Abstract
Some strains of white rot fungi, non-lignolytic fungi and litter-decomposing basidiomycetes have been recognized as PAH degraders. The purpose of our research was to enlarge the scope of PAH-degrading fungi and explore the huge endophytic microorganism resource for bioremediation of PAHs. In this study, phenanthrene was used as a model PAHs compound. Nine strains of endophytic fungi isolated from four kinds of plant from Eupharbiaceae were screened for degradation of phenanthrene. The endophytic fungus Ceratobasidum stevensii (strain B6) isolated from Bischofia polycarpam showed high degradation efficiency and was selected for further studies. Into the fungal culture, 100 mg l−1 phenanthrene was added, and after 10 days of incubation, about 89.51% of the phenanthrene was removed by strain B6. Extracellular ligninolytic enzyme activities of strain B6 were tested. The results showed that manganese peroxidase [MnP] was the predominant ligninolytic enzyme and that its production was greatly induced by the presence of phenanthrene. To confirm the involvement of MnP in phenanthrene degradation, promotion and inhibition studies on MnP in different concentration level of Mn2+ and NaN3 were performed. Additionally, fungal mycelium-free and resuspended experiments were carried out. The results showed no apparent correlation between MnP activity and phenanthrene degradation. The mycelium and fresh medium were the crucial factors affecting the degradation of phenanthrene. To date, this is the first report on PAH degradation by Ceratobasidum stevensii. This study suggests that endophytic fungi might be a novel and important resource for microorganisms that have PAH-degrading capabilities.
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References
Bezalel L, Hadar Y, Fu PP, Freeman JP, Cerniglia CE (1996a) Metabolism of phenanthrene by the white rot fungus Pleurotus ostreatus. Appl Environ Microbiol 62:2547–2553
Bezalel L, Hadar Y, Fu PP, Cerniglia CE (1996b) Mineralization of polycyclic aromatic hydrocarbons by the white rot fungus Pleurotus ostreatus. Appl Microbiol Biotechnol 62:292–295
Bogan BW, Lamar RT (1996) Polycyclic aromatic hydrocarbon degrading capabilities of Phanerochaete laevis HHB-1625 and its extracellular ligninolytic enzymes. Appl Environ Microbiol 62:1597–1603
Cajthaml T, Moder MP, 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 974:213–222
Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351–368
Cerniglia CE (1997) Fungal metabolism of polycyclic aromatic hydrocarbons: past, present and future applications in bioremediation. J Microbiol Biotechnol 19:324–333
Clemente AR, Anazawa TA, Durrant LR (2001) Biodegradation of polycyclic aromatic hydrocarbons by soil fungi. Braz J Microbiol 32:255–261
Dai CC, Yu BY, Wang XF, Jiang JH, Shi Y (2006) Identification of endophytic fungi killing Pieris rapae and primary determination of its chemical matter. J Anhui Agric Sci (in Chinese) 34(4):694–697
Darlington AB, Dat JF, Dixon MA (2001) The biofiltration of indoor air: air flux and temperature influences the removal of toluene, ethylbenzene, and xylene. Environ Sci Technol 35:240–246
De Kempeneer L, Sercu B, Vanbrabant W, Van Langenhove H, Verstraete W (2004) Bioaugmentation of the phyllosphere for the removal of toluene from indoor air. Appl Microbiol Biotechnol 64:284–288
Dhawale SW, Dhawale SS, Dean-Ross D (1992) Degradation of phenanthrene by Phanerochaete chrysosporium occurs under ligninolytic as well as nonligninolytic conditions. Appl Environ Microbiol 58:3000–3006
