Advertisement

Bioremediation of PAH-Contaminated Soil by Fungi

  • Irma Susana MorelliEmail author
  • Mario Carlos Nazareno Saparrat
  • María Teresa Del Panno
  • Bibiana Marina Coppotelli
  • Angélica Arrambari
Chapter
Part of the Soil Biology book series (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.

Keywords

Ligninolytic Enzyme PAHs Degradation Ligninolytic Fungus Free Laccase Cunninghamella Elegans 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

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.

References

  1. 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 80:271–278PubMedCrossRefGoogle Scholar
  2. 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 185:212–219PubMedCrossRefGoogle Scholar
  3. April TM, Fought JM, Currah RS (2000) Hydrocarbon-degrading filamentous fungi isolated from flare pit soils in northern and western Canada. Can J Microbiol 46:38–49PubMedCrossRefGoogle Scholar
  4. Bamforth SM, Singleton I (2005) Bioremediation of polycyclic aromatic hydrocarbons: current knowledge and future directions. J Chem Technol Biotechnol 80:723–736CrossRefGoogle Scholar
  5. Berthe-Corti L, Del Panno MT, Hulsch R, Morelli IS (2007) Bioremediation and bioaugmentation of soils contaminated with polyaromatic hydrocarbons. Curr Trends Microbiol 3:1–30Google Scholar
  6. Bezalel L, Hadar Y, Cerniglia CE (1997) Enzymatic mechanisms involved in phenanthrene degradation by the white rot fungus Pleurotus ostreatus. Appl Environ Microbiol 63:2495–2501PubMedGoogle Scholar
  7. 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 28:250–254CrossRefGoogle Scholar
  8. 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 66:107–1019CrossRefGoogle Scholar
  9. 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 42:2087–2093CrossRefGoogle Scholar
  10. Cañas AI, Camarero S (2010) Laccases and their natural mediators: biotechnological tools for sustainable eco-friendly processes. Biotechnol Adv 28:694–705PubMedCrossRefGoogle Scholar
  11. 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 15:79–85PubMedCrossRefGoogle Scholar
  12. 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 16:205–215PubMedCrossRefGoogle Scholar
  13. Cerniglia CE (1984) Microbial metabolism of polycyclic aromatic hydrocarbons. Adv Appl Microbiol 30:31–71PubMedCrossRefGoogle Scholar
  14. Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351–368CrossRefGoogle Scholar
  15. Cerniglia CE (1997) Fungal metabolism of polycyclic aromatic hydrocarbons: past, present and future applications in bioremediation. J Ind Microbiol Biotechnol 19:324–333PubMedCrossRefGoogle Scholar
  16. 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 155:587–595PubMedCrossRefGoogle Scholar
  17. 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 94:355–362PubMedCrossRefGoogle Scholar
  18. 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 90:723–731PubMedCrossRefGoogle Scholar
  19. 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 72:28–36PubMedCrossRefGoogle Scholar
  20. 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 39:3663–3670PubMedCrossRefGoogle Scholar
  21. Ferreira MMC (2001) Polycyclic aromatic hydrocarbons: a QSPR study. Chemosphere 44:124–146CrossRefGoogle Scholar
  22. Gianfreda L, Rao MA (2004) Potential of extracellular enzymes in relation of polluted soils: a review. Enzyme Microb Technol 33:339–354CrossRefGoogle Scholar
  23. 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 75:3944–3953PubMedCrossRefGoogle Scholar
  24. 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 383:142–147PubMedCrossRefGoogle Scholar
  25. Habe H, Omori T (2003) Genetic of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci Biotechnol Biochem 67:225–243PubMedCrossRefGoogle Scholar
  26. Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169:1–15PubMedCrossRefGoogle Scholar
  27. Head IM (1998) Bioremediation: towards a credible technology. Microbiology 144:599–608CrossRefGoogle Scholar
  28. 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 3:73–79CrossRefGoogle Scholar
  29. Johnsen AR, Wick LY, Harms H (2005) Principles of microbiol PAH-degradation in soil. Environ Pollut 133:71–84PubMedCrossRefGoogle Scholar
  30. 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 595–603Google Scholar
  31. Kirk TK, Farrell RL (1987) Enzymatic ‘combustion’: the microbial degradation of lignin. Annu Rev Microbiol 41:465–505PubMedCrossRefGoogle Scholar
  32. 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 64:2853–2858PubMedGoogle Scholar
  33. 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 41:477–488PubMedCrossRefGoogle Scholar
  34. Launen LA, Pinto LJ, Percival PW, Lam SFS, Moore MM (2000) Pyrene is metabolized to bound residues by Penicillium janthinellum SFU403. Biodegradation 11:305–312PubMedCrossRefGoogle Scholar
  35. 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 101:273–285PubMedCrossRefGoogle Scholar
