Fungal Degradation of Polycyclic Aromatic Hydrocarbons

Home , Cunninghamella elegans

Available online at www.ijpab.com Al-Hawash et al Int. J. Pure App. Biosci. 6 (2): 8-24 (2018) ISSN: 2320 – 7051 DOI: http://dx.doi.org/10.18782/2320-7051.6302 ISSN: 2320 – 7051 Int. J. Pure App. Biosci. 6 (2): 8-24 (2018) Research Article

Adnan B. Al-Hawash1, 2, Jawadayn T. Alkooranee3, Xiaoyu Zhang1 and Fuying Ma1* 1Key Laboratory of Molecular Biophysics of MOE, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan 430074, China 2Ministry of Education, Directorate of Education, Basra 61001, Iraq 3College of Agriculture, University of Wasit, Iraq *Corresponding Author E-mail: [email protected] Received: 3.03.2018 | Revised: 29.03.2018 | Accepted: 2.04.2018

ABSTRACT Polycyclic aromatic hydrocarbons (PAHs) are two or more rings of benzene fused with both natural and anthropogenic sources. PAHs are to a large degree distributed contaminants of environmental that have detrimental biological effects, carcinogenicity toxicity, and mutagenicity. Because of their ubiquitous occurrence, bioaccumulation potential, recalcitrance and carcinogenic activity, the PAHs have compiled significant environmental concern. The PAHs may undergo volatilization, photolysis, adsorption, and chemical degradation. The microbial degradation is the main degradation process, numerous of fungi metabolize PAHs by using enzymes that include laccase, lignin and manganese peroxidase, as wall as cytochrome P450 and epoxide hydrolase. The enzymes of fungi implicated in the PAHs degradation, the fungal lignolytic enzymes are laccase, lignin and manganese peroxidase, those fungi extracellular and stimulate radical formation through oxidation to destabilize bonds in a molecule.In this review explains the biodegradation potential of ligninolytic and non-ligninolytic fungi to PAHs and also shows known conversion pathways. Key words: Fungi, Polycyclic Aromatic Hydrocarbons, Biodegradation , Metabolize, Enzymes

Highlights ●The enzymes of fungi involved in the PAHs degradation

● The microbial degradation can be considered as a key element to PAHs remediation

INTRODUCTION bioremediation is intended to convert organic Microbial degradation is a viable technique for contaminants into non-harmful metabolites or bioremediation of organic contaminants. It has mineralization of pollutants to water and long been known that microorganisms carbon dioxide1,2. Effective remedial environmental contaminants of degrade in technology requires that microorganisms be diverse matrices and environments. In process able to adapt quickly to the effective utilizes of of bioremediation uses the metabolic diversity contaminants of interest in a given situation of microorganisms to degrade hazardous within a reasonable time. contaminants. The technique of

Cite this article: Al-Hawash, A.B., Alkooranee, J.T., Zhang, X. and Ma, F., Fungal Degradation of Polycyclic Aromatic Hydrocarbons, Int. J. Pure App. Biosci. 6(2): 8-24 (2018). doi: http://dx.doi.org/10.18782/2320-7051.6302

