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Exploring micromycetes biodiversity for screening benzo[a]pyrene degrading potential

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Abstract

Twenty-five strains of filamentous fungi, encompassing 14 different species and belonging mainly to Ascomycetes, were tested for their ability to degrade benzo[a]pyrene (BaP) in mineral liquid medium. The most performing isolates for BaP degradation (200 mg l−1) in mineral medium were Cladosporium sphaerospermum with 29 % BaP degradation, i.e., 82.8 μg BaP degraded per day (day−1), Paecilomyces lilacinus with 20.5 % BaP degradation, i.e., 58.5 μg BaP day−1, and Verticillium insectorum with 22.3 % BaP degradation, i.e., 64.3 μg BaP day−1, after only 7 days of incubation. Four variables, e.g., biomass growth on hexadecane and glucose, BaP solubilization, activities of extracellular- and mycelium-associated peroxidase, and polyethylene glycol degradation, were also studied as selective criteria presumed to be involved in BaP degradation. Among these variables, the tests based on polyethylene glycol degradation and on fungal growth on hexadecane and glucose seemed to be the both pertinent criteria for setting apart isolates competent in BaP degradation, suggesting the occurrence of different mechanisms presumed to be involved in pollutant degradation among the studied micromycetes.

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References

  • April TM, Foght 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  CAS  Google Scholar 

  • Barclay CD, Farquhar GF, Legge RL (1995) Biodegradation and sorption of polyaromatic hydrocarbons by Phanerochaete chrysosporium. Appl Microbiol Biotechnol 42:958–963

    Article  CAS  Google Scholar 

  • Barnett HL, Hunter BB (1998) Illustrated genera of imperfect fungi, 4th edn. APS, St. Paul, p 218

    Google Scholar 

  • Bennett JW, Faison BD (1997) Use of fungi in biodegradation. In: Hurst CJ (ed) Manual of environmental microbiology. American Society for Microbiology, Washington, pp 758–765

    Google Scholar 

  • Bhadury P, Bridge PD, Austen MC, Bilton DT, Smerdon GR (2009) Detection of fungal 18S rRNA sequences in conjunction with marine nematode 18S rRNA amplicons. Aquatic Biol 5:149–155

    Article  Google Scholar 

  • Bogan BW, Trbovic V, Paterek JR (2003) Inclusion of vegetable oils in Fenton’s chemistry for remediation of PAH-contaminated soils. Chemosphere 50:15–21

    Article  CAS  Google Scholar 

  • Cajthaml T, Erbanova P, Kollmann A, Novotny C, Sasek V, Mougin C (2008) Degradation of PAHs by ligninolytic enzymes in Irpex lacteus. Folia Microbiol 53:289–294

    Article  CAS  Google Scholar 

  • Cerniglia CE, Gibson DT (1979) Oxidation of benzo[a]pyrene by the filamentous fungus Cunninghamella elegans. J Biol Chem 254:12174–12180

    CAS  Google Scholar 

  • Cerniglia CE (1993) Biodegradation of polycyclic aromatic hydrocarbons. Curr Opin Biotechnol 4:331–338

    Article  CAS  Google Scholar 

  • Chulalaksananukul S, Gadd GM, Sangvanich P, Sihanonth P, Piapukiew J, Vangnai AS (2006) Biodegradation of benzo[a]pyrene by a newly isolated Fusarium sp. FEMS Microbiol Lett 262:99–106

    Article  CAS  Google Scholar 

  • Cooney JJ, Siporin C, Smucker RA (1980) Physiological and cytological responses to hydrocarbons by the hydrocarbon-using fungus Cladosporium resinae. Bot Mar 23:227–232

    CAS  Google Scholar 

  • Covino S, Svobodova K, Kresinova Z, Petruccioli M, Federici F, D’Annibale A, Cvancarova M, Cajthaml T (2010) In vivo and in vitro polycyclic aromatic hydrocarbons degradation by Lentinus (Panus) tigrinus CBS 577.79. Bioresource Technol 101:3004–3012

    Article  CAS  Google Scholar 

  • Fernández-Luqueño F, Valenzuela-Encinas C, Marsch R, Martínez-Suárez C, Vázquez-Núñez E, Dendooven L (2011) Microbial communities to mitigate contamination of PAHs in soil—possibilities and challenges: a review. Environ Sci Pollut Res 18:12–30

    Article  Google Scholar 

  • Gadd GM (2001) Fungi in bioremediation. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Gesell M, Hammer E, Specht M, Francke W, Schauer F (2001) Biotransformation of biphenyl by Paecilomyces lilacinus characterization of ring cleavage products. Appl Environ Microbiol 67:1551–1557

    Article  CAS  Google Scholar 

  • Hadibarata T, Kristanti RA (2012) Fate and cometabolic degradation of benzo[a]pyrene by white-rot fungus Armillaria sp. F022. Bioresour Technol 107:314–318

