashes caused byblocked fuel lines due to the growth of Cladosporium resi-nne, frrst reported during World

'!Var Il, are among the

more dramatic negative consequcnces of the abi l i ty of fungito thrive in extreme habitats (113). Considerable infor-mation is available about the mycological flora associatedwith marine petroleum spills (33). On the industrial side,the years of research on single-cell protein, instituted withthe goal of turning petroleum hydrocarbons into feed, havepaid off in the study of the enzymatic mechanisms used byyeasts and other microorganisms in the biodegradation ofpetroleum wastes for environmental remediation (100,140). Cytochrome P-450s are mixed-function oxidases(monooxygenases), derived from a superfamily of genes,which are involved in many steps of petroleum degradationand in the biotransformation of a variety of environmentalpollutants ( 166). Both detoxification and activation are as-sociated with the action of P-450. Fungal monooxygenasesare more similar to mammalian than to bacterial cyto-chromes; Sariaslani (146) has presented a particularly thor-ough review of these enzymes, and Kellner et al. ( 10i ) havediscussed their use in bioremediation. Extensive biochem-ical and genetic data are available for several yeasts; thereis also a large literature surrounding the aseptate filamen-tous species Cunninghamelln elegans (33, 66).

Similarly, and to an even greater extent, research onpulp waste treatment, such as the decolorization of effluentfrom kraft pulp mills, and the subsequent mushrooming ofresearch on rvhite rot fungi have shown the power of rvoocl-

decaying species against a surprisingly largc battery of en-vironmental contaminants (79, 58). Recent advances inthe use of fungi in environmental remediation and bio-technology have been summarized by Paszczynski andCrarvford (137).

PHAN EROCHAETE CH RYSOSPORI U MPhanerochaete chrysosponum is a higher basidiomycete be-longing to the white rot group of fungi. P. chrysosporium isthe best studied of the ligninolytic fungi, a group whosenatural habitat is forest litter and rotting wood. White rotfungi are unique among eukaryotes in having evolved non-specific mechanisms for degrading lignin.

Lignin is unlike many natural polymers in that it con-sists of irregular phenylpropanoid units linked by nonhy-drolyzable carbon-carbon and ether bonds. Lignin containschiral carbons in both the L and n configuration, and thisstereo irregularity renders it still more resistant to attackby most microorganisms. Nevertheless, many extracellularligninolytic enzymes produced by white rot fungi can cat-alyze the breakdown of lignin.

Under conditions of nitrogen, sulfur, and/or carbondeprivation, P. chrys osporium produces families of lignino-lytic enzymes (54, 68, 160) including lignin peroxidase(L iP) (EC 1.11.1.12) (160) and manganese-dependent per-ox idase (MnP) (EC 1.11.1.13) (69) . The perox idases usehydrogen peroxide generated by glyoxal oxidase, glucoseoxidase, and cellobiose oxidase to promote the oxidationof lignin to free radicals that then undergo spontaneousreactions with oxygen or water, which leads to depolyrner-ization. The depolymerization of lignin by nonspecificextracellular peroxidases is sometimes called enzymaticcombustion (108). Both LiP and MnP are encoded by fam-ilies of structurally related genes that have been cloned andsequenced (for reviews, see references 7, 25,40, and 87).These genes are differentially regulated in response [o avariety of environmental signals, especially starvation (91).

During the 1980s it became apparent that P. chryso-sporium, in addition to degrading lignin, is capable of

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964 I BIOTRANSFORMATION AND BIODECRADATION

degrading a wide variety of xenobiotics. Polyaromatichydrocarbons, chlorinated phenols, nitroaromatics, dyes,and many other environmental toxins have been biotrans-formed or mineralized by P. chrysosporium, sometimes incomplex mixtures of xenobiotics (Table 2). The ability todegrade such a broad spectrum of highly toxic and gener-ally recalcitrant substrates is unusual for a single species. Itis often assumed that this broad-spectrum xenobiotic bio-degradation is effected by the same extracellular enzymesused in lignin degradation. In addition, a variety of otherfactors are thought to contribute, such as intracellular en-zymes (e.g., reductase, methyltransferases, and cytochromeP-450 oxygenases), "plasma membrane potentials," andbioabsorption onto mycelia (17, 99, 163, 164). Postulatedmechanisms used by the white rot fungi to degrade pollut-ants have been summarized by Barr and Aust (17).