Al-Hawash et al Int. J. Pure App. Biosci. 6 (2): 8-24 (2018) ISSN: 2320 – 7051 Numerous factors affect microorganisms to their solubility in the water and vapor pressure utlize contaminants as substrates or co- decreases, while melting and boiling point metabolize them. For understanding the both increases5. PAHs fate in the environment pathways of catabolic and responsible includes adsorption on soil particles, chemical enzymes is an effective way to identify oxidation, volatilization, photo-oxidation and significant factors for effective cleaning of leaching6. Those compounds are tough to contaminants. Studies have been conducted to degrade in the natural matrices and also their understand the biological treatment of the persistence increases much with their environmental contaminants such as molecular weight. Moreover , PAHs represent Polycyclic aromatic hydrocarbons (PAHs), a significant concern because of their which are among the most widespread and widespread existence in environment, their persistent environmental contaminants. PAHs potential to accumulate, and their resistance are consist of two or more intensive aromatic towards biodegradation and their carcinogenic rings of carbon and hydrogen atoms; rings are and mutagenic impacts that occur by connected together in angular and linear breathable air containing PAHs in the arrangements. Due to their large negative workplace, or through coming in contact with resonance energy, they chemically stable at water, air, soil nearby hazardous waste sites or ambient temperature, because of their via drinking polluted milk or water etc.7. hydrophobic structures, and almost highly Potential treatments have performed to restrain lipophilic or completely insoluble in water3. further economic consequences and Low molecular weight (LMW) PAHs such as deterioration of water and soil quality. The naphthalene, that two six-membered rings; process of bioremediation promise to deliver fluorine, acenaphthene acenaphthylene and long lasting with low cost solutions to biphenylene, thta two six-membered rings and degradation of PAHs. Possible treatments have a four- or five-membered ring; and anthracene performed to prevent further economic and phenanthrene, that three six-membered consequences and degradation of water and rings. High molecular weight (HMW) PAHs soil quality. Biodegradation of petroleum such as, pyrene, chrysene, benza, anthracene hydrocarbons was done via bacteria, fungi and and fluoranthene, that four rings; alga8,10. According to the results of numerous benzo[a]pyrene, benzo[e]pyrene perylene, and researchers over the years, the fungi protrude dibenza,h, anthracene having five rings; and the as a powerful choice to PAHs degradation. others having six or more rings, Table 1. Fungi have characteristics over bacteria Despite, PAHs are present in petroleum and because their ability to grow into a large coal, the main modern source to PAHs is the spectrum of substrates and meanwhile, they incomplete combustion of organic matter from produce intracellular and extracellular sources e.g., cars, coal fired power plants, enzymes, which can break through the forest fires and home heating furnaces4. PAHs contaminated soil and remove the petroleum are produced when petroleum products, coal, hydrocarbons11. Therefore, many factors must wood, old tires, urban solid wastes are burned. to be taken into consideration due to affect Also, other PAHs sources include oil their in the rate of PAHs biodegradation refineries, steel mills, coke ovens, aluminum includes oxygen, temperature, accessibility for plants coal and gasification plants. spills of nutrients, and optimum conditions of enzyme crude oil from drilling, pipelines and like pH, cellular transport properties, chemical supertankers that deposit huge amounts of structure for compound and chemical PAHs on the ocean and soil. PAHs are occur partitioning into growth medium12. The rates as colorless, white and pale yellow solids, low of PAHs biodegradation are highly related to solubility into water, high boiling and melting conditions of the environmental for the activity points and lower vapor pressure as shown in of enzyme and also to the growth of fungal. Table.1. In an increase of molecular weight, Biodegradation is a very broad field and Copyright © March-April, 2018; IJPAB 9

Al-Hawash et al Int. J. Pure App. Biosci. 6 (2): 8-24 (2018) ISSN: 2320 – 7051 encompass the use of a wide range of oxidized, however, via cytochrome P450 microbial to break down chemical bonds. In monooxygenases in the liver of mammalian. fact, fungus is implicated in three main types The products are ordinarily water soluble of hydrocarbon metabolism, each with its compounds that are excreted, But little of the distinct characteristic. Partial transformation metabolites probably be genotoxic compounds reactions, complete degradation of that form adducts with DNA15. Studies with hydrocarbons in the presence of second animals have shown the ability of many other compatible substrate and independent use of PAHs to cause cancer. The exposed of hydrocarbons as a carbon source to energy .the workers to industrial processes that released present review is focused on fungal metabolize PAHs have also been exposed to high bladder pathways of some polycyclic aromatic cancer and lung cancer, and some PAHs have contaminants under aerobic conditions of anti-estrogenic or weak estrogenic impacts16. culture. Dibenza,h,anthracene was showed to cause skin 2. PAHs Toxicity tumors to mice, and also benzo[a]pyrene was PAHs are widespread contaminants, some of proved to be more carcinogenic. Other studies which have found to be genotoxic, cytotoxic, have found that mammalian carcinogens are carcinogenic, or ecotoxic by studies carried ultimately derived from benzo[a]pyrene, a out in vitro and also in vivo in animals, aquatic stereoisomer of benzo[a]pyrene-7,8-diol-9,10- microorganisms, plants and humans. In epoxide, and are produced by a series of contaminated air, PAHs are abundant in enzymatic reactions induced by volatile particulate fractions and organic13. monoxygenases and epoxide Hydrolysis15. Photochemical reactions may change 3. PAHs Metabolism by microbial dramatically to carcinogenic nitro-PAHs or to Bacteria are a type of microorganism actively endoproxides of the PAH and the radicals that participated in the organic pollutants are quickly converted to the quinones. Surface degradation into polluted sites. A lots of runoff water contains fluoranthene, pyrene and bacterial species are known in the PAHs phenanthrene, and other PAHs emerging from degrade. Most of which, representing wear and tear on vehicles and road. Many of efficiency of biodegradation, are isolated from those related areas are often associated with polluted sediments or soil. Benzo[a]pyrene is particles2. Soils along highway margins are one of the most carcinogenic and also toxic in contaminated from PAHs from exhaust, road PAH-petrochemical waste, researchs have tar, motor fuels, and street dust. These found that bacteria able to degrade compounds may be related to organic Benzo[a]pyrene when grown into it as sole molecules, silt or other fine particles in surface carbon source in aqueous culture soils, or may absorb dissolved organic matter experiments17. Sphingomonas paucimobilis and filter into the soils.14. Some LMW PAHs strain EPA 505 found a 5% decrease in are very toxic for aquatic organisms; and also Benzo[a]pyrene concentration within 168 h of several HMW PAHs are teratogenic and incubation period18. Aitken et al.19 reported carcinogenic to mammals and also a that the 11 strains isolated from a different mutagenic to bacteria. The germination of polluted sites (refinery oil, motor oil and wood spore is prevented by phenanthrene in some treatment) was with great efficiency to degrade fungi, The irradiation of the light of the PAHs of Benzo[a]pyrene. A huge diversity of that are in contact with the DNA may bacteria that are capable to oxidise stimulate the cleavage of one strand of DNA, Benzo[a]pyrene includes Pseudomonas, formation of DNA-PAH adducts, or oxidation Bacillus, Agrobacterium, Burkholderia and of guanine to the 8-hydroxyguanine2. When Sphingomonas species20. Benzo[a]pyrene has the HMW PAHs are adsorbed to particulate reported to be degraded via another bacteria matter in water sediments or soil, they are including Mycobacterium, Rhodococcus sp bioconverted a slowly. They also can be and mixed culture of Flavobacterium and Copyright © March-April, 2018; IJPAB 10

