Advertisement

Biodegradation

, Volume 18, Issue 3, pp 359–369 | Cite as

Enhancement of bioconversion of high-molecular mass polycyclic aromatic hydrocarbons in contaminated non-sterile soil by litter-decomposing fungi

  • Kari T. SteffenEmail author
  • Sven Schubert
  • Marja Tuomela
  • Annele Hatakka
  • Martin Hofrichter
Original Paper

Abstract

With the focus on alternative microbes for soil-bioremediation, 18 species of litter-decomposing basidiomycetous fungi were screened for their ability to grow on different lignocellulosic substrates including straw, flax and pine bark as well as to produce ligninolytic enzymes, namely laccase and manganese peroxidase. Following characteristics have been chosen as criteria for the strain selection: (i) the ability to grow at least on one of the mentioned materials, (ii) production of either of the ligninolytic enzymes and (iii) the ability to invade non-sterile soil. As the result, eight species were selected for a bioremediation experiment with an artificially contaminated soil (total polycyclic aromatic hydrocarbon (PAH) concentration 250 mg/kg soil). Up to 70%, 86% and 84% of benzo(a)anthracene, benzo(a)pyrene, and dibenzo(a,h)anthracene, respectively, were removed in presence of fungi while the indigenous microorganisms converted merely up to 29%, 26% and 43% of these compounds in 30 days. Low molecular-mass PAHs studied were easily degraded by soil microbes and only anthracene degradation was enhanced by the fungi as well. The agaric basidiomycetes Stropharia rugosoannulata and Stropharia coronilla were the most efficient PAH degraders among the litter-decomposing species used.

Keywords

Agrocybe Biodegradation Litter-decomposing fungi Polycyclic aromatic hydrocarbons Soil bioremediation Stropharia 

Abbreviations

BaP

Benzo(a)pyrene

LiP

Lignin peroxidase

LPO

Lipid peroxidation

LDF

Litter-decomposing fungi

MnP

Manganese peroxidase

PAHs

Polycyclic aromatic hydrocarbons

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

The work was financed by the Helsinki University Environmental Research Center (HERC), the Academy of Finland research grants 52063, 106213 and 209079, and the grant for the Centre of Excellence “Microbial Resources”. We thank G. Liepelt (International Graduate School of Zittau) for excellent technical assistance and the PAH analyses.