  36. Maliszewska-Kordybach B, Smreczak B (2003) Habitual function of agricultural soils as affected by heavy metals and polycyclic aromatic hydrocarbons contamination. Environ Int 28:719–728PubMedCrossRefGoogle Scholar
  37. 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 8:95–204Google Scholar
  38. 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 36:1545–1551CrossRefGoogle Scholar
  39. Pazos M, Rosales E, Alcántara T, Gómez J, Sanromán MA (2010) Decontamination of soils containing PAHs by electroremediation: a review. J Hazard Mater 177:1–11PubMedCrossRefGoogle Scholar
  40. 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 32:927–955PubMedCrossRefGoogle Scholar
  41. 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, SeattleGoogle Scholar
  42. 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 54:45–52CrossRefGoogle Scholar
  43. 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 285–306Google Scholar
  44. 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 26:745–758CrossRefGoogle Scholar
  45. 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 36:909–916CrossRefGoogle Scholar
  46. Romero MC, Urrutia MI, Reinoso HE, Moreno Kiernan M (2010) Benzo[a]pyrene degradation by soil filamentous fungi. J Yeast Fungal Res 1:25–29Google Scholar
  47. 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 2:164–177PubMedCrossRefGoogle Scholar
  48. Sack U, Fritsche W (1997) Enhancement of pyrene mineralization in soil by wood-decaying fungi. FEMS Microbiol Ecol 22:77–83CrossRefGoogle Scholar
  49. 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 81-89233-28-9Google Scholar
  50. Saparrat MCN, Hammer E (2006) Decolorization of synthetic dyes by the deuteromycete Pestalotiopsis guepinii CLPS no. 786 strain. J Basic Microbiol 46:28–33PubMedCrossRefGoogle Scholar
  51. 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 68:1534–1540PubMedCrossRefGoogle Scholar
  52. 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 44:400–407CrossRefGoogle Scholar
  53. 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 43:368–375CrossRefGoogle Scholar
  54. Saparrat MCN, Balatti PA, Martínez MJ, Jurado M (2010) Differential regulation of laccase gene expression in Coriolopsis rigida LPSC No. 232. Fungal Biol 114:999–1006PubMedCrossRefGoogle Scholar
  55. Saraswathy A, Hallberg R (2005) Mycelial pellet formation by Penicillium ochrochloron species due to exposure to pyrene. Microbiol Res 160:375–383PubMedCrossRefGoogle Scholar
  56. Schmidt S, Christensen J, Johnsen A (2010) Fungal PAH-metabolites resist mineralization by soil microorganisms. Environ Sci Technol 44:1677–1682PubMedCrossRefGoogle Scholar
  57. Semple KT, Morriss WJ, Paton GI (2003) Bioavailability of hydrophobic organic contaminants in soils, fundamental concepts and techniques for analysis. Eur J Soil Sci 54:809–818CrossRefGoogle Scholar
  58. Sigma–Aldrich Company (http://www.sigmaaldrich.com)
  59. 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 100:4669–4675PubMedCrossRefGoogle Scholar
  60. 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 65:389–395PubMedGoogle Scholar
  61. Torres E, Bustos-Jaimes I, Le Borgne S (2003) Potential use of oxidative enzymes for the detoxification of organic pollutants. Appl Catal B 46:1–15CrossRefGoogle Scholar
  62. 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 23:1739–1745CrossRefGoogle Scholar
  63. Wild SR, Jones KC (1995) Polynuclear aromatic hydrocarbons in the United Kingdom environment: a preliminary source inventory and budget. Environ Pollut 88:91–108PubMedCrossRefGoogle Scholar
  64. 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 19:247–257PubMedCrossRefGoogle Scholar
  65. 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 40:789–796CrossRefGoogle Scholar
  66. 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 167:310–316PubMedCrossRefGoogle Scholar
  67. 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 158:2170–2174PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Irma Susana Morelli
    • 1
    • 2
    • 3
    Email author
  • Mario Carlos Nazareno Saparrat
    • 4
    • 5
    • 6
  • María Teresa Del Panno
    • 1
    • 2
  • Bibiana Marina Coppotelli
    • 1
  • Angélica Arrambari
    • 4
  1. 1.Centro de Investigación y Desarrollo en Fermentaciones IndustrialesCINDEFI (UNLP, CCT-La Plata, CONICET)La PlataArgentina
  2. 2.Cátedra de Microbiología, Facultad de Ciencias ExactasUNLPLa PlataArgentina
  3. 3.Comisión de Investigaciones Científicas de la Provincia de Buenos Aires (CIC-PBA)La PlataArgentina
  4. 4.Instituto de Botánica Spegazzini, Facultad de Ciencias Naturales y MuseoUNLPLa PlataArgentina
  5. 5.Instituto de Fisiología VegetalINFIVE (UNLP, CCT-La Plata, CONICET)La PlataArgentina
  6. 6.Cátedra de Microbiología Agrícola, Facultad de Ciencias Agrarias y ForestalesUNLPLa PlataArgentina

Personalised recommendations