Al-Hawash et al Int. J. Pure App. Biosci. 6 (2): 8-24 (2018) ISSN: 2320 – 7051 Pseudomonas species19. Pseudomonas via the strain 984 with Mn-peroxidase aeruginosa isolated from a stream heavily activity, for the strain 870 by 17% observing contaminated by a petroleum refinery, which lignin peroxidase and laccase activities. was showed to be actively growing over high Phenanthrene degradation by 12% was found phenanthrene dosages and complete removal in strain 870 having Mn-peroxidase and of the pollutant at 30 days of incubation21. laccase activities. A high level of anthracene Romero et al.21,reported that the phenanthrene degradation (65%) was showed by the strain degradation using microorganisms isolated 71025. LMW PAHs (2-3 rings) were showed from a polluted current, both Pseudomonas to be degraded more widely via aeruginosa and Rhodotorula glutinis were the Trichocladium canadense Aspergillus sp., and prevailing microorganisms using Fusarium oxysporum. While HMW PAHs (4- phenanthrene. Other studies performed to 7rings), the optimum degradation has showd decontamination of contaminated soil in PAHs via Aspergillus sp., Trichocladium canadense., using a mixed microbial culture of the bacteria Achremonium sp and Verticillium sp. These from the genera Klebsiella and Acenitobacter studies have observed that fungi have a exhibited that after 6 months a great decline by significant efficiency to degrade a wide range 98% from PAH content took place. Several of PAHs with low-oxygen conditions. The bacteria that have isolated and that utilizing a system of monooxygenase cytochrome P450 naphthalene as a energy and sole source of also generate epoxies that are implicated in carbon are belong to the genera Rhodococcus, degradation. Epoxides can be hydrolyzed to Pseudomonas, Sphingomonas, Streptomyces, vicinal dihydrodiols or they may be rearranged Ralstonia, Polaromonas, Alcaligenes, into hydroxyl derivatives. Cajthaml et al.26, Burkholderia and Mycobacterium22. studied the pathway for degradation of Mycobacterium has most widely studied to anthracene and phenanthrene using lignolytic degrading pyrene in culture to using it as a fungus. Both bacteria and fungi metabolize a single carbon source23. Some fungi are known wide range of PAHs, but the main pathways to have the ability to degradation of persistent used by each group are various, see Fig.1. pollutants. The degradation of lignolitic fungi Metabolism of PAHs by aerobic bacteria is has been studied intensively over the past few usually started by dioxygenases, that years, because of the irregular structure of incorporate atoms of O2 in to PAH to lignin, lynolytic fungi produce extracellular configure one or more isomeric cis- enzymes in the privacy of the substrate low, dihydrodiol metabolites. making them suitable to degradation of various Bacterial dioxygenases are enzyme compounds. The system of lignolytic consists systems of multi component ; for example , from three major enzyme groups including naphthalene dioxygenase comprises of a lignin peroxidase, phenoloxidases (lacases, ferredoxin, a ferredoxin reductase and the tyrosinases), manganese dependent terminal iron-sulfur protein with small β and peroxidase, and H2O2-producing enzymes. large α subunits. The cis-dihydrodiols are The researches using purified enzymes found decreased by dihydrodiol dehydrogenases to that lignolytic enzymes are capable for configure a dihydroxylated aromatic degrade PAHs24. Lignolytic enzymes execute a intermediates (catechols), that can serve as one electron radical oxidation, producing substrates to ortho and meta ring-fission cation radicals from pollutants after then dioxygenases27. The ring cleavage products are followed by quinines appearance. Clemente et aslo metabolized for tricarboxylic acid cycle 25 al. , reported that the degradation of PAH by intermediates and finally to CO2. Tongpim and 13 deuteromycete ligninolytic fungal strains, Pickard28, reported that the Mycobacterium shown that the degradation rate differs with spp. and Streptomyces produce the difference of lignolytic enzymes. Higher monooxygenases, which can oxidize PAHs to naphthalene degradation by 69% was shown trans-dihydrodiols. The trans-dihydrodiols are Copyright © March-April, 2018; IJPAB 11