In the laboratory, most of the successful mineralizationexperiments have been conducted under ligninolytic con-ditions using rvhole ceils in liquid culture. Moreover, pu-ri{ied preparations of lignin peroxidases are capable ofoxidizing a variety of the xenobiotics known to be miner-alized by whole cell cultures of P. chrysosponum (e.g.,7,(-dinitrotoluene, lignite, polyaromatics, pentachlorophenols,and dichlorodibenzo-p-dioxin, pyrene), although they arenot involved in others (".g., DDT [1,1,1-tr ichloro-2,2-bis(4-chlorophenyl)ethanel) (85, 86, 110). On the otherhand, many questions remain unanswered. In one study,the disappearance of 2,4,6-trinitrotoluene (TNT) beganprior to the onset of ligninase activity, while secondaryproducts were formed after the appearance of LiP and MnP(78). In another study, P. chrysosporium removed phenan-threne under both ligninolytic and nonligninolytic condi-t ions (43) .

To recapitulate, among filamentous fungi, P. chrysospor-izm has become a model system for studying xenobioticdegradation. A critical assessment of its potential as a bio-remediation tool has been given by Paszczynski and Craw-ford (131), who point out rhar the field applications havebeen unpredictable and that even under ideal laboratory

conditions many contaminants are only partially brokendown. In some cases, envlronmentally undesirable break-down products are formed. In addition, many theoreticalquestions remain about the biochemical activities of P.chrysosponum in nature and the relationship between theenzymes of lignin degradation and the rnechanisms of xe-nobiotic removal. In practice, the application of P. chry-sosporium to contaminated habitats has been hampered bythe fact that its natural habitat is not soil. Notwithstand-ing, the successes of P. chrys osporium in laboratory biodeg-radation studies ensure that intensive research on thisspecies will continue. These successes have also stimulatedquests for other filamentous fungi with the porential fordegrading xenobiotics.

wooD ROTS, LTTTER ROTS, AND OTHERFILAMENTOUS FUNGIThere are more than 1,500 different species of white rotfungi. In addition, there are thousands of orher fungal spe-cies loosely categorized as brorvn rots, dry rots, litter rors,soft rots, mycorrhiza, terricolous, and so fcrrth. Most ofthese species have never been studied in the laboratory andrepresent a large potenrial for biodegradation research. Inrecent years, several groups have done comparative studiesof white rot fungi with the expectarion of linding betterl ignin-degrading sysrems (45, 46,136). Others have takenadvantage of this resource by screening isolates fromculture col lect ions and natural habitars against a varietyof pollutants. Many new species with bioremediarion po-tential have been identi l ied (58, 118, 170). In a num-ber of cases, these fungi show more practical promise thanP. chrysosporium since their growrh strategies offer bettersustainability in natural habits; for example, they do notrequire constant additions of wood or orher substrates (73).ln addition, their enzymaric reperroires offer fresh ap-proaches to xenobiotic degradation. In the survey byGramss et al. (71), 58 species from differenr physioecol-

TABLE 2 Examples of xenobiotics degraded or transformed by P. chrys osporium

Type of compound Exarnples Reference(s)