    Article  CAS  Google Scholar 

  • Hammel KE, Kapich AN, Jensen KA, Ryan ZC (2002) Reactive oxygen species as agents of wood decay by fungi. Enzyme Microb Technol 30:445–453

    Article  CAS  Google Scholar 

  • Hong JW, Park JY, Gadd GM (2009) Pyrene degradation and copper and zinc uptake by Fusarium solani and Hypocrea lixii isolated from petrol station soil. J Appl Microb 108:2030–2040

    Google Scholar 

  • Howard RJ, Ferrari MA, Roach DH, Money NP (1991) Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc Natl Acad Sci 88:11281–11284

    Article  CAS  Google Scholar 

  • Juhasz AL, Naidu R (2000) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. Int Biodeterior Biodegrad 45:54–88

    Article  Google Scholar 

  • Kiffer E, Morelet M (1997) Les Deutéromycètes. Classification et clés d’identification générique. INRA, Paris, p 306

    Google Scholar 

  • Kwon SI, Anderson AJ (2001) Laccase isozymes: production by an opportunistic pathogen, a Fusarium proliferatum isolate from wheat. Physiol Mol Plant Pathol 59:235–242

    Article  CAS  Google Scholar 

  • Lindley ND, Heydeman MT (1983) Uptake of vapour phase [14C]dodecane by whole mycelia of Cladosporium resinae. J Gen Microbiol 129:2301–2305

    CAS  Google Scholar 

  • Machín-Ramírez C, Morales D, Martínez-Morales F, Okoh AI, Trejo-Hernández MR (2010) Benzo[a]pyrene removal by axenic- and co-cultures of some bacterial and fungal strains. Int Biodeterior Biodegrad 64:538–544

    Article  Google Scholar 

  • Majeau JA, Brar SK, Tyagi RD (2010) Laccases for removal of recalcitrant and emerging pollutants. Bioresource Technol 101:2331–2350

    Article  CAS  Google Scholar 

  • Malagnac F, Lalucque H, Lepère G, Silar P (2004) Two NADPH oxidase isoforms are required for sexual reproduction and ascospore germination in the filamentous fungus Podospora anserina. Fungal Genet Biol 41:982–997

    Article  CAS  Google Scholar 

  • Money NP (1990) Measurement of pore size in the hyphal cell wall of Achlya bisexualis. Exp Mycol 14:234–242

    Article  Google Scholar 

  • Pacioni G, Leonardi M, Aimola P, Ragnelli AM, Rubini A, Paolocci F (2007) Isolation and characterization of some mycelia inhabiting Tuber ascomata. Mycol Res 111:1450–1460

    Article  CAS  Google Scholar 

  • Pointing SB (2001) Feasibility of bioremediation by white-rot fungi. Appl Microbiol Biotechnol 57:20–33

    Article  CAS  Google Scholar 

  • Potin O, Rafin C, Veignie E (2004a) 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 

  • Potin O, Veignie E, Rafin C (2004b) Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by Cladosporium sphaerospermum isolated from an aged PAH contaminated soil. FEMS Microbiol Ecol 51:71–78

    Article  CAS  Google Scholar 

  • Puntus IF, Sakharovsky VG, Filonov AE, Boronin AM (2005) Surface activity and metabolism of hydrocarbon-degrading microorganisms growing on hexadecane and naphthalene. Process Biochem 40:2643–2648

    Article  CAS  Google Scholar 

  • Prenafeta-Boldu FX, Kuhn A, Luykx D, Anke H, van Groenestijn JW, Debont JAM (2001) Isolation and characterisation of fungi growing on volatile aromatic hydrocarbons as their sole carbon and energy source. Mycol Res 105:477–484

    Article  CAS  Google Scholar 

  • Rafin C, Potin O, Veignie E, Lounes-Hadj Sahraoui A, Sancholle M (2000) Degradation of benzo[a]pyrene as sole carbon source by a non white rot fungus, Fusarium solani. Polycycl Aromat Comp 21:311–329

    Article  CAS  Google Scholar 

  • Rafin C, Veignie E, Woisel P, Cazier F, Surpateanu G (2006) New potential of a deuteromycete fungus Fusarium solani in benzo[a]pyrene degradation: an eco-physiological hypothesis? In: Glazer MP (ed) New frontiers in environmental research. Nova Science, New York, pp 165–179

    Google Scholar 

  • Regalado V, Perestelo F, Rodriguez A, Carnicero A, Sosa FJ, Delafuente G, Falcon MA (1999) Activated oxygen species and two extracellular enzymes: laccase and aryl-alcohol oxidase, novel for the lignin-degrading fungus Fusarium proliferatum. Appl Microbiol Biotechnol 51:388–390

    Article  CAS  Google Scholar 

  • Rogerson CT, Stephenson SL (1993) Myxomyceticolous fungi. Mycologia 85:456–469

    Article  Google Scholar 

  • Romero MC, Salvioli ML, Cazau MC, Arambarri AM (2002) Pyrene degradation by yeasts and filamentous fungi. Environ Pollut 117:159–163

