Synergistic degradation of pyrene and volatilization of arsenic by cocultures of bacteria and a fungus

Abstract

The combination of two bacteria (Bacillus sp. PY1 and Sphingomonas sp. PY2) and a fungus (Fusarium sp. PY3), isolated from contaminated soils near a coking plant, were investigated with respect to their capability to degrade pyrene and volatilize arsenic. The results showed that all strains could use pyrene and arsenic as carbon and energy sources in a basal salts medium (BSM), with the combined potential to degrade pyrene and volatilize arsenic. Bacillus sp. PY1, Sphingomonas sp. PY2 and Fusarium sp. PY3 were isolated from the consortium and were shown to degrade pyrene and volatilize arsenic independently and in combination. Fungal-bacterial coculture has shown that the most effective removal of pyrene was 96.0% and volatilized arsenic was 84.1% after incubation in liquid medium after 9 days culture, while bioremediation ability was 87.2% in contaminated soil with 100 mg·kg^-1 pyrene. The highest level of arsenic volatilization amounted to 13.9% of the initial As concentration in contaminated soil after 63 days. Therefore, a synergistic degradation system is the most effective approach to degrade pyrene and remove arsenic in contaminated soil. These findings highlight the role of these strains in the bioremediation of environments contaminated with pyrene and arsenic.

Keywords

pyrene / arsenic / bioremediation / bacteria / fungus

References

[1] Keith L H, Telliard W A. ES&T special report: priority pollutants I–a perspective view. Environmental Science and Technology, 1979, 13(4): 416–423

[2] Karagas M R, Tosteson T D, Blum J, Morris J S, Baron J A, Klaue B. Design of an epidemiologic study of drinking water arsenic exposure and skin and bladder cancer risk in a U.S. population. Environmental Health Perspectives, 1998, 106(Suppl 4): 1047–1050

[3] Maier A, Schumann B L, Chang X Q, Talaska G, Puga A. Arsenic co-exposure potentiates benzo[a]pyrene genotoxicity. Mutation Research, 2002, 517(1–2): 101–111

[4] Atlas R M, Cerniglia C E. Bioremediation of petroleum pollutants. Bioscience, 1995, 45(5): 332–339

[5] Wilson S C, Jones K C. Bioremediation of soil contaminated with polynuclear aromatic hydrocarbons (PAHs): a review. Environmental Pollution, 1993, 81(3): 229–249

[6] Cerniglia C E, Heitkamp M A. Microbial degradation of polycyclic aromatic hydrocarbons in the aquatic environment. In: Varanasi U ed. Metabolism of Polycyclic Aromatic Hydrocarbons in the Aquatic Environment. Boca Raton: CRC Press, 1989

[7] Cerniglia C E. Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation, 1992, 3(2–3): 351–368

[8] Aitken M D, Stringfellow W T, Nagel R D, Kazunga Ch, Chen S H. Characteristics of phenanthrene-degrading bacteria isolated from soils contaminated with polycyclic aromatic hydrocarbons. Canadian Journal of Microbiology, 1998, 44(8): 743–752

[9] Potin O, Rafin C, Veignie E. Bioremediation of an aged polycyclic aromatic hydrocarbons (PAHs)-contaminated soil by filamentous fungi isolated from the soil. International Biodeterioration and Biodegradation, 2004, 54(1): 45–52

[10] Juhasz A L, Naidu R. Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. International Biodeterioration and Biodegradation, 2000, 45(1–2): 57–88

[11] Säsëk V, Glaser J A, Baveye P. The utilization of bioremediation to reduce soil contamination: problems and solution. Nato Science Series, IV. Earth and Environ Sciences. Kluwer Academic Publishers, Dordrecht, 2003

[12] Jakob R, Roth A, Haas K, Krupp E M, Raab A, Smichowski P, Gómez D, Feldmann J. Atmospheric stability of arsines and the determination of their oxidative products in atmospheric aerosols (PM₁₀): evidence of the widespread phenomena of biovolatilization of arsenic. Journal of Environmental Monitoring, 2010, 12(2): 409–416

[13] Cox D P, Alexander M. Effect of phosphate and other anions on trimethylarsine formation by Candida humicola. Applied Microbiology, 1973, 25(3): 408–413

[14] Rodriguez R. Bioavailability and biomethylation of arsenic in contaminated soils and solid wastes. Dissertation for the Doctoral Degree. Stillwater: Oklahoma State University, 1998

[15] McBride B. Anaerobic and aerobic alkylation of arsenic. In: Brickman F E, Bellama J M, eds. Organometals and Organometaloids Occurrence and Fate in the Environment. Washington, DC: American Chemical Society, 1978

[16] Sanford R A, Klein D A. Environmental bioremediation for organometallic compounds: microbial growth and arsenic volatilization from soil and retorted shale. Applied Organometallic Chemistry, 1988, 2(2): 159–169

[17] Valls M, de Lorenzo V. Exploiting the genetic and biochemical capacities of bacteria for the remediation of heavy metal pollution. FEMS Microbiology Reviews, 2002, 26(4): 327–338

