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Fungi as Bioremediators pp 159–179Cite as

Bioremediation of PAH-Contaminated Soil by Fungi

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Part of the book series: Soil Biology ((SOILBIOL,volume 32))

Abstract

Polycyclic aromatic hydrocarbons (PAHs) are by-products of the incomplete combustion of organic materials. They are considered to be priority pollutants in the environment due to their recalcitrance and mutagenic properties. The principal PAH loss process from soil is through microbial degradation; therefore, the bioremediation is considered as an efficient, financially affordable, and adaptable alternative for the recuperation of PAH-contaminated soil. Several microorganisms, such as bacteria, yeasts, and filamentous fungi, are capable of degrading different types of PAHs. The ability of the fungi to degrade the high-molecular-weight PAHs, together with their physiological versatility, converts the fungal remediation in a promising technique for the cleanup of PAH-contaminated soil. This chapter summarizes the recent information on the metabolic pathway of the fungal transformation of PAHs and provides a critical review of previous work about fungal bioremediation of PAH-contaminated soil. Also, some of the most recently used fungal technology to enhance PAHs bioremediation processes is discussed.

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References

  • Acevedo F, Pizzul L, Castillo MP, González ME, Cea M, Gianfreda L, Diez MC (2010) Degradation of polycyclic aromatic hydrocarbons by free and nanoclay-immobilized manganese peroxidase from Anthracophyllum discolor. Chemosphere 80:271–278

    Article  PubMed  CAS  Google Scholar 

  • Acevedo F, Pizzul L, Castillo MP, Cuevas R, Diez MC (2011) Degradation of polycyclic aromatic hydrocarbons by the Chilean white-rot fungus Anthracophyllum discolor. J Hazard Mater 185:212–219

    Article  PubMed  CAS  Google Scholar 

  • April TM, Fought JM, Currah RS (2000) Hydrocarbon-degrading filamentous fungi isolated from flare pit soils in northern and western Canada. Can J Microbiol 46:38–49

    Article  PubMed  CAS  Google Scholar 

  • Bamforth SM, Singleton I (2005) Bioremediation of polycyclic aromatic hydrocarbons: current knowledge and future directions. J Chem Technol Biotechnol 80:723–736

    Article  CAS  Google Scholar 

  • Berthe-Corti L, Del Panno MT, Hulsch R, Morelli IS (2007) Bioremediation and bioaugmentation of soils contaminated with polyaromatic hydrocarbons. Curr Trends Microbiol 3:1–30

    CAS  Google Scholar 

  • Bezalel L, Hadar Y, Cerniglia CE (1997) Enzymatic mechanisms involved in phenanthrene degradation by the white rot fungus Pleurotus ostreatus. Appl Environ Microbiol 63:2495–2501

    PubMed  CAS  Google Scholar 

  • Bogan BW, Lamar RT, Burgos WD, Tien M (1999) Extent of humification of anthracene, fluoranthene, and benzo[alpha]pyrene by Pleurotus ostreatus during growth in PAH-contaminated soils. Lett Appl Microbiol 28:250–254

    Article  CAS  Google Scholar 

  • Boonchan S, Britz ML, Stanley GA (2000) Degradation and mineralization of high-molecular-weight polycyclic aromatic hydrocarbons by defined fungal bacterial cocultures. Appl Environ Microbiol 66:107–1019

    Article  Google Scholar 

  • Borràs E, Caminal G, Sarrà M, Novotný C (2010) Effect of soil bacteria on the ability of polycyclic aromatic hydrocarbons (PAHs) removal by Trametes versicolor and Irpex lacteus from contaminated soil. Soil Biol Biochem 42:2087–2093

    Article  Google Scholar 

  • Cañas AI, Camarero S (2010) Laccases and their natural mediators: biotechnological tools for sustainable eco-friendly processes. Biotechnol Adv 28:694–705

    Article  PubMed  Google Scholar 

  • Capotorti G, Digianvincenzo P, Cesti P, Bernardi A, Guglielmetti G (2004) Pyrene and benzo(a)pyrene metabolism by an Aspergillus terreus strain isolated from a polycyclic aromatic hydrocarbons polluted soil. Biodegradation 15:79–85