Al-Hawash et al Int. J. Pure App. Biosci. 6 (2): 8-24 (2018) ISSN: 2320 – 7051 encountered often among the metabolites implement more wide metabolism to the resulted by fungi. Generally, aerobic PAHs that lead to rings cleavage and microorganisms degrade LMW PAHs more production of CO2. WRF is a big group faster than HMW PAHs. There are at four belong to ligninolytic, wood-degrading possible reasons make the degrade PAHs of basidiomycetes which includes species of HMW more slowly than PAHs of LMW: Pleurotus, Trametes and Phanerochaete might lower water solubility, insufficient ability to induce a cytochrome P450 that functions in the stimulate degradative enzymes, slower uptake initial PAHs oxidation. Phanerochaete into the cells and lower energy yield to chrysosporium has three cytochrome P450 growth29. If HMW PAHs are supplied as an genes CYP63 (A1, A2 and A3) could encode energy carbon source, available energy from enzymes implicated to oxidation of low and the start reactions may not be satisfactory for HMW PAHs35. The CYP63 genes expression growth. Thus , other carbon source is normally is depends on the cultural conditions, nutrients added to supply the conditions to a co- and the substrates used as inducer. Moreover, metabolism. Due to the toxicity and white rot fungi (WRF) can secrete persistence of HMW PAHs into the extracellular ligninolytic enzymes, which are environment, numerous laboratories have lignin peroxidases, laccases and manganese tested a broader phylogenetic spectrum of peroxidasesthat are also probable to be microorganisms to the possible to degrade implicated. Those enzymes generally degrade them30,31. components of wood but also oxidize PAHs to 4. PAHs Metabolism by Fungi transient PAH diphenols, that are easily The Efficient PAHs biodegradation by a fungi autoxidized to the quinones. and another microorganisms has reported Lignin peroxidase with of H2O2, intensively in the last few years32. The oxidizes PAHs by oxidation possibilities ≤ ligninolytic fungi (a group that secrete 7.55 eV36, the Manganese peroxidase can be enzymes to breakdown a lignin in wood) and oxidizes the PAHs through means of the Mn- non-ligninolytic fungi (a group that do not dependent unsaturated lipids peroxidation37. secrete those enzymes) involved to the The laccase, a copper-containing enzyme, degradation of PAHs are listed in Table.2. oxidizes PAHs with mediator compounds Most of the main groups of non-ligninolytic existence, includes aniline, phenol, 4- fungi are ascomycetes, zygomycetes, hydroxybenzyl alcohol, 4-hydroxybenzoic hyphomycetes, and also others, include acid, methionine, cysteine/reduced degraders of PAH. The Aspergillus species, glutathione38. Lignin is consdred a Cunninghamella, and Penicillium the initial heterogeneous, HMW polymer from PAH transformation includes oxidation via the phenylpropane subunits along with β-aryl O2 cytochrome and P450 monooxygenase to ether, carbon-carbon, and another kindso f form the water and an arene oxide. The arene connectors. Due to the lignin has chemical oxide unsteady intermediate either is hydrated likeness with PAHs and some another via the epoxide hydrolase to the trans- environmental contaminants, ligninolytic fungi dihydrodiol Or re-arranged nonenzymatically have considered promising candidates for to configure a phenol. PAH trans-dihydrodiols tested the deterioration degradation of PAH39. and phenols could be methylated or The PAHs degradation by ligninolytic fungi transformed to sulfates, glucuronides, probably implicate intracellular enzymes, xylosides or glucosides33. The metabolites of including an epoxide hydrolase and PAHs using nonligninolytic fungi are mostly cytochrome P450 monooxygenase40. When the same to those configured by mammalian stage Phanerochaete chrysosporium grown in the I and phase II reactions , despite the existence high-nitrogen medium, metabolizes of variances in the regio- and stereoselectivity phenanthrene to many metabolites, such as of a participating enzymes34. Some fungi phenanthrene trans-9S,10S-dihydrodiol, the Copyright © March-April, 2018; IJPAB 12