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Seghezzi W, Sanglard D, Fiechter A (1991) Characterization of a second alkane-inducible cytochrome P450-encoding gene, Cyp52A2, from Candida tropicalis. Gene 106:51–60

    Article  CAS  Google Scholar 

  • Silva IS, Grossman M, Durrant LR (2009) Degradation of polycyclic aromatic hydrocarbons (2–7 rings) under microaerobic and very-low-oxygen conditions by soil fungi. Int Biodeterior Biodegrad 63:224–229

    Article  CAS  Google Scholar 

  • Singh H (2007) Mycoremediation: fungal bioremediation. Wiley, Hoboken

    Google Scholar 

  • Sutherland JB (1992) Detoxification of polycyclic aromatic hydrocarbons by fungi. J Ind Microbiol 9:53–62

    Article  CAS  Google Scholar 

  • Terao J, Lim BP, Murakami H, Matsushita S (1987) Quinone formation from carcinogenic benzo[a]pyrene mediated by lipid peroxidation in phosphatidylcholine liposomes. Arch Biochem Biophys 254:472–481

    Article  CAS  Google Scholar 

  • Thion C, Cébron A, Beguiristain T, Leyval C (2012) PAH biotransformation and sorption by Fusarium solani and Arthrobacter oxydans isolated from a polluted soil in axenic cultures and mixed co-cultures. Int Biodeterior Biodegrad 68:28–35

    Article  CAS  Google Scholar 

  • van den Brink HJM, van Gorcom RFM, van den Hondel CAJJ, Punt PJ (1998) Review: cytochrome P450 enzyme systems in fungi. Fungal Genet Biol 23:1–17

    Article  Google Scholar 

  • Veignie E, Rafin C, Woisel P, Lounes-Hadj Sahraoui A, Cazier F (2002) Metabolization of the polycyclic aromatic hydrocarbon benzo[a]pyrene by a non-white rot fungus (Fusarium solani) in a batch reactor. Polycycl Aromat Comp 22:87–97

    Article  CAS  Google Scholar 

  • Veignie E, Rafin C, Woisel P, Cazier F (2004) Preliminary evidence of the role of hydrogen peroxide in the degradation of benzo[a]pyrene by a non-white rot fungus Fusarium solani. Environ Pollut 129:1–4

    Article  CAS  Google Scholar 

  • Veignie E, Rafin C, Landy D, Fourmentin S, Surpateanu G (2009) Fenton degradation assisted by cyclodextrins of a high molecular weight polycyclic aromatic hydrocarbon benzo[a]pyrene. J Hazard Mater 168:1296–1301

    Article  CAS  Google Scholar 

  • Vigueras G, Shirai K, Martins D, Franco TT, Fleuri LF, Revah S (2008) Toluene gas phase biofiltration by Paecilomyces lilacinus and isolation and identification of a hydrophobin protein produced thereof. Appl Microbiol Biotechnol 80:147–154

    Article  CAS  Google Scholar 

  • Weber FJ, Hage KC, Debont JAM (1995) Growth of the fungus Cladosporium sphaerospermum with toluene as the sole carbon and energy source. Appl Environ Microbiol 61:3562–3566

    CAS  Google Scholar 

  • Wright H, Nicell JA (1999) Characterization of soybean peroxidase for the treatment of aqueous phenols. Bioresource Technol 70:69–79

    Article  CAS  Google Scholar 

  • Wu Y, Teng Y, Li Z, Liao X, Luo Y (2008) 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 

  • Wu YR, He TT, Lun JS, Maskaoui K, Huang TW, Hu Z (2009) Removal of benzo[a]pyrene by a fungus Aspergillus sp. BAP14. World J Microbiol Biotechnol 25:1395–1401

    Article  CAS  Google Scholar 

  • Wunder T, Kremer S, Sterner O, Anke H (1994) Metabolism of the polycyclic aromatic hydrocarbon pyrene by Aspergillus niger S K 9317. Appl Microbiol Biotechnol 42:636–641

    Article  CAS  Google Scholar 

  • Zalar P, de Hoog GS, Schroers HJ, Crous PW, Groenewald JZ, Gunde-Cimerman N (2007) Phylogeny and ecology of the ubiquitous saprobe Cladosporium sphaerospermum with descriptions of seven new species from hypersaline environments. Stud Mycol 58:157–183

    Article  CAS  Google Scholar 

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The authors thank S. Bones for help in English revision of this article.

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Correspondence to Catherine Rafin.

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Responsible editor: Robert Duran

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Rafin, C., de Foucault, B. & Veignie, E. Exploring micromycetes biodiversity for screening benzo[a]pyrene degrading potential. Environ Sci Pollut Res 20, 3280–3289 (2013). https://doi.org/10.1007/s11356-012-1255-8

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