Aromatic hydrocarbons

Chlorinate..l organics

Nitrocen aromatics

Benzo[a]pyrene

Phenanthrene

Pyrene

Alkyl halide insecticides

Atrazine

Chloroanilines

DDTPentachlorophenols

Tiichlorophenol

Polychlorinated biphenyls, Aroclor

Polychlorinated dibenzo-p-diox ins

Trichlorophenoxyacetic acid

2,4-Dinitrotoluene

TNTHexahydro- 1,3,5-tr ini tro- 1 ,3,5 -tr iazine

Dyes

752 7 , r 7 5 , 1 5 776

103rz6l l

2 8 , 1 1 0

lll, 172

99

44, 47

70 ,76 , 164

r45

t62<'7

56

39, 130, 134,135Miscellaneous

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ogical groups (wood degrading, woocl and straw degrading,terricolous, ectomycorrhizal, and mitosporic) were grownin liquid cultures and tested against a battery of polyaro-matic hydrocarbons. On average, wood-degrading speciesrvere best at metabolizing polyaromatic hydrocarbons, butcompetent fungi were found in all five groups. Polyaromatichydrocarbon conversion was correlated rvith the produc-t ion of MnP, peroxidase, and laccase (71).

Two particular white rot species that have received con-siderable attention are Pleurotus ostreatus and Tiametes uer-sicolor. They are both efficient at mineralizing polyaromarichydrocarbons (20, 165) and at degrading polychlorinatedbiphenyls (174).P. ostreatu.s is better able to colonize soilsthan P. chrysosporium (129), and although it is a successfullignin-clegrading species, it does not exhibit LiP acriviry(77). P. ostre&tus does, however, produce several laccaseisoenzymes encoded by families of laccase genes (64, 65).Laccase (p-diphenol-dicrxygen oxidoreducrase [EC1.10.3.21) is a member of the "blue copper oxidase" family( 104, 159, 172). Laccases oxiclize subsrrares by one-elecrrontransfer steps and are active against lignin model corn-pounds in the presence of mediators (93, 116). Many phe-nols and chlorophenols are transformed by these enzymesto radicals that subsequently undergo spontaneous poly-merizations. Laccase-mediator combinations also showactivity against acenaphthene, acenapthylene, andanthracene (94,95). a puri f ied laccase isolated from T.uersicolor could oxidize a variety of polyaromatic hydrocar-bons in vitro, including anthracene, benzo[a]pyrene, fluor-anthene, and chrysene (115). In addit ion to laccase, anenzyme with properries of both LiP and MnP has beenisolated from species of Pleurotus and Bjerknndera. This"third type" of lignin peroxidase shares catalytic propertiesof MnP (eflicient oxidation of MnZ* ro Mnr*) and LiP(oxidarion of lignin model dimers) and has a high affinityfor substituted hydroquinones (171, I47).

A representarive list of filamentous fungi with the abil-ity to degrade xenobiotics is presented in Table 3. Cell-freestudies with enzymes from some of these species have beenconducted. For example, a cell-free sysrem of the MnP ofthe white rot fungus Nematoloma frowardii is capable ofmineralizing pentachlorophenol, carechol, and pyrene. Theratio of MnP activity to rhe concentration of reduced glu-tathione affects the extent of mineral izarion (85).

Brown rot fungi degrade the cellulose and hemicellulosecomponents of rvood, leaving a residue of modified ligninthat is dark brown. Although they are enormously destruc-tive of rvood produc$, the mechanism of wood decay bybrown rot fungi has received far less attention than that ofwood decay by white ror fungi (173). l t is bel ieved thatthe early steps in brown rot decay are nonenzymaric. Earlystudies demonsrrate that the cellulose in wood can be de-polymerized by Fenton's reagenr [H2O2 plus Fe(ll)], andmost contemporary models invoke a Fenton-type extracel-lular system that produces hydroxyl radicals or-other pow-erful oxidants thar then attack the wood components (72).Different mechanisms proposed for hydroxyl radical pro-duction by brorvn ror fungi have been reviewed by Hydeand Wood (90). In studies on Gloeophyllum nabeum, 4,5-dimethoxycatechol and 2,5-dimerhoxyhydroquinone havebeen implicated as electron transport carriers to Fenton'sreactions ( 133). The ability of brown rors to degrade xeno-biotics is a relatively new avenue of research. Cirrent stud-ies have implicared two species of Gloeophyllum in thedegradatit-rn ,rf chlorophenols (52, 149), and G . trabeum isactive against polyethylene glycol (105) and ciprofloxacin,

BZ. Use of Fungi in B iodegradat ion I 965

a f luoroquinolone anribioric (167).No doubt many orherinteresting brown rot species will be found to demonstrareactivity against a spectrum of xenobiotics.