    Article  PubMed  CAS  Google Scholar 

  • Casillas RP, Crow SA, Heinze TM, Deck J, Cerniglia CE (1996) Initial oxidative and subsequent conjugative metabolites produced during the metabolism of phenanthrene by fungi. J Ind Microbiol 16:205–215

    Article  PubMed  CAS  Google Scholar 

  • Cerniglia CE (1984) Microbial metabolism of polycyclic aromatic hydrocarbons. Adv Appl Microbiol 30:31–71

    Article  PubMed  CAS  Google Scholar 

  • Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351–368

    Article  CAS  Google Scholar 

  • Cerniglia CE (1997) Fungal metabolism of polycyclic aromatic hydrocarbons: past, present and future applications in bioremediation. J Ind Microbiol Biotechnol 19:324–333

    Article  PubMed  CAS  Google Scholar 

  • Chaillan F, Le Fleche A, Bury E, Phantavong Y, Grimont P, Saliot A (2004) Identification and biodegradation potential of tropical aerobic hydrocarbon-degrading microorganisms. Res Microbiol 155:587–595

    Article  PubMed  CAS  Google Scholar 

  • Colombo J, Cabello M, Arambarri AM (1996) Biodegradation of aliphatic and aromatic hydrocarbons by natural soil microflora and pure cultures of imperfected and lignolitic fungi. Environ Pollut 94:355–362

    Article  PubMed  CAS  Google Scholar 

  • D’Annibale A, Ricci M, Leornadi V, Quaratino D, Micione E, Petruccioli M (2005) Degradation of aromatic hydrocarbons by white-rot fungi in a historically contaminated soil. Biotechnol Bioeng 90:723–731

    Article  PubMed  Google Scholar 

  • D’Annibale A, Rosetto F, Leonardi V, Federici F, Petruccioli M (2006) Role of autochthonous filamentous fungi in bioremediation of a soil historically contaminated with aromatic hydrocarbons. Appl Environ Microbiol 72:28–36

    Article  PubMed  Google Scholar 

  • Doick KJ, Klingelmann E, Burauel P, Jones KC, Semple KT (2005) Long-term fate of polychlorinated biphenyls and polycyclic aromatic hydrocarbons in an agricultural soil. Environ Sci Technol 39:3663–3670

    Article  PubMed  CAS  Google Scholar 

  • Ferreira MMC (2001) Polycyclic aromatic hydrocarbons: a QSPR study. Chemosphere 44:124–146

    Article  Google Scholar 

  • Gianfreda L, Rao MA (2004) Potential of extracellular enzymes in relation of polluted soils: a review. Enzyme Microb Technol 33:339–354

    Article  Google Scholar 

  • Gómez-Toribio V, García-Martin AB, Martínez MJ, Martínez AT, Guillén F (2009) Induction of extracellular hydroxyl radical production by white-rot fungi through quinone redox cycling. Appl Environ Microbiol 75:3944–3953

    Article  PubMed  Google Scholar 

  • Guillén F, Gómez-Toribio V, Martínez MJ, Martínez AT (2000) Production of hydroxyl radical by the synergistic action of fungal laccase and aryl alcohol oxidase. Arch Biochem Biophys 383:142–147

    Article  PubMed  Google Scholar 

  • Habe H, Omori T (2003) Genetic of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci Biotechnol Biochem 67:225–243

    Article  PubMed  CAS  Google Scholar 

  • Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169:1–15

    Article  PubMed  CAS  Google Scholar 

  • Head IM (1998) Bioremediation: towards a credible technology. Microbiology 144:599–608

    Article  CAS  Google Scholar 

  • in der Wiesche C, Martens R, Zadrazil F (2003) The effect of interaction between white-root fungi and indigenous microorganisms on degradation of polycyclic aromatic hydrocarbons in soil. Water Air Soil Pollut 3:73–79

    Article  Google Scholar 

  • Johnsen AR, Wick LY, Harms H (2005) Principles of microbiol PAH-degradation in soil. Environ Pollut 133:71–84

    Article  PubMed  CAS  Google Scholar 

  • Jurado M, Martinez AT, Martinez MJ, Saparrat MCN (2011) Wastes from agriculture, forestry and food processing. Application of white-rot fungi in transformation, detoxification, or revalorization of agriculture wastes: role of laccase in the processes. In: Murray Moo-Young (ed.), Comprehensive Biotechnology, Second Edition, Elsevier, pp 595–603

