Skip to main content
SpringerLink
Log in

Degradation of polycyclic aromatic hydrocarbons with three to seven aromatic rings by higher fungi in sterile and unsterile soils

  • Published:
Biodegradation Aims and scope Submit manuscript

Abstract

Seven commercial 3- to 7-ring (R) polycyclic aromatic hydrocarbons (PAH) as well as PAH derived from lignite tar were spiked into 3 soils (0.8 to 9.7% of organic carbon). The disappearance of the original PAH was determined for the freshly spiked soils, for soils incubated for up to 287 d with their indigenous microflora, and for autoclaved, unsterile and pasteurized soils inoculated with basidiomycetous and ascomycetous fungi. Three to 12 d after spiking, 22 to 38% of the PAH could no longer be recovered from the soils. At 287 d, 88.5 to 92.7%, 83.4 to 87.4%, and 22.0 to 42.1% of the 3-, 4-, and 5- to 7-R PAH, respectively, had disappeared from the unsterile, uninoculated soils. In 2 organic-rich sterile soils, the groups of wood- and straw-degrading, terricolous, and ectomycorrhizal fungi reduced the concentration of 5 PAH by 12.6, 37.9, and 9.4% in 287 d. Five- to 7-R PAH were degraded as efficiently as most of the 3- to 4-R PAH. In organic-rich unsterile soils inoculated with wood- and straw-degrading fungi, the degradation of 3- to 4-R PAH was not accelerated by the presence of fungi.The 5- to 7-R PAH, which were not attacked by bacteria, were degraded by fungi to 29 to 42% in optimum combinations of fungal species and soil type. In organic-poor unsterile soil, these same fungi delayed the net degradation of PAH possibly for 2 reasons. Mycelia of Pleurotus killed most of the indigenous soil bacteria expected to take part in the degradation of PAH, whereas those of Hypholoma and Stropharia promoted the development of opportunistic bacteria in the soil, which must not necessarily be PAH degraders. Contemporarily, the contribution of the fungi themselves to PAH degradation may be negligible in the absence of soil organic matter due to the lower production of ligninolytic enzymes. It is concluded that fungi degrade PAH irrespective of their molecular size in organic-rich and wood chip-amended soils which promote fungal oxidative enzyme production.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bogan BW & Lamar RT (1995) One-electron oxidation in the degradation of creosote polycyclic aromatic hydrocarbons by Phanerochaete chrysosporium. Appl. Environ. Microbiol. 61: 2631–2635

    Google Scholar 

  • Bogan BW, Schoenike B, Lamar RT & Cullen D (1996a) Manganese peroxidase mRNA and enzyme activity levels during bioremediation of polycyclic aromatic hydrocarbon-contaminated soil with Phanerochaete chrysosporium. Appl. Environ. Microbiol. 62: 2381–2386

    Google Scholar 

  • Bogan BW, Schoenike B, Lamar RT & Cullen D (1996b) Expression of lip genes during growth in soil and oxidation of anthracene by Phanerochaete chrysosporium. Appl. Environ. Microbiol. 62: 3697–3703

    Google Scholar 

  • Calderbank A (1989) The occurrence and significance of bound pesticide residues in soil. Rev. Environ. Contam. Toxicol. 108: 71–103

    Google Scholar 

  • Carmichael LM & Pfaender FK (1997) The effect of inorganic and organic supplements on the microbial degradation of phenanthrene and pyrene in soils. Biodegradation 8: 1–13

    Google Scholar 

  • Cavalieri E & Rogan E (1985) Role of radical cations in aromatic hydrocarbon carcinogenesis. Environ. Health Persp. 64: 69–84

    Google Scholar 

  • Cavalieri EL, Rogan EG, Roth RW, Saugier RK & Hakam A (1983) The relationship between ionization potential and horseradish peroxidase/hydrogen peroxide-catalyzed binding of aromatic hydrocarbons to DNA. Chem.-Biol. Interact. 47: 87–109

    Google Scholar 

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

    Google Scholar 

  • Cerniglia CE & Heitkamp MA (1989) Microbial degradation of polycyclic aromatic hydrocarbons (PAH) in the aquatic environment. In: Varanasi U (Ed) Metabolism of Polycyclic Aromatic Hydrocarbons in the Aquatic Environment (pp 41–68). CRC Press, Boca Raton, FL