References

  1. Andersson BE, Lundstedt S, Tornberg K, Schnurer Y, Oberg LG, Mattiasson B (2003) Incomplete degradation of polycyclic aromatic hydrocarbons in soil inoculated with wood-rotting fungi and their effect on the indigenous soil bacteria. Environ Toxicol Chem 22:1238–1243CrossRefGoogle Scholar
  2. Baldrian P (2004) Increase of laccase activity during interspecific interactions of white-rot fungi. FEMS Microbiol Ecol 50:245–253CrossRefGoogle Scholar
  3. Baldrian P, in der Wiesche C, Gabriel J, Nerud F, Zadrazil F (2000) Influence of cadmium and mercury on activities of ligninolytic enzymes and degradation of polycyclic aromatic hydrocarbons by Pleurotus ostreatus in soil. Appl Environ Microbiol 66:2471–2478CrossRefGoogle Scholar
  4. Bezalel L, Hadar Y, Fu PP, Freeman JP, Cerniglia CE (1996) Initial oxidation products in the metabolism of pyrene, anthracene, fluorene and dibenzothiophene by white-rot fungus Pleurotus ostreatus. Appl Environ Microbiol 62:2554–2559Google Scholar
  5. Bhatt M, Cajthaml T, Sasek V (2002) Mycoremediation of PAH-contaminated soil. Folia Microbiol 47:255–258Google Scholar
  6. Bogan BW, Lamar RT (1996) Polycyclic aromatic hydrocarbon-degrading capabilities of Phanerochaete laevis HHB-1625 and its extracellular ligninolytic enzymes. Appl Environ Microbiol 62:1597–1603Google Scholar
  7. 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 66:1007–1019CrossRefGoogle Scholar
  8. Bumpus JA (1989) Biodegradation of polycyclic hydrocarbons by Phanerochaete chrysosporium. Appl Environ Microbiol 55:154–158Google Scholar
  9. Bumpus JA, Tien M, Wright D, Aust SD (1985) Oxidation of persistent environmental pollutants by a white-rot fungus. Science 228:1434–1436CrossRefGoogle Scholar
  10. Cajthaml T, Moder M, Kacer P, Sasek V, Popp P (2002) Study of fungal degradation products of polycyclic aromatic hydrocarbons using gas chromatography with ion trap mass spectrometry detection. J Chromatogr 974:213–222CrossRefGoogle Scholar
  11. Canet R, Birnstingl JG, Malcolm DG, Lopez-Real JM, Beck AJ (2001) Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by native microflora and combinations of white-rot fungi in a coal-tar contaminated soil. Biores Technol 76:113–117CrossRefGoogle Scholar
  12. Cerniglia CE (1993) Biodegradation of polycyclic aromatic hydrocarbons. Curr Opin Biotechnol 4:331–338CrossRefGoogle Scholar
  13. Collins PJ, Kotterman MJ, Field JA, Dobson ADW (1996) Oxidation of anthracene and benzo(a)pyrene by laccases from Trametes versicolor. Appl Environ Microbiol 62:4563–4567Google Scholar
  14. Eggen T, Majcherczyk A (1998) Removal of polycyclic aromatic hydrocarbons (PAH) in contaminated soil by white-rot fungus Pleurotus ostreatus. Int Biodet Biodegr 41:111–117CrossRefGoogle Scholar
  15. Eggert C, Temp U, Eriksson KEL (1996) The ligninolytic system of the white rot fungus Pycnoporus cinnabarinus: purification and characterization of the laccase. Appl Environ Microbiol 62:1151–1158Google Scholar
  16. Field JA, de Jong E, Feijoo-Costa G, de Bont JAM (1993) Screening for ligninolytic fungi applicable to the biodegradation of xenobiotics. Trends Biotechnol 11:44–49CrossRefGoogle Scholar
  17. Gramss G, Kirsche B, Voigt K-D, Günther T, Fritsche W (1999a) Conversion rates of five polycyclic aromatic hydrocarbons in liquid cultures of fifty-eight fungi and the concomitant production of oxidative enzymes. Mycol Res 103:1009–1018CrossRefGoogle Scholar
  18. Gramss G, Voigt KD, Kirsche B (1999b) Degradation of polycyclic aromatic hydrocarbons with three to seven aromatic rings by higher fungi in sterile and unsterile soils. Biodegradation 10:51–62CrossRefGoogle Scholar
  19. Grimm LH, Kelly S, Krull R, Hempel DC (2005) Morphology and productivity of filamentous fungi. Appl Microbiol Biotechnol 69:375–384CrossRefGoogle Scholar
  20. Hammel KE, Kalyanaraman B, Kirk TK (1986) Oxidation of polycyclic aromatic hydrocarbons and dibenzo[p]-dioxins by Phanerochaete chrysosporium ligninase. J␣Biol Chem 261:16948–16952Google Scholar
  21. Hatakka A (2001) Biodegradation of lignin. In: Hofrichter M, Steinbüchel A (eds) Lignin, humic substances and coal. Wiley-VCH, Weinheim, Germany, pp 129–180Google Scholar
  22. Hintikka V (1970) Studies on white-rot humus formed by higher fungi in forest soils. Communicationes Instituti Forestalis Fenniae 69:2Google Scholar
  23. Juhasz AL, Naidu R (2000) Bioremediation of high␣molecular weight polycyclic aromatic hydrocarbons: a␣review of the microbial degradation of benzo[a]pyrene. Int Biodet Biodegr 45:57–88CrossRefGoogle Scholar
  24. Kapich AN, Steffen KT, Hofrichter M, Hatakka A (2005) Involvement of lipid peroxidation in the degradation of a non-phenolic lignin model compound by manganese peroxidase of the litter-decomposing fungus Stropharia coronilla. Biochem Biophys Res Comm 330:371–377CrossRefGoogle Scholar
  25. Kotterman MJ, 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 64:2853–2858Google Scholar