    Google Scholar 

  • Kirk TK, Farrell RL (1987) Enzymatic ‘combustion’: the microbial degradation of lignin. Annu Rev Microbiol 41:465–505

    Article  PubMed  CAS  Google Scholar 

  • Kotterman MJJ, Vis EH, Field JA (1998) Successive mineralization and detoxification of benzo[a]pyrene by the white rot fungus Bjerkandera sp strain BOS55 and indigenous microflora. Appl Environ Microbiol 64:2853–2858

    PubMed  CAS  Google Scholar 

  • Launen L, Pinto LJ, Wiebe C, Kiehlmann E, Moore MM (1995) The oxidation of pyrene and benzo[a]pyrene by non-basidiomycete soil fungi. Can J Microbiol 41:477–488

    Article  PubMed  CAS  Google Scholar 

  • Launen LA, Pinto LJ, Percival PW, Lam SFS, Moore MM (2000) Pyrene is metabolized to bound residues by Penicillium janthinellum SFU403. Biodegradation 11:305–312

    Article  PubMed  CAS  Google Scholar 

  • Leonardi V, Giubilei MA, Federici E, Spaccapelo R, Šašek V, Novotný C, Petruccioli M, D’Annibale A (2008) Mobilizing agents enhance fungal degradation of polycyclic aromatic hydrocarbons and affect diversity of indigenous bacteria in soil. Biotechnol Bioeng 101:273–285

    Article  PubMed  CAS  Google Scholar 

  • Maliszewska-Kordybach B, Smreczak B (2003) Habitual function of agricultural soils as affected by heavy metals and polycyclic aromatic hydrocarbons contamination. Environ Int 28:719–728

    Article  PubMed  CAS  Google Scholar 

  • Martínez AT, Speranza M, Ruiz-Dueñas FJ, Ferreira P, Camarero S, Guillén F, Martínez MJ, Gutiérrez A, del Río JC (2005) Biodegradation of lignocellulosics: microbiological, chemical and enzymatic aspects of fungal attack to lignin. Int Microbiol 8:95–204

    Google Scholar 

  • Novotný Č, Svobodová K, Erbanová P, Cajthaml T, Kasinath A, Lang E, Šašek V (2004) Ligninolytic fungi in bioremediation: extracellular enzyme production and degradation rate. Soil Biol Biochem 36:1545–1551

    Article  Google Scholar 

  • Pazos M, Rosales E, Alcántara T, Gómez J, Sanromán MA (2010) Decontamination of soils containing PAHs by electroremediation: a review. J Hazard Mater 177:1–11

    Article  PubMed  CAS  Google Scholar 

  • Peng RH, Xiong AS, Xue Y, Fu XY, Gao F, Zhao W, Tian YS, Yao QH (2008) Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32:927–955

    Article  PubMed  CAS  Google Scholar 

  • Pessacq J, Bianchini FE, Terada C, Da Silva M, Morelli IS, Del Panno MT (2010) Effect of different stress treatments on microbial catabolic diversity of chronically hydrocarbon contaminated-soil in Buenos Aires, Argentina. In: Book of abstracts of 13th international symposium on microbial ecology. International Society for Microbial Ecology, Seattle

    Google Scholar 

  • Potin O, Rafin C, Veignie E (2004) Bioremediation of an aged polycyclic aromatic hydrocarbons (PAHs)-contaminated soil by filamentous fungi isolated from the soil. Int Biodeterior Biodegrad 54:45–52

    Article  CAS  Google Scholar 

  • Quiquampoix H, Servagent-Noinville S, Baron MH (2002) Enzymes adsorption on soil mineral surfaces and consequences for the catalytic activity. In: Burns RG, Dick RP (eds) Enzymes in the environment: activity, ecology, and applications. Marcel Dekker, New York, pp 285–306

    Google Scholar 

  • Richnow HH, Seifert R, Hefter J, Link M, Francke W, Schaefer G, Michaelis W (1997) Organic pollutants associated with macromolecular soil organic matter: mode of binding. Org Geochem 26:745–758

    Article  CAS  Google Scholar 

  • Rodríguez E, Nuero O, Guillén F et al (2004) Degradation of phenolic and non-phenolic aromatic pollutants by four Pleurotus species: the role of laccase and versatile peroxidase. Soil Biol Biochem 36:909–916