Al-Hawash et al Int. J. Pure App. Biosci. 6 (2): 8-24 (2018) ISSN: 2320 – 7051 similar enantiomer as that configured thru sulfation, or conjugation with glucuronic acid mammals, when grown in a low concentration xylose, or glucose. Despite most of non- of nitrogen culture medium, metabolizes ligninolytic fungi are not able to complete phenanthrene instead to phenanthrene 9,10- PAHs mineralisation, those conjugates PAH quinone, with following cleavage of ring at are mostly less toxic and much soluble than the C-9 and the C-10 positions to configure their respective orginal compounds. Pothuluri 2,2 0-diphenic acid and ultimately CO2, Fig. et al.45 reported that the fluoranthene 2.41. Therefore, at least two pathways of degradation by using the species of non- metabolic for PAHs coexist in Phanerochaete ligninolytic fungal Cunninghamella elegans, chrysosporium; first leads to trans- the metabolites 3-fluoranthene-β- dihydrodiols, second to the quinones and other glucopyranoside, 3-(8-hydroxy-fluoranthene)- products of oxidation. A Pleurotus ostreatus β-glucopyranoside, fluoranthene trans-2,3- is belong to a ligninolytic fungus, it can dihydrodiol and also 8-hydroxy-fluoranthene- metabolize and mineralize anthracene, pyrene, trans-2,3-dihydrodiol showed no mutagenic fluorene and phenanthrene, when grown in impacts to a mouse liver homogenate fraction, both high and low nitrogen culture medium. and 9- hydroxy-fluoranthene-trans-2,3- The pathways suggested for the PAHs dihydrodiol was considerably lower toxic than metabolism by Pleurotus ostreatus refer that it fluoranthene. Aspergillus niger, metabolizes them in a highly regio- and Chrysosporium pannorum and stereoselective manner42. The pathway of Cunninghamella elegans are instance of non- Pleurotus ostreatus is the same as to that in ligninolytic fungi that use a cytochrome P450 Phanerochaete chrysosporium different only monoxygenase enzyme-mediated oxidative in stereoselectivity and the production of route for degradation of PAH. An instance the laccase as an alternative of LiP42. Moreover, cytochrome P450-mediated oxidation pathway two major types of fungal PAHs metabolism; of phenanthrene is detailed in the Fig 2,steps 1 those are mediated by both non-ligninolytic to 4 of . and ligninolytic fungi. Most of non- 4.2. Ligninolytic fungi ligninolytic fungi can not grow on wood, and WRF are a major group from fungi that then they have no need to produce the lignin secrete ligninolytic enzymes that implicated in peroxidase enzymes like in the ligninolytic the lignin oxidation with extant in wood and fungi. another organic material. Ligninolytic 4. 1. Non-ligninolytic fungi enzymes include two classes; those being The initial step of PAHs metabolism via non- laccases and peroxidases. Those enzymes are ligninolytic fungi is to oxidise the PAH in a produced extracellularly, and oxidise organic cytochrome P450 monoxygenase enzyme substance by a non-specific radical based stimulated reaction to configure an arene reaction. A two major kinds of peroxidase oxide43. This pathway is same to the enzyme depending on their reducing kind of mammalian PAHs metabolism. In comparison substrate, manganese peroxidase (MnP) and for aromatic compound oxidation via lignin peroxidase (LP), those enzymes are able dioxygenase enzymes to configure to oxidising the PAHs46. Laccases, that are cisdihydrodiols, the monoxygenase enzyme phenol oxidase enzymes, are also able of involves just one oxygen atom onto the oxidizing PAHs. In ligninolytic conditions, compound to configure an arene oxide. this is WRF can oxidise PAHs via generating free hydrated by an epoxide-hydrolase catalysed radicals (i.e., hydroxyl free radicals) via the reaction to configure a transdihydrodiol44. donation of one electron, that oxidises the ring Moreover, phenol derivatives could resulted of PAH43. This generates a selection of PAH- from arene oxides via the non-enzymatic re- quinones and acids instead dihydrodiols, arrangement of compound, that can act as llustrated in, Fig. 3, steps 5 and 6 . There is substrates to subsequent methylation or considerable interest for use the ligninolytic Copyright © March-April, 2018; IJPAB 13