    Google Scholar 

  • Collins PJ, Kotterman MJJ, Field JA & Dobson ADW (1996) Oxidation of anthracene and benzo[a]pyrene by laccases from Trametes versicolor. Appl. Environ. Microbiol. 62: 4563–4567

    Google Scholar 

  • Cremonesi P, Cavalieri EL & Rogan EG (1989) One-electron oxidation of 6-substituted benzo[a]pyrenes by manganic acetate. A model for metabolic activation. J. Org. Chem. 54: 3561–3570

    Google Scholar 

  • Davis MW, Glaser JA, Evans JW & Lamar RT (1993) Field evaluation of the lignin-degrading fungus Phanerochaete sordida to treat creosote-contaminated soil. Environ. Sci. Technol. 27: 2572–2576

    Google Scholar 

  • Felby C, Nielsen BR, Olesen PO & Skibsted LH (1997) Identification and quantification of radical reaction intermediates by electron spin resonance spectrometry of laccase-catalyzed oxidation of wood fibers from beech (Fagus sylvatica). Appl. Microbiol. Biotechnol. 48: 459–464

    Google Scholar 

  • Field JA, Feiken H, Hage A & Kotterman MJJ (1995a) Application of a white-rot fungus to biodegrade benzo[a]pyrene in soil. In: Hinchee RE, Fredrickson J & Alleman BC (Eds) Bioaugmentation for Site Remediation (pp 165–171). Battelle Press, Columbus, Ohio

    Google Scholar 

  • Field JA, Stams AJM, Kato M & Schraa G (1995b) Enhanced biodegradation of aromatic pollutants in cocultures of anaerobic and aerobic bacterial consortia. Antonie van Leeuwenhoek 67: 47–77

    Google Scholar 

  • Findlay M, Fogel S, Conway L & Taddeo A (1995) Field treatment of coal tar-contaminated soil based on results of laboratory treatability studies. In: Young LY & Cerniglia CE (Eds) Microbial Transformation and Degradation of Toxic Organic Chemicals (pp 487–513). Wiley-Liss, Inc., New York

    Google Scholar 

  • Gierer J, Yang E & Reitberger T (1992) The reaction of hydroxyl radicals with aromatic rings in lignin, studied with cresol and 4-methylveratrol. Holzforschung 46: 495–504

    Google Scholar 

  • Gramss G (1979) Role of soil mycelium in nutrition of wood-destroying basidiomycetous fungi on inoculated wood blocks in soil. J. Basic Microbiol. 19: 143–145

    Google Scholar 

  • Gramss G (1987) The influence of the concomitant microflora on establishment and dieback of decay fungi in standing timber. J. Phytopath. 120: 205–215

    Google Scholar 

  • Gramss G (1997) Activity of oxidative enzymes in fungal mycelia from grassland and forest soils. J. Basic Microbiol. 37: 407–423

    Google Scholar 

  • Hammel KE, Kalyanaraman B & Kirk TK (1986) Oxidation of polycyclic aromatic hydrocarbons and dibenzo[p]dioxins by Phanerochaete chrysosporium ligninase. J. Biol. Chem. 261: 16948–16952

    Google Scholar 

  • Hatzinger PB & Alexander M (1995) Effect of aging of chemicals in soil on their biodegradability and extractability. Environ. Sci. Technol. 29: 537–545

    Google Scholar 

  • Kanaly R, Bartha R, Fogel S & Findlay M (1997) Biodegradation of [14C]benzo[a]pyrene added in crude oil to uncontaminated soil. Appl. Environ. Microbiol. 63: 4511–4515

    Google Scholar 

  • Lamar RT, Davis MW, Dietrich DM & Glaser JA (1994) Treatment of a pentachlorophenol-and creosote-contaminated soil using the lignin-degrading fungus Phanerochaete sordida: A field demonstration. Soil Biol. Biochem. 26: 1603–1611

    Google Scholar 

  • Mabey WR, Smith JH, Podoll RT, Johnson HL, Mill T, Chou TW, Gates J, Partridge IW, Jaber H & Vandenberg D (1982) Aquatic fate processes for organic priority pollutants. U. S. Environmental Protection Agency, Washington, DC