    Article  Google Scholar 

  • Romero MC, Urrutia MI, Reinoso HE, Moreno Kiernan M (2010) Benzo[a]pyrene degradation by soil filamentous fungi. J Yeast Fungal Res 1:25–29

    CAS  Google Scholar 

  • Ruiz-Dueñas FJ, Martínez AT (2009) Microbial degradation of lignin: how a bulky recalcitrant polymer is efficiently recycled in nature and how we can take advantage of this. Microb Biotechnol 2:164–177

    Article  PubMed  Google Scholar 

  • Sack U, Fritsche W (1997) Enhancement of pyrene mineralization in soil by wood-decaying fungi. FEMS Microbiol Ecol 22:77–83

    Article  CAS  Google Scholar 

  • Saparrat MCN, Balatti PA (2005) The biology of fungal laccases and their potential role in biotechnology (chapter 4). In: Thangadurai D, Pullaiah T, Tripathy L (eds) Genetic resources and biotechnology, vol 3. Regency, New Delhi, pp 94–120, 366 pp. ISBN 81-89233-28-9

    Google Scholar 

  • Saparrat MCN, Hammer E (2006) Decolorization of synthetic dyes by the deuteromycete Pestalotiopsis guepinii CLPS no. 786 strain. J Basic Microbiol 46:28–33

    Article  PubMed  CAS  Google Scholar 

  • Saparrat MCN, Guillén F, Arambarri AM, Martínez AT, Martínez MJ (2002) Induction, isolation, and characterization of two laccases from the white-rot basidiomycete Coriolopsis rigida. Appl Environ Microbiol 68:1534–1540

    Article  PubMed  CAS  Google Scholar 

  • Saparrat MCN, Rocca M, Aulicino MB, Arambarri A, Balatti P (2008a) Celtis tala and Scutia buxifolia leaf litter decomposition by selected fungi in relation to their physical and chemical properties and the lignocellulolytic enzyme activity. Eur J Soil Biol 44:400–407

    Article  CAS  Google Scholar 

  • Saparrat MCN, Mocchiutti P, Liggieri CS, Aulicino M, Caffini N, Balatti PA, Martínez MJ (2008b) Ligninolytic enzyme ability and potential biotechnology applications of the white-rot fungus Grammothele subargentea LPSC no. 436 strain. Process Biochem 43:368–375

    Article  CAS  Google Scholar 

  • Saparrat MCN, Balatti PA, Martínez MJ, Jurado M (2010) Differential regulation of laccase gene expression in Coriolopsis rigida LPSC No. 232. Fungal Biol 114:999–1006

    Article  PubMed  CAS  Google Scholar 

  • Saraswathy A, Hallberg R (2005) Mycelial pellet formation by Penicillium ochrochloron species due to exposure to pyrene. Microbiol Res 160:375–383

    Article  PubMed  CAS  Google Scholar 

  • Schmidt S, Christensen J, Johnsen A (2010) Fungal PAH-metabolites resist mineralization by soil microorganisms. Environ Sci Technol 44:1677–1682

    Article  PubMed  CAS  Google Scholar 

  • Semple KT, Morriss WJ, Paton GI (2003) Bioavailability of hydrophobic organic contaminants in soils, fundamental concepts and techniques for analysis. Eur J Soil Sci 54:809–818

    Article  CAS  Google Scholar 

  • Sigma–Aldrich Company (http://www.sigmaaldrich.com)

  • Silva IS, Santos ED, Menezes CR, Faria AF, Franciscon E, Grossman M, Durrant LR (2009) Bioremediation of a polyaromatic hydrocarbon contaminated soil by native soil microbiota and bioaugmentation with isolated microbial consortia. Bioresour Technol 100:4669–4675

    Article  PubMed  CAS  Google Scholar 

  • Temp U, Eggert C (1999) Novel interaction between laccase and cellobiose dehydrogenase during pigment synthesis in the white rot fungus Pycnoporus cinnabarinus. Appl Environ Microbiol 65:389–395

    PubMed  CAS  Google Scholar 

  • Torres E, Bustos-Jaimes I, Le Borgne S (2003) Potential use of oxidative enzymes for the detoxification of organic pollutants. Appl Catal B 46:1–15

    Article  CAS  Google Scholar 

  • Ueno A, Ito Y, Yumoto I, Okuyama H (2007) Isolation and characterization of bacteria from soil contaminated with diesel oil and the possible use of these in autochthonous bioaugmentation. World J Microbiol Biotechnol 23:1739–1745