Al-Hawash et al Int. J. Pure App. Biosci. 6 (2): 8-24 (2018) ISSN: 2320 – 7051 fungi for degrade PAHs, Since they have a low be oxidized by using the laccase of WRF substrate specificity and are therefore capable (Coriolopsis gallica) in the ABTS presence, to degrade even the most compounds and via the LiP of Phanerochaete recalcitrant. Degradation researches of the chrysosporium52. Cunninghamella elegans ligninolytic fungi have reported that PAHs metabolized acenaphthene to the 1- probably degraded by a incorporation of acenaphthenol, 1,5-dihydroxyacenaphthene, epoxide hydrolases, cytochrome P450 cis- and then to trans-1,2- monooxygenases and ligninolytic enzymes, dihydroxyacenaphthenes, 1-acenaphthenone, which can lead in the complete mineralisation 6-hydroxy-1-acenaphthenone, and after to 1,2- of the compound47. Degradation experiments acenaphthenedione53. Cunninghamella elegans of HMW PAHs includes benzo[a]pyrene and oxidized the fluorine to form 9-fluorenol, 9- pyrene using ligninolytic fungi (Pleurotus fluorenone, and to the 2-hydroxy-9- ostreatus and Phanerochaete chrysosporium) fluorenone54. Other fungi incudes referred that a combination of non-ligninolytic Cryphonectria parasitica, Ceriporiopsis and ligninolytic enzymes probably the key to subvermispora Bjerkandera adusta, the complete mineralisation of those Drechslera spicifera, Sporormiella australis, recalcitrant compounds47. Substantial studies Aspergillus terreus, Embellisia annulata, has focused in the possibility of this group of Colletotrichum dematium, Cunninghamella fungi to remediate materials of PAH-polluted. blakesleeana, and Cunninghamella echinulata In bioremediation field that used ligninolytic also can create the 9-fluorenol and 9- fungi to remediate polluted soils by PAH and fluorenone when oxidized the fluorine55. The sediments have found mixed results. Canet et laccases of Coriolopsis gallica and Trametes al.48proved that four WRF species was used to versicolor oxidize the fluorine to 9-fluorenone degrade a coal-tar-polluted soil, in this study, in the existence HBT mediator38. the soil was supplemented with straw (as a Cunninghamella elegans can be oxidized substrate for the ligninolytic fungi). Moreover Phenanthrene to form the trans-1,2-, 3,4-, and , the indigenous soil microorganisms were 9,10- dihydrodiols, glucosides of the 1-, 2-, 3-, successful in PAHs degradation than the 4-, and then to 9-phenanthrols, and 6-sulfates, introduced fungal species. Andersson and Syncephalastrum racemosum also can Lundstedt49, reported that the WRF and oxidized it to the trans-3,4- and 9,10- brown-rot fungi (Antrodia vaillantii and dihydrodiols, 4-phenanthrols, 5-sulfates, and a Pleurotus ostreatus) were used to degrade a glucuronide Fig. 2.56. The process appears to high range of PAHs. have been initiated by the cytochrome P450 5. Fungal metabolism of LMW PAHs which is also implicated in steroid Naphthalene was used as a model hydrocarbon hydroxylation. Aspergillus niger metabolized compound to examine the ability of microbial the phenanthrene to form he trans-9,10- to degrade PAHs due it is the simplest and the dihydrodiol, the 1- and 2-phenanthrols, 1- most soluble PAH. Naphthalene metabolized methoxyphenanthrene, and to a glucuronide, by Cunninghamella bainieri and many other three sulfates, and protocatechuic fungi50. A cytochrome P450 monooxygenase acid57.Penicillium spp., Cyclothyrium sp., at first produces a transient naphthalene 1,2- Mucor ramosissimus, Aspergillus terreus and epoxide, that is immediately converted further various other fungi are able to degraded the to metabolites which include the trans-1,2- Phenanthrene58. phenanthrene metabolizes by dihydrodiol, 1- and 2-naphthols, 4-hydroxy-1- Phanerochaete chrysosporium using a tetralone, 1,2- and 1,4-naphthoquinones, and cytochrome P450, configuring the trans-9,10- sulfate and also glucuronide conjugates. and 3,4-dihydrodiols, 9-, 3-, and then to 4- Yogambal and Karegoudar51, reported that the phenanthrols, and a glucoside conjugate59, Aspergillus niger has been metabolized the Cunninghamella elegans oxidized anthracene naphthalene by gentisic acid. Biphenylene can to the trans-1,2-dihydrodiol, 1-anthrol, and Copyright © March-April, 2018; IJPAB 14