  26. Kästner M (2000) Degradation of aromatic and polyaromatic compounds. In: Rehm H-J, Reed G (eds) Biotechnology. Wiley-VCH, Weinheim, Germany, pp 211–239Google Scholar
  27. Martens R, Wolter M, Bahadir M, Zadrazil F (1999) Mineralization of 14C-labelled highly-condensed polycyclic aromatic hydrocarbons in soils by Pleurotus sp. Florida. Soil Biol Biochem 31:1893–1899CrossRefGoogle Scholar
  28. Martinez AT (2002) Molecular biology and structure-function of lignin- degrading heme peroxidases. Enzyme Microb Technol 30:425–444CrossRefGoogle Scholar
  29. Masaphy S, Levanon D, Henis Y, Venkateswarlu K, Kelly SL (1996) Evidence for cytochrome P-450 and P-450-mediated benzo(a)pyrene hydroxylation in the white-rot fungus Phanerochaete chrysosporium. FEMS Microbiol Lett 135:51–55CrossRefGoogle Scholar
  30. Morgan P, Lee SA, Lewis ST, Sheppard AN, Watkinson RJ (1993) Growth and biodegradation by white-rot fungi inoculated into soil. Soil Biol Biochem 25:279–287CrossRefGoogle Scholar
  31. Novotny C, Erbanová P, Sasek V, Kubátová A, Cajthaml T, Lang E, Krahl J, Zadrazil F (1999) Extracellular oxidative enzyme production and PAH removal in soil by exploratory mycelium of white rot fungi. Biodegradation 10:159–168CrossRefGoogle Scholar
  32. Potin O, Veignie E, Rafin C (2004) Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by Cladosporium sphaerospermum isolated from an aged PAH contaminated soil. FEMS Microbiol Ecol 51:71–78CrossRefGoogle Scholar
  33. Rodriguez E, Nuero O, Guillen F, Martinez AT, Martinez MJ (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
  34. Sack U, Fritsche W (1997) Enhancement of pyrene mineralization in soil by wood-decaying fungi. FEMS Microbiol Ecol 22:77–83CrossRefGoogle Scholar
  35. Sack U, Hofrichter M, Fritsche W (1997) Degradation of polycyclic aromatic hydrocarbons by manganese peroxidase of Nematoloma frowardii. FEMS Microbiol Lett 152:227–234CrossRefGoogle Scholar
  36. Sasek V (2003) Why mycoremediations have not come into practice. In: Sasek V, Glaser A, Baveye P (eds) The ultilization of bioremediation to reduce soil contamination: problems and solutions. Kluiwer Academic Publishers, Netherlands, pp 247–266Google Scholar
  37. Schneider J, Grosser R, Jayasimhulu K, Xue W, Warshawsky D (1996) Degradation of pyrene, benz[a]anthracene, and benzo[a]pyrene by Mycobacterium sp. strain RJGII-135, isolated from a former coal gasification site. Appl Environ Microbiol 62:13–19Google Scholar
  38. Schützendübel A, Majcherczyk A, Johannes C, Hüttermann A (1999) Degradation of fluorene, anthracene, phenanthrene, fluoranthene, and pyrene lacks connection to the production of extracellular enzymes by Pleurotus ostreatus and Bjerkandera adusta. Internat Biodet Biodegr 43:93–100CrossRefGoogle Scholar
  39. Steffen KT, Hatakka A, Hofrichter M (2002a) Removal and mineralization of polycyclic aromatic hydrocarbons by litter-decomposing basidiomycetous fungi. Appl Microbiol Biotechnol 60:212–217CrossRefGoogle Scholar
  40. Steffen KT, Hatakka A, Hofrichter M (2003) Degradation of benzo[a]pyrene by the litter-decomposing basidiomycete Stropharia coronilla: role of manganese peroxidase. Appl Environ Microbiol 69:3957–3964CrossRefGoogle Scholar
  41. Steffen KT, Hofrichter M, Hatakka A (2000) Mineralisation of 14C-labelled synthetic lignin and ligninolytic enzyme activities of litter-decomposing basidiomycetous fungi. Appl Microbiol Biotechnol 54:819–825CrossRefGoogle Scholar
  42. Steffen KT, Hofrichter M, Hatakka A (2002b) Purification and characterization of manganese peroxidases from the litter-decomposing basidiomycetes Agrocybe praecox and Stropharia coronilla. Enzyme Microb Technol 30:550–555CrossRefGoogle Scholar
  43. Tuomela M, Lyytikäinen M, Oivanen P, Hatakka A (1999) Mineralization and conversion of pentachlorophenol (PCP) in soil inoculated with the white-rot fungus Trametes versicolor. Soil Biol Biochem 31:65–74CrossRefGoogle Scholar
  44. Wariishi H, Valli K, Gold MH (1992) Manganese(II) oxidation by manganese peroxidase from the basidiomycete Phanerochaete chrysosporium. Kinetic mechanism and role of chelators. J Biol Chem 267:23688–23695Google Scholar
  45. Wunch KG, Alworth WL, Bennett JW (1999) Mineralization of benzo[a]pyrene by Marasmiellus troyanus, a mushroom isolated from a toxic waste site. Microbiol Res 154:75–79Google Scholar
  46. Wunch KG, Feibelman T, Bennett JW (1997) Screening for fungi capable of removing benzo(a)pyrene in culture. Appl Microbiol Biotechnol 47:620–624CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Kari T. Steffen
    • 1
    Email author
  • Sven Schubert
    • 2
    • 3
  • Marja Tuomela
    • 1
  • Annele Hatakka
    • 1
  • Martin Hofrichter
    • 2
  1. 1.Department of Applied Chemistry and MicrobiologyUniversity of HelsinkiHelsinkiFinland
  2. 2.Chair of Environmental BiotechnologyInternational Graduate School ZittauZittauGermany
  3. 3.Chair for Process BiotechnologyUniversity of BayreuthBayreuthGermany

Personalised recommendations