Degradation and Mineralization of High-Molecular-Weight Polycyclic Aromatic Hydrocarbons by Defined Fungal-Bacterial Cocultures

ABSTRACT This study investigated the biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons (PAHs) in liquid media and soil by bacteria (Stenotrophomonas maltophilia VUN 10,010 and bacterial consortium VUN 10,009) and a fungus (Penicillium janthinellum VUO 10,201) that were isolated from separate creosote- and manufactured-gas plant-contaminated soils. The bacteria could use pyrene as their sole carbon and energy source in a basal salts medium (BSM) and mineralized significant amounts of benzo[a]pyrene cometabolically when pyrene was also present in BSM. P. janthinellum VUO 10,201 could not utilize any high-molecular-weight PAH as sole carbon and energy source but could partially degrade these if cultured in a nutrient broth. Although small amounts of chrysene, benz[a]anthracene, benzo[a]pyrene, and dibenz[a,h]anthracene were degraded by axenic cultures of these isolates in BSM containing a single PAH, such conditions did not support significant microbial growth or PAH mineralization. However, significant degradation of, and microbial growth on, pyrene, chrysene, benz[a]anthracene, benzo[a]pyrene, and dibenz[a,h]anthracene, each as a single PAH in BSM, occurred when P. janthinellum VUO 10,201 and either bacterial consortium VUN 10,009 or S. maltophilia VUN 10,010 were combined in the one culture, i.e., fungal-bacterial cocultures: 25% of the benzo[a]pyrene was mineralized to CO2 by these cocultures over 49 days, accompanied by transient accumulation and disappearance of intermediates detected by high-pressure liquid chromatography. Inoculation of fungal-bacterial cocultures into PAH-contaminated soil resulted in significantly improved degradation of high-molecular-weight PAHs, benzo[a]pyrene mineralization (53% of added [14C]benzo[a]pyrene was recovered as14CO2 in 100 days), and reduction in the mutagenicity of organic soil extracts, compared with the indigenous microbes and soil amended with only axenic inocula.

[1]  M. Tien,et al.  Oxidation of persistent environmental pollutants by a white rot fungus. , 1985, Science.

[2]  R. Legge,et al.  Enhanced biodegradation of phenanthrene in oil tar-contaminated soils supplemented with Phanerochaete chrysosporium , 1992, Applied and environmental microbiology.

[3]  H. Rijnaarts,et al.  Partially oxidized polycyclic aromatic hydrocarbons show an increased bioavailability and biodegradability. , 1997, FEMS microbiology letters.

[4]  M. Britz,et al.  Surfactant-enhanced biodegradation of high molecular weight polycyclic aromatic hydrocarbons by stenotrophomonas maltophilia , 1998, Biotechnology and bioengineering.

[5]  A. Juhasz,et al.  Degradation of fluoranthene, pyrene, benz[a]anthracene and dibenz[a,h]anthracene by Burkholderia cepacia , 1997 .

[6]  M. Kästner,et al.  Enumeration and characterization of the soil microflora from hydrocarbon-contaminated soil sites able to mineralize polycyclic aromatic hydrocarbons (PAH) , 1994, Applied Microbiology and Biotechnology.

[7]  A. Tiehm,et al.  Degradation of phenanthrene, fluorene, fluoranthene, and pyrene by a Mycobacterium sp , 1993, Applied and environmental microbiology.

[8]  B. Ames,et al.  Revised methods for the Salmonella mutagenicity test. , 1983, Mutation research.

[9]  Y. Hadar,et al.  Initial Oxidation Products in the Metabolism of Pyrene, Anthracene, Fluorene, and Dibenzothiophene by the White Rot Fungus Pleurotus ostreatus , 1996, Applied and environmental microbiology.

[10]  P J Chapman,et al.  Isolation and characterization of a fluoranthene-utilizing strain of Pseudomonas paucimobilis , 1990, Applied and environmental microbiology.

[11]  T. Wunder,et al.  1-Methoxypyrene and 1,6-dimethoxypyrene: two novel metabolites in fungal metabolism of polycyclic aromatic hydrocarbons , 1997, Archives of Microbiology.

[12]  D. Warshawsky,et al.  Mineralization of polycyclic and N‐heterocyclic aromatic compounds in hydrocarbon‐contaminated soils , 1995 .

[13]  J. Bumpus Biodegradation of polycyclic hydrocarbons by Phanerochaete chrysosporium , 1989, Applied and environmental microbiology.