Al-Hawash et al Int. J. Pure App. Biosci. 6 (2): 8-24 (2018) ISSN: 2320 – 7051 then to 1-anthryl sulfate, a cytochrome P450 Penicillium janthinellum, Penicillium seems implicated in the initial oxidation60. ochrochloron and Coniothyrium fuckelii are Aspergillus terreus, Rhodotorula glutin, degrade pyrene70. The metabolizes of pyrene Ulocladium chartarum, Mucor ramosissimus, by Aspergillus niger is to 1-hydroxypyrene, 2- Cyclothyrium sp., is also able to degraded quinones, 2- diols, 1-methoxypyrene, 1- anthracene58. The anthracene cleavage by pyrenyl sulfate, and to the 1-hydroxy-8- Aspergillus niger led to producing a gentisic pyrenyl sulfate71. Aspergillus terreus oxidizes acid51. The anthracene metabolize by WRF pyrene to 1-pyrenyl sulfate by cytochrome using laccase, LiP or MnP, oxidizes of P450 monooxygenation and sulfate anthracene by Phanerochaete chrysosporium conjugation reactions72. LiP of Phanerochaete to 9,10-anthraquinone, then acid is the ring chrysosporium is metabolizes pyrene to one or cleavage product61. The crude MnP of more quinones and finally to CO258,73. Nematoloma frowardii oxidizes anthracene to Nematoloma frowardii produces an LiP that the CO2, particularly in the reduced oxidizes pyrene at a rate which is improved glutathione presence62. The degrades of with presence of veratryl Alcohol, while the anthracene by Irpex lacteus produces MnP produced from the same strain is also anthraquinone, 1- and 2- oxidizes and mineralizes pyrene, particularly hydroxyanthraquinones, anthrone, and in the presence of reduced glutathione73. hydroxyanthrone, 2-(2 0-hydroxybenzoyl) Trametes versicolor laccase can oxidizes benzoic acid, and then to phthalic acid, 2- pyrene, with the addition of HBT68. Growth of (hydroxymethyl) benzoic acid, and then Rhodotorula glutinis and Fusarium solani, dimethylphthalic acid63. isolated from contaminated sediments, and for 6. Fungal metabolism of HMW PAHs four various Penicillium spp. and Trichoderma Cunninghamella elegans and other fungi can harzianum, isolated from soil at a be transformed the fluoranthene to difference formergasworks site on pyrene as a energy and metabolites that such as the trans-2,3- single carbon source has been reported74. dihydrodiol, 9-hydroxy- and also 8-hydroxy- Cunninghamella elegans is oxidized trans-2,3-dihydrodiols, 3-hydroxyfluoranthene, Benza,anthracene to the trans- 8,9-, 10,11-, and and the 2- glucosides64. There are many fungi 3,4-dihydrodiols and also the 3,4-diol-1,2- metabolize fluoranthene includes Absidia epoxides75. The laccase produces by Trametes cylindrospora, Absidia fusca, Penicillium sp., versicolor oxidizes benza, anthracene; Flammulina velutipes, Marasmiellus sp., oxidation is improved with HBT76. Passarini Laetiporus sulphureus, Trametes et al.77,reported that the Aspergillus versicolor,Pleurotus ostreatus, Agrocybe sclerotiorum CBMAI 849 exhibited the better praecox, Daedalea quercina, Bjerkandera execution with regard to pyrene degradation adusta, and others65,67. The MnP produced by and benzoa, pyrene, and also Mucor racemosus Nematoloma frowardii mineralizes the CBMAI 847 was capable to metabolize pyrene fluoranthene in the existence of reduced and benzo[a]pyrene, the hydroxylation glutathione62. The laccase of Trametes mechanism was mediated by the cytochrome versicolor able to oxidizes fluoranthene, P-450 monooxygenase. Machín-Ramírez et particularly in the presence of HBT68. Pyrene al.78, found that the use of Aspergillus niger, by fungus Cunninghamella elegans Penicillium Trichoderm harzianum has high transformed to 1-hydroxypyrene, the 1,6- and effective to benzoa, pyrene degradation. 1,8-quinones, and to the glucoside conjugates, Verdin et al.79, isolated fungi have been a see Fig. 369. Mucor racemosus var. greater ablity to degrade benzoa, pyrene Gliocladium virens, sphaerosporus, includes Trichoderma viride and Fusarium Trichoderma harzianum, Scopulariopsis solani convert different amounts of brumptii, Penicillium simplicissimum, benzoa,pyrene in liquid state.