MYCOREMEDIATIONMany rvorkers divide bioremediation strategies into threegeneral categories: (i) the target compo,,.rd is used as acarbon source, (ii) the rarger compound is enzymaticallyattacked but is not used as a carbon source (cometabolism),and (iii) the target compound is not metabolized at all butis taken up and concenrrated within the organism (bioac-cumulation). Although fungi parricipare in all three srrat-egies, they are often more proficient at cometabolism andbioaccumulation than at using xenobiotics as sole carbonsources.

The attributes that distinguish filamentous fungi fromother life-forms determine why they are good biodegraders.First, the mycelial growrh habit gives a comperirive advan-tage over single cells such as bacteria and yeasts, especiallywith respect to the colonization of ir-rsoluble substrates.Fungi can rapidly ramify through subsrrares, literally di-gesting their way along by secreting a battery of extracel-lular degradative enzymes. Hyphal penetrarion provides amechanical adjunct ro rhe chemical breakdown effected bythe secreted enzymes. The high surface-to-cell ratio char-acteristic of filaments maximizes both mechanical andenzymatic contact with the environment. Second, theextracellular nature of the degradative enzvmes enablesfungi to tolerate higher .o.,...,i.rtions of toxic chemicalsthan would be possible if these compounds had to bebrought into the cell. In addition, insoluble compoundsthat cannot cross a cell membrane are susceptible to attack.Fungi even solubilize low-rank coal, a parricularly persis-tent, irregular, and complex polymeric substrate, althoughthey do so slowly (33,53,132). Final ly, since the relevantenzymes are usually induced by nutritional signals indepen-dent of the target compound during secondary metabolism,they can act independently of the concentration of thesubstrate, and their frequently nonspecific nature meansthat they can act on chemically diverse substrates.

Among filamentous fungi, Phanerochaete chrysosporiumhas emerged as the model sysrem for studying xenobioticdegradation. A great deal remains ro be learned about thefundamentals of how this lvhite rot fungus mineralizes pol-lutants; not surprisingly, even less is known about the deg-radative mechanisms used by fungi in general. Oxidativeenzymes play a major role, but organic acids and chelatorsexcreted by the fungus also contribute to the process. Manyof the toxic chemicals mineralized by fungi are alreadyhighly oxidized. The ability of fungi to lower the pH oftheir environment appears to be involved in the reductionof some of these compounds (17).

What about the futurel Various brown rots, litrer rors,aquatic fungi, anaerobic fungi, and mycorrhizal fungi, inconjunction with pollutant-tolerant plants, all provide op-portunities for new research. Genetic engineering is an-other frontier. Fungal genes for degradative enzymes can beadded to bacteria; alternatively, comperent fungi can bemodilied to grow in an extended range of environments.For example, several groups have investigated the recom-binant expression of fungal peroxidases in order to facilitatelarge-scale commercial production of these enzymes. LiPand MnP have been produced in an Aspergillus niger hostand in the insect bacr-rlovirus expression system, althoughthe LiP was not active (35, 96). Another development is

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966 T BIOTRANSFORMATION AND BIODECRADATION

TABLE 3 Representative xenobiotic-degrading filamentous fungi

Group Species Substrate(s) Reference(s)

White rot fungi

Mycorrhizal fungi

Others

Agroc.^tbe aegarita

Agrocybe praecox

Clitocybula duseni

Coriolopsis gallica

Dichomitus squabns

Doedoela quercina

Ganodtrma applarwtum

Hypholoma fascicukne

Kuehner omy c e s munbili s

Itntinus edodes

Itnzites betulina

Nemntoloma frowardii

Pleurotus dryinus, P. eryngii,P. fuscul^otns, P. flabellntus,P. pulmonnius, P. sajor-caju

P 1 cnop or u s cinnab annu s

S tr opharia r u go s o annulntn

Trametes hirsuta.