    Google Scholar 

  • Mahro B & Kästner M (1993) The microbial degradation of polycyclic aromatic hydrocarbons in soils and sediments. BioEngineering 9: 50–58

    Google Scholar 

  • Masaphy S, Levanon D, Henis Y, Venkateswarlu K & Kelly SL (1995) Microsomal and cytosolic cytochrome P450 mediated benzo[a]pyrene hydroxylation in Pleurotus pulmonarius. Biotechnol. Lett. 17: 969–974

    Google Scholar 

  • Periasamy M & Vivekananda Bhatt M (1978) Facile oxidation of aromatic rings by Mn2(SO4)3. Tetrahedron Lett. 46: 4561–4562

    Google Scholar 

  • Sack U (1996) Abschlußbericht Verbundvorhaben Dekontamination von PAK-belasteten Böden durch Pilze. I. Screening von PAK-abbauenden Pilzen und Identifizierung der Metabolite. Friedrich-Schiller-Universität Jena, Biologisch-Pharmazeutische Fakultät, Jena

    Google Scholar 

  • Sack U, Hofrichter M & Fritsche W (1997) Degradation of polycyclic aromatic hydrocarbons by manganese peroxidase of Nematoloma frowardii. FEMS Microbiol. Lett. 152: 227–234

    Google Scholar 

  • Schinner F, Öhlinger R, Kandeler E & Margesin R (1993) Bodenbiologische Arbeitsmethoden, 2nd Ed. Springer, Berlin

    Google Scholar 

  • Schneider J, Grosser R, Jayasimhulu K, Xue W & Warshawsky D (1996) Degradation of pyrene, benzo[a]anthracene, and benzo[a]pyrene by Mycobacterium sp. strain RJG 11–135, isolated from a former coal gasification site. Appl. Environ. Microbiol. 62: 13–19

    Google Scholar 

  • Schomburg D, Salzmann M & Stephan D (1994) Enzyme Handbook. Vol. 1–10. Springer, Berlin

    Google Scholar 

  • Smith JD (1980) Is biologic control of Marasmius oreades fairy rings possible? Plant Disease 64: 348–354

    Google Scholar 

  • Wang TSC, Huang PM, Chou C-H & Chen J-H (1986) The role of soil minerals in the abiotic polymerization of phenolic compounds and formation of humic substances. In: Huang PM & Schnitzer M (Eds) Interactions of soil minerals with natural organics and microbes. Special Publication No. 17 (pp 251–281). Soil Sci. Soc. of America, Inc., Madison, Wisconsin

    Google Scholar 

  • Wilk M, Bez W & Rochlitz J (1966) Neue Reaktionen der carcinogenen Kohlenwasserstoffe 3,4-Benzpyren, 9,10-Dimethyl-1,2-benzanthracen und 20-Methylcholanthren. Tetrahedron 22: 2599–2608

    Google Scholar 

  • Wittmaier M, Harborth P & Hanert HH (1992) Biological activity, pollutant degradation and detoxification in soil highly contaminated with tar oil (> 100000 mg PAH/kg dry subst.) (pp 611–617). Internat. Symp. Soil Decontamination Using Biological Processes, Karlsruhe/D, 6–9 December 1992. DECHEMA, Frankfurt am Main

    Google Scholar 

  • Wolter M, Zadrazil F, Martens R & Bahadir M (1997) Degradation of eight highly condensed polycyclic aromatic hydrocarbons by Pleurotus sp. Florida in solid wheat straw substrate. Appl. Microbiol. Biotechnol. 48: 398–404

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Project Development Centre, Magdeburger Allee 134, D-99086, Erfurt, Germany

    Gerhard Gramss, Klaus-Dieter Voigt & Brigitta Kirsche

Authors
  1. Gerhard Gramss
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Klaus-Dieter Voigt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Brigitta Kirsche
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gramss, G., Voigt, KD. & Kirsche, B. Degradation of polycyclic aromatic hydrocarbons with three to seven aromatic rings by higher fungi in sterile and unsterile soils. Biodegradation 10, 51–62 (1999). https://doi.org/10.1023/A:1008368923383

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1008368923383

Search

Navigation