[18] Boonchan S, Britz M L, Stanley G A. Degradation and mineralization of high-molecular-weight polycyclic aromatic hydrocarbons by defined fungal-bacterial cocultures. Applied Environmental Microbiology, 2000, 66(3): 1007–1019

[19] Kotterman M J J, Vis E H, Field J A. Successive mineralization and detoxification of benzo[a]pyrene by the white rot fungus Bjerkandera sp. strain BOS55 and indigenous microflora. Applied Environmental Microbiology, 1998, 64(8): 2853–2858

[20] Brodkorb T S, Legge R L. Enhanced biodegradation of phenanthrene in oil tar-contaminated soils supplemented with Phanerochaete chrysosporium. Applied Environmental Microbiology, 1992, 58(9): 3117–3121

[21] Onions A H S, Allsopp D, Eggins H O W. Smith’s Introduction to Industrial Mycology. New York: John Willey & Sons, Inc., 1981

[22] Von-Arx J A. The genera of fungi sporulating in pure culture. Vaduz: J Cramer, 1974

[23] Larone D H. Medically Important Fungi a Guide to Identification. 2nd ed. Washington, DC: American Society for Microbiology, 1993, 210

[24] Deacon J W. Modern Micology. Oxford, USA: Blackwell Science, 1997

[25] Tamura K, Dudley J, Nei M, Kumar. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology Evolution, 2007, 24(8): 1596–1599

[26] Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology Evolution, 1987, 4(4): 406–425

[27] Su D, Li P J, Stagnitti F. Biodegradation of benzo[a]pyrene in soil by Mucor sp. SF06 and Bacillus subtilis SB02 co-immobilized on vermiculite. Journal of Environmental Sciences (China), 2006, 18(6): 1205–1209

[28] Seeley W H, Van Denmark P J. Microbes in action. A laboratory manual of microbiology. Pennsylvania: W H Freeman and Co., 1981

[29] Dean-Ross D, Moody J, Cerniglia C E. Utilization of mixtures of polycyclic aromatic hydrocarbons by bacteria isolated from contaminated sediment. FEMS Microbiology Ecology, 2002, 41(1): 1–7

[30] Mestrot A, Uroic M K, Plantevin T, Islam M R, Krupp E M, Feldmann J, Meharg A A. Quantitative and qualitative trapping of arsines deployed to assess loss of volatile arsenic from paddy soil. Environ mental Science and Technology, 2009, 43(21): 8270–8275

[31] Kästner B, Tenhaken R, Kauss H. Chitinase in cucumber hypocotyls is induced by germinating fungal spores and by fungal elicitor in synergism with inducers of acquired resistance. Journal of Plant, 1998, 13(4): 447–454

[32] Cerniglia C E. Biodegradation of polycyclic aromatic hydrocarbons. Current Opinion in Biotechnology, 1993, 4(3): 331–338

[33] Rodriguez R. Bioavailability and biomethylation of arsenic in contaminated soils and solid wastes. Dissertation for the Doctoral Degree. Stillwater: Oklahoma State University, 1998

[34] Salicis F, Krivobok S, Jack M, Benoit-Guyod J L. Biodegradation of fluoranthene by soil fungi. Chemosphere, 1999, 38(13): 3031– 3039

[35] Rafin C, Potin O, Veignie E, Lounes-Hadj Sahraoui A, Sancholle M. Degradation of benzo[a]pyrene as sole carbon source by a non white rot fungus Fusarium solani. Polycyclic Aromatic Compounds, 2000, 21(1–4): 311–329

[36] Ravelet C, Krivobok S, Sage L, Steiman R. Biodegradation of pyrene by sediment fungi. Chemosphere, 2000, 40(5): 557–563

[37] Romero M C, Salvioli M L, Cazau M C, Arambarri A M. Pyrene degradation by yeasts and Filamentous fungi. Environmental Pollution, 2002, 117(1): 159–163

[38] Veignie E, Rafin C, Woisel P, Lounes-Hadj Sahraoui A, Cazier F. Metabolization of the polycyclic aromatic hydrocarbon benzo[a]pyrene by a non white rot fungus (Fusarium solani) in a batch reactor. Polycyclic Aromatic Compounds, 2002, 22(1): 87–97

[39] Mukhopadhyay R, Rosen B P, Phung L T, Silver S. Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiology Reviews, 2002, 26(3): 311–325

[40] Heinaru E, Viggor S, Vedler E, Truu J, Merimaa M, Heinaru A. Reversible accumulation of p-hydroxybenzoate and catechol determines the sequential decomposition of phenolic compounds in mixed substrate cultivations in Pseudomonads. FEMS Microbiology Ecology, 2001, 37(1): 79–89

[41] Speitel G E Jr, Alley E R Jr. Bioremediation of unsaturated soils contaminated with chlorinated solvents. Journal of Hazardous Materials, 1991, 28(1–2): 81–90

[42] Brockman F J, Payne W, Workman D J, Soong A, Manley S, Hazen T C. Effect of gaseous nitrogen and phosphorus injection on in situ bioremediation of a trichloroethylene-contaminated site. Journal of Hazardous Materials, 1995, 41(2–3): 287–298

RIGHTS & PERMISSIONS

Higher Education Press and Springer-Verlag Berlin Heidelberg