Eibes GT, Lu-Chau TL, Feijoo G, Moreira MT, Lema JM (2005) Complete degradation of anthracene by manganese peroxidase in organic solvent mixtures. Enzyme Microb Technol 37:365–372
Field AJ, de Jong E, Feijoo-Costa FE, de Bont JAM (1993) Screening for ligninolytic fungi applicable to the biodegradation of xenobiotics. Trends Biotechnol 11:44–49
Gramss G, Kirsche B, Voigt K-D, Gunther T, Fritsche W (1999) Conversion rates of five polycyclic aromatic hydrocarbons in liquid cultures of fifty-eight fungi and the concomitant production of oxidative enzymes. Mycol Res 103:1009–1018
Hallsworth JE, Nomura Y (1999) A simple method to determine the water activity of ethanol-containing samples. Biotechnol Bioeng 62:242–245
Hallsworth JE, Heim S, Timmis KN (2003) Chaotropic solutes cause water stress in Pseudomonas putida. Environ Microbiol 5:1270–1280
Hallsworth JE, Yakimov MM, Golyshin PN, Gillion JLM, D’Auria G, Alves FL, Cono VL, Genovese M, McKew BA, Hayes SL, Harris G, Giuliano L, Timmis KN, McGenity TJ (2007) Limits of life in MgCl2-containing environments: chaotropicity defines the window. Environ Microbiol 9:801–813
Hamman OB, De la Rubia T, Martınez J (1999) The effect of manganese on the production of Phanerochaete flavidoalba ligninolytic peroxidases in nitrogen limited cultures. FEMS Microbiol Lett 177:137–142
Han MJ, Choi HT, Song HG (2004) Degradation of phenanthrene by Trametes versicolor and its laccase. J Microbiol 42:94–98
Hofrichter M, Scheibener K, Schneegab I, Fritsche W (1998) Enzymatic combustion of aromatic and aliphatic compounds by manganese peroxidase from Nematoloma frowardii. Appl Environ Microbiol 64:399–404
Jordaan A, Taylor JE, Rossenkhan R (2006) Occurrence and possible role of endophytic fungi associated with seed pods of Colophospermum mopane (Fabaceae) in Botswana. S Afr J Bot 72:245–255
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 45:57–88
Kashangura C, Hallsworth JE, Mswaka AY (2006) Phenotypic diversity amongst strains of Pleurotus sajor-caju: implications for cultivation in arid environments. Mycol Res 110:312–317
Kim MS, Huh EJ, Kim HK, Moon KW (1998) Degradation of polycyclic aromatic hydrocarbons by selected white-rot fungi and the influence of lignin peroxidase. J Microbiol Biotechnol 8:129–133
Kishi K, Wariishi H, Marquez L, Dunford HB, Gold MH (1994) Mechanism of manganese peroxidase compound II reduction. Effect of organic acid chelators and pH. Biochemistry 33:8694–8701
Koide K, Osono T, Takeda H (2005) Colonization and lignin decomposition of Camellia japonica leaf litter by endophytic fungi. Mycoscience 46:280–286
Magan N, Mswaka AY (1998) Wood degradation, and cellulase and ligninase production, by Trametes and other wood-inhabiting basidiomycetes from indigenous forests of Zimbabwe. Mycol Res 102:1399–1404
Mori T, Kitano S, Kondo R (2003) Biodegradation of chloronaphthalenes and polycyclic aromatic hydrocarbons by the white-rot fungus Phlebia lindtneri. Appl Microbiol Biotechnol 61:380–383
Paszczynski A, Crawford RL (1995) Potential for bioremediation of xenobiotic compounds by the white-rot fungus Phanerochaete chrysosporium. Biotechnol Prog 11:368–379
Petrini LE, Petrini O, Leuchtmann A, Carroll GC (1991) Conifer inhabiting species of phyllosticta. Sydowia 43:148–169
Pickard MA, Roman R, Tinoco R, Vazquez-Duhalt R (1999) Polycyclic aromatic hydrocarbon metabolism by white rot fungi and oxidation by Coriolopsis gallica UAMH 8260 laccase. Appl Environ Microbiol 65:3805–3809
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 51:71–78