[14]  D. Warshawsky,et al.  Degradation of Pyrene, Benz[a]anthracene, and Benzo[a]pyrene by Mycobacterium sp. Strain RJGII-135, Isolated from a Former Coal Gasification Site , 1996, Applied and environmental microbiology.

[15]  C. Cerniglia,et al.  Pyrene degradation by a Mycobacterium sp.: identification of ring oxidation and ring fission products , 1988, Applied and environmental microbiology.

[16]  M. Moore,et al.  The biotransformation of chrysene to trans-1,2-dihydroxy-1,2-dihydrochrysene by filamentous fungi , 1996 .

[17]  C. Cerniglia,et al.  Fungal oxidation of benzo[a]pyrene and (+/-)-trans-7,8-dihydroxy-7,8-dihydrobenzo[a]pyrene. Evidence for the formation of a benzo[a]pyrene 7,8-diol-9,10-epoxide. , 1980, The Journal of biological chemistry.

[18]  B. Lake,et al.  The sorption of PAH onto dissolved organic matter in Lake Michigan waters , 1986 .

[19]  R. Kanaly,et al.  Biodegradation of [(sup14)C]Benzo[a]pyrene Added in Crude Oil to Uncontaminated Soil , 1997, Applied and environmental microbiology.

[20]  M. Leisola,et al.  Role of extracellular ligninases in biodegradation of benzo(a)pyrene by Phanerochaete chrysosporium , 1986 .

[21]  P. Collins,et al.  Oxidation of Anthracene and Benzo[a]pyrene by Laccases from Trametes versicolor , 1996, Applied and environmental microbiology.

[22]  K. Jones,et al.  Bioremediation of soil contaminated with polynuclear aromatic hydrocarbons (PAHs): a review. , 1993, Environmental pollution.

[23]  A. Badr Cytogenetic activities of a triazine herbicide in root tips of Allium cepa and Vicia faba , 1983 .

[24]  Hak-Sung Kim,et al.  Degradation of Chloronitrobenzenes by a Coculture of Pseudomonas putida and a Rhodococcussp , 1999, Applied and Environmental Microbiology.

[25]  William A. Telliard,et al.  PRIORITY POLLUTANTS I-A PERSPECTIVES VIEW , 1979 .

[26]  V. Šašek,et al.  Degradation of anthracene by selected white rot fungi , 1994 .

[27]  C. Cerniglia,et al.  Oxidation of benzo[a]pyrene by the filamentous fungus Cunninghamella elegans. , 1979, The Journal of biological chemistry.

[28]  D. Jerina,et al.  Oxidation of the carcinogens benzo [a] pyrene and benzo [a] anthracene to dihydrodiols by a bacterium. , 1975, Science.

[29]  Alexander E. Maccubbin,et al.  Degradation of Polynuclear Aromatic Hydrocarbons by Sphingomonas paucimobilis , 1996 .

[30]  T. Henrysson,et al.  Accumulation and degradation of dead-end metabolites during treatment of soil contaminated with polycyclic aromatic hydrocarbons with five strains of white-rot fungi , 1996, Applied Microbiology and Biotechnology.

[31]  B. W. Bogan,et al.  Polycyclic aromatic hydrocarbon-degrading capabilities of Phanerochaete laevis HHB-1625 and its extracellular ligninolytic enzymes , 1996, Applied and environmental microbiology.

[32]  D. Warshawsky,et al.  Indigenous and enhanced mineralization of pyrene, benzo[a]pyrene, and carbazole in soils , 1991, Applied and environmental microbiology.

[33]  O. Ward,et al.  Degradation of polycyclic aromatic hydrocarbons (PAHs) by a mixed culture and its component pure cultures, obtained from PAH-contaminated soil. , 1995, Canadian journal of microbiology.

[34]  C. Cerniglia,et al.  Transformation of chrysene and other polycyclic aromatic hydrocarbon mixtures by the fungus Cunninghamella elegans , 1995 .

[35]  M. Moore,et al.  The oxidation of pyrene and benzo[a]pyrene by nonbasidiomycete soil fungi. , 1995, Canadian journal of microbiology.

[36]  J. Sleigh Microbiological Methods , 1990 .

[37]  J. Foght,et al.  A method for monitoring mineralization of 14C-labeled compounds in aqueous samples , 1982 .

[38]  C. Cerniglia,et al.  Comparison of phenanthrene and pyrene degradation by different wood-decaying fungi , 1997, Applied and environmental microbiology.

[39]  J. Field,et al.  Successive Mineralization and Detoxification of Benzo[a]pyrene by the White Rot FungusBjerkandera sp. Strain BOS55 and Indigenous Microflora , 1998, Applied and Environmental Microbiology.