    Article  CAS  Google Scholar 

  • Wild SR, Jones KC (1995) Polynuclear aromatic hydrocarbons in the United Kingdom environment: a preliminary source inventory and budget. Environ Pollut 88:91–108

    Article  PubMed  CAS  Google Scholar 

  • Wu YC, Luo YM, Zou DX, Ni JZ, Liu WX, Teng Y, Li ZG (2008a) Bioremediation of polycyclic aromatic hydrocarbons contaminated soil with Monilinia sp.: degradation and microbial community analysis. Biodegradation 19:247–257

    Article  PubMed  CAS  Google Scholar 

  • Wu YC, Teng Y, Li ZG, Liao XW, Luo YM (2008b) Potential role of polycyclic aromatic hydrocarbons (PAHs) oxidation by fungal laccase in the remediation of an aged contaminated soil. Soil Biol Biochem 40:789–796

    Article  CAS  Google Scholar 

  • Wunder T, Marr J, Kremer S, Sterner O, Anke H (1997) 1-methoxypyrene and 1,6-dimethoxypyrene: two novel metabolites in fungal metabolism of polycyclic aromatic hydrocarbons. Arch Microbiol 167:310–316

    Article  PubMed  CAS  Google Scholar 

  • Yang Y, Zhang N, Xue M, Tao S (2010) Impact of soil organic matter on the distribution of polycyclic aromatic hydrocarbons (PAHs) in soils. Environ Pollut 158:2170–2174

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

Arambarri A. M. and Saparrat M. C. N. are research members of CONICET, and Morelli I.S. is research member of CIC-PBA. Coppotelli B. M. is postdoctoral fellow of CONICET. This review was partially supported by a grant from ANPCyT (PICT 884) and CONICET (PIP 1422) Argentina.

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Authors and Affiliations

  1. Centro de Investigación y Desarrollo en Fermentaciones Industriales, CINDEFI (UNLP, CCT-La Plata, CONICET), La Plata, 1900, Argentina

    Irma Susana Morelli, María Teresa Del Panno & Bibiana Marina Coppotelli

  2. Cátedra de Microbiología, Facultad de Ciencias Exactas, UNLP, La Plata, Argentina

    Irma Susana Morelli & María Teresa Del Panno

  3. Comisión de Investigaciones Científicas de la Provincia de Buenos Aires (CIC-PBA), La Plata, Argentina

    Irma Susana Morelli

  4. Instituto de Botánica Spegazzini, Facultad de Ciencias Naturales y Museo, UNLP, La Plata, Argentina

    Mario Carlos Nazareno Saparrat & Angélica Arrambari

  5. Instituto de Fisiología Vegetal, INFIVE (UNLP, CCT-La Plata, CONICET), La Plata, Argentina

    Mario Carlos Nazareno Saparrat

  6. Cátedra de Microbiología Agrícola, Facultad de Ciencias Agrarias y Forestales, UNLP, La Plata, Argentina

    Mario Carlos Nazareno Saparrat

Authors
  1. Irma Susana Morelli
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  2. Mario Carlos Nazareno Saparrat
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  3. María Teresa Del Panno
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  4. Bibiana Marina Coppotelli
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  5. Angélica Arrambari
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Corresponding author

Correspondence to Irma Susana Morelli .

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Editors and Affiliations

  1. College of Agriculture, Dept. of Plant Pathology, Tarbiat Modares University, Jalal Ale Ahmad Highway, Tehran, 14115, Iran

    Ebrahim Mohammadi Goltapeh

  2. Faculty of Agriculture, Dep Plant Protection, Urmia University, no street, Urmia, 165, Iran

    Younes Rezaee Danesh

  3. Amity Institute of Microbial Technology, Amity University Uttar Pradesh, E-3 Block, Sector 125, Noida, 201303, Uttar Pradesh, India

    Ajit Varma

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Morelli, I.S., Saparrat, M.C.N., Panno, M.T.D., Coppotelli, B.M., Arrambari, A. (2013). Bioremediation of PAH-Contaminated Soil by Fungi. In: Goltapeh, E., Danesh, Y., Varma, A. (eds) Fungi as Bioremediators. Soil Biology, vol 32. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-33811-3_7

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