Salvo VS, Gallizia I, Moreno M, Fabiano M (2005) Fungal communities in PAH-impacted sediments of Genoa-Voltri Harbour (NW Mediterranean, Italy). Mar Pollut Bull 50:553–559
Sandhu A, Halverson LJ, Beattie GA (2007) Bacterial degradation of airborne phenol in the phyllosphere. Environ Microbiol 9:383–392
Shi Y, Dai CC, Lu L, Yu BY (2002) Comparison of the extracellular enzyme activities of the endophytic fungi in four species of medicinal plants from Euphorbiaceae. J Plant Resour Environ (in Chinese) 11(2):17–20
Steffen KT, Hatakka A, Hofrichter M (2002) Removal and mineralization of polycyclic aromatic hydrocarbons by litter-decomposing basidiomycetous fungi. Appl Microbiol Biotechnol 60:212–217
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 69:3957–3964
Steffen KT, Schubert S, Tuomela M, Hatakka A, Hofrichter M (2007) Enhancement of bioconversion of high-molecular mass polycyclic aromatic hydrocarbons in contaminated non-sterile soil by litter-decomposing fungi. Biodegradation 18:359–369
Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67:491–502
Tekere M, Mswaka AY, Zvauya R, Read JS (2001) Growth, dye degradation and ligninolytic activity studies on Zimbabwean white rot fungi. Enzyme Microb Tech 28:420–426
Terrazas E, Alvarez T, Benoit G, Mattiasson B (2005) Isolation and characterization of a white rot fungus Bjerkandera sp. strain capable of oxidizing phenanthrene. Biotechnol Lett 27:845–851
Tian LS, Dai CC, Zhao YT, Zhao M, Yong YH, Wang XX (2007) The degradation of phenanthrene by endophytic fungi Phomopsis sp. single and co-cultured with rice. Chin Environ Sci (in Chinese) 27(6):757–762
Tien M, Kirk TK (1983) Lignin degrading from Phanerochaete chrysosporium: purification, characterization and catalytic properties of unique H2O2-requiring oxygenase. Proc Natl Acad Sci 81:2280–2284
Verdin A, Sahraoui AL, Durand R (2004) Degradation of benzo[a]pyrene by mitosporic fungi and extracellular oxidative enzymes. Int Biodeter Biodeger 53:65–70
Waight K, Pinyakong O, Luepromchai E (2007) Degradation of phenanthrene on plant leaves by phyllosphere bacteria. J Gen Appl Microbiol 53:265–272
Wang JW, Wu JH, Huang WY, Tan RX (2006) Laccase production by Monotospora sp., an endophytic fungus in Cynodon dactylon. Bioresour Technol 97:786–789
Wariishi H, Valli K, Gold MH (1992) Manganese(II) oxidation by manganese peroxidase from the basidiomycete Phanerochaete chrysosporium. J Biol Chem 267:23688–23695
Wolfenden BS, Wilson RL (1982) Radical-cations as reference chromogens in kinetic studies of one-electron transfer reactions. J Chem Soc-Perkin Trans 2:805–812
Yuan ZL, Dai CC, Li X, Tian LS, Wang XX (2007) Extensive host range of an endophytic fungus affects the growth and physiological functions in rice (Oryza sativa L.). Symbiosis 43:21–28
Zheng ZM, Obbard JP (2002) Oxidation of polycyclic aromatic hydrocarbons (PAH) by the white rot fungus, Phanerochaete chrysosporium. Enzyme Microb Technol 31:3–9
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This work was financially supported by the National Natural Science Foundation of China (No. 30770073, 30500066). The authors express their great thanks to reviewers and the editorial staff for their time and attention.
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Dai, Cc., Tian, Ls., Zhao, Yt. et al. Degradation of phenanthrene by the endophytic fungus Ceratobasidum stevensii found in Bischofia polycarpa . Biodegradation 21, 245–255 (2010). https://doi.org/10.1007/s10532-009-9297-4
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DOI: https://doi.org/10.1007/s10532-009-9297-4