Morchella conica

Tylospcno fibrilnsa

Agaricus bisporus

Copinus comatus

Crinipellis stipinna

Glaeophyllum striatum

G. trabeum

Marasmiellus tToJonus

M. rotuln

Benz[a]anthracene

Phenanthrene, pyrene

Lignite

Anthracene, phenanthrene, pyrene

Benz[a]anthracene

Benz[a]anthracene

Benz[c]anthracene

Anthracene, fluoranthene, pyrene

Anthracene, fl uoranthene,phenanthrene, pyrene

Benz[a]anthracene

Anthracene, phenanthrene

Dinitrotoluene and trinitrotoluene,lignite coal, pentachlorophenol

Benz[a]anthracene

Dibenzofuran

Anthracene, fluoranthene,phenanthrene, pyrene

Textile dyes

Anthracene, fluoranthene,phenanthrene

Fluorobiphenyl

Anthracene, fluoranthene,phenanthene, pyrene

Anthracene, fluoranthene,phenanthrene, pyrene

Pyrene

Dichlorophenol

Pentachlorophenol

Benzo[a]pyrene

Pyrene

1 1 8

7 1

86

r371 1 8

1 1 8

i 1 8

7 r7 r

1 1 8

7 I85, 96, 149

1 1 8

9 7 , 1 1 8

7 1 , 1 1 9

1

7 r

73

7 r

7 r

r1752r49l7rll7

that of large-scale DNA sequencing. As this review is beingcompleted, the genomic analysis of white rot fungi is beinginitiated. The U.S. Department of Energy is using a whole-shotgun approach to sequence the genome of P. chrys-osponum (D. Cullen, personal communication). Theavailability of DNA sequence data for the model white rotfungus, coupled with the capacity to build DNA microar-rays for transcriptional profrling and gene discovery, willprovide powerful tools for identifying genes for hithertoundiscovered degradative enzymes from other filamentousfungi.

As we get better at recognizing what can and cannotbe done with bioremediation, we will create a menu ofchoices using a broad range of organisms. In some situa-tions, bioconcentration of a toxic waste is the best we cando. ln others, the nonspecificity of the white rot fungi isideally suited to treating low concentrations of mixedwastes in a nutrient-deficient habitat. ln vet others. anaer-obic bacteria are clearly the best candidates. Microbiolo-gists know that pure cultures are rare in nature. Commonsense tells us that in the real world, complete pathways of

degradation are more likely to occur through the combinedeffects of many organisms. For example, cocultures of thebacterium Stencttrophomonns maltophilia and the fungus Pen-icillium j anthinellum degrade high-molecular-weight poly-cyclic aromatic hydrocarbons more efficiently than doeseither microorganism alone (73),

Judicious combinations of chemical and physical pro-cesses with biological schemes also offer promise. Filamen-tous fungi, yeasts, and nonphotosynthetic bacteria are theworkhorses of biological degradation. Therefore, it is ironicthat the popular press has chosen the word "green" to de-scribe environmentally friendly technologies such as bio-remediation. Decidedly not green in color (except for a fewspore types) and most certainly underappreciated (even bymost microbiologists), the fungi possess the most variedand most efficient battery of depolymerizing enzymes of alldecomposers. When joined with their bacterial brethren incooperative catabolism, fungal-bacterial consortia will fos-ter the ecological recovery of contaminated habitats world.u'ide. Filamentous fungi will always be major players in the"greening" of toxic \r'aste sites and other polluted habitats.

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Recent research in the laboratorl of J .W.8. has been supported b1

o grant from Exxon Corp. B.F.D . is supported by the NASA Asrro'

biology Program.We thank Jason Beadle and Sara Clttrk for mnnuscript preparation

and Tnna Loomis and Jennifer Liu for help with the Iiterautre rec)rcw.

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