Al-Hawash et al Int. J. Pure App. Biosci. 6 (2): 8-24 (2018) ISSN: 2320 – 7051

Fig. 1: Three main pathways for the metabolism of PAHs by fungi and bacteria 80

Fig. 2: Pathways for the metabolism of phenanthrene by various fungi81,82

Al-Hawash et al Int. J. Pure App. Biosci. 6 (2): 8-24 (2018) ISSN: 2320 – 7051 Table 1: Physical -chemical characteristics of PAHs

Compound Formula Mol. wt. CAS registry Boiling Melting Aqueous Structure (g/mol) No. point (°C) point (°C) solubility (mg/l)

Naphthalene C10H8 128 91-20-3 218 80.2 30

Anthracene C14H10 178 120-12-7 340 216.4 0.015

Phenanthrene C14H10 178 85-01-8 339 -340 100.5 0.25

Fluoranthene C16H10 202 206-44-0 375 -393 108.8 0.12 -0.18

Pyrene C16H10 202 129-00-0 360 -404 393 0.0057

Benz[a]anthracene C18H12 228 56-55-3 438 162 0.0038

Chrysene C18H12 205-99-2 448 254 Insoluble 228

Benzo[b]fluoranthene C20H12 252 205-99-2 168 168.3 Insoluble

Benz[a]pyrene C20H12 252 50-32-8 495 179 0.0038

Table 2: Polycyclic aromatic hydrocarbons oxidized by different species of fungi Fungi Compound References Trichoderma harzianum Naphthalene Mollea, Bosco [81] Phanerochaete chrysosporium Mollea, Bosco [81] Cunninghamellaelegans Cerniglia, Hebert [82] Aspergillus niger Cerniglia, Hebert [82] Cunninghamella bainieri Ferris, Fasco [48] Cunninghamella elegans Anthracene Cerniglia [83] Pleurotus ostreatus Schützendübel, Majcherczyk [84] Aspergillus fumigatus Ye, Yin [85] Phanerochaete chrysosporium Juan, Jun [86] Cunninghamella elegans Phenanthrene Romero, Cazau [19] Aspergillus niger Hammel, Kalyanaraman [34] Phanerochaete chrysosporium Sack, Hofrichter [87] Pleurotus ostreatus Bezalel, Hadar [40] Cunninghamella elegans Fluoranthene Pothuluri, Freeman [52] Penicillium sp Pointing [30] Pleurotus ostreatus Pozdnyakova, Rodakiewicz-Nowak [88] Aspergillus niger Pyrene Sack [63] Cunninghamella elegans Cerniglia, Mahaffey [89] Pleurotus ostreatus Sack, Heinze [65] Candida krusei Benzo[a]anthracene MacGillivray and Shiaris [90] Cunninghamella elegans Cerniglia and Yang [91] Phanerochaete chrysosporium Bogan, Schoenike [92] Aspergillus ochraceus Benzo[a]pyrene Passarini, Rodrigues [75] Cunninghamella elegans Cerniglia, Mahaffey [89] Trametes versicolor Collins, Kotterman [93] Trichoderma viride Machín-Ramírez, Morales [76] Mucor sp Dan, Li [94] Fusarium solani Fayeulle, Veignie [95] Cunninghamella elegans Chrysene Pothuluri, Selby [96] Penicillum janthinellum Boonchan, Britz [97]

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