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Polycyclic Aromatic Hydrocarbons (PAHs) Biodegradation by Basidiomycetes Fungi, Pseudomonas Isolate, and Their Cocultures: Comparative In Vivo and In Silico Approach

Abstract

The polycyclic aromatic hydrocarbons (PAHs) biodegradation potential of the five basidiomycetes’ fungal monocultures and their cocultures was compared with that of a Pseudomonas isolate recovered from oil-spilled soil. As utilization of hydrocarbons by the microorganisms is associated with biosurfactant production, the level of biosurfactant production and its composition by the selected microorganisms was also investigated. The Pseudomonas isolate showed higher ability to degrade three of the five PAHs but the isolate did not produce biosurfactant higher than C. versicolor and P. ostreatus. Among the PAHs, the most effective biodegradation of PAH—pyrene (42%)—was obtained with the fungus C. versicolor. Cocultures involving the fungi and Pseudomonas could not significantly degrade the selected PAHs compounds above that degraded by the most efficient monoculture. A slight increase in pyrene degradation was observed in cocultures of C. versicolor and F. palustris (93.7% pyrene). The crude biosurfactant was biochemically characterized as a multicomponent surfactant consisting of protein and polysaccharides. The PAH biodegradation potential of the basidiomycetes fungi positively correlated with their potential to express ligninolytic enzymes such as lignin peroxidase (Lip), manganese peroxidase (Mnp), and laccase. The present study utilized in silico method such as protein–ligand docking using the FRED in Open Eye software as a tool to assess the level of ligninolytic enzymes and PAHs interactions. The in silico analysis using FRED revealed that of the five PAHs, maximum interaction occurred between pyrene and all the three ligninolytic enzymes. The results of the in silico analysis corroborated with our experimental results showing that pyrene was degraded to the maximum extent by species such as C. versicolor and P. ostreatus.

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References

  1. 1.

    Fang, G. C., Wu, Y. S., & Chen, J. C. (2006). Environmental Pollution, 142, 388–396.

    Article  CAS  Google Scholar 

  2. 2.

    Perera, P. F., Tang, D., Rauh, V., Lester, K., Tsai, W. Y., Tu, Y. H., et al. (2005). Environmental Health Perspectives, 113(8), 1062–1067.

    CAS  Google Scholar 

  3. 3.

    Taneja, A., & Masih, A. (2006). Chemosphere, 65(5), 449–456.

    Google Scholar 

  4. 4.

    Sharma, H., Jain, V. K., & Khan, Z. H. (2006). Chemosphere, 66(2), 302–310.

    Article  CAS  Google Scholar 

  5. 5.

    Chang V, B., Wei, S. H., & Yuan, S. Y. (2000). Chemosphere, 41, 1463–1468.

    Article  Google Scholar 

  6. 6.

    Sims, R. C., & Overcast, M. R. (1983). Residue Reviews, 88, 1–68.

    CAS  Google Scholar 

  7. 7.

    Bezalel, L., Hadavar, Y., & Cerniglia, C. E. (1996). Applied and Environmental Microbiology, 62, 292–295.

    CAS  Google Scholar 

  8. 8.

    Wolter, M., Zadrazil, F., Martens, R., & Bahadir, H. (1997). Applied and Environmental Microbiology, 48, 398–404.

    CAS  Google Scholar 

  9. 9.

    Kotterman, M. J. J., Vis, E. H., & Field, J. A. (1998). Applied and Environmental Microbiology, 64, 2853–2858.

    CAS  Google Scholar 

  10. 10.

    Vares, T., Niemenmaa, O., & Hatakka, A. (1994). Applied and Environmental Microbiology, 60, 569–575.

    CAS  Google Scholar 

  11. 11.

    Bezalel, L., Hadavar, Y., Fu, P. P., Freeman, J. P., & Cerniglia, C. E. (1996). Applied and Environmental Microbiology, 62, 2554–2559.

    CAS  Google Scholar 

  12. 12.

    Pickard, M. A., Roman, R., Tinoco, R., & Duhalt, R. V. (1996). Applied and Environmental Microbiology, 65, 3805–3809.

    Google Scholar 

  13. 13.

    Novotny, C., Svobodova, K., Exbanova, P., Cajthaml, T., Kasinath, A., Lang, E., et al. (2004). Soil Biology & Biochemistry, 36, 1545–1551.

    Article  CAS  Google Scholar 

  14. 14.

    Guiot, S. R., Beron, P., Yerushalmi, L., & Sarthoros, C. (2005). Chemosphere, 61, 1042–1050.

    Article  CAS  Google Scholar 

  15. 15.

    Aronstein, B. N., Calvillo, Y. M., & Alexander, M. (1991). Environmental Science and Technology, 25, 1728–1731.

    Article  CAS  Google Scholar 

  16. 16.

    Rouse, J. D., Sabatini, D. A., Suflita, J. M., & Harwell, J. H. (1994). Environmental Science and Technology, 24, 325–370.

    CAS  Google Scholar 

  17. 17.

    Tiehm, A. (1994). Applied and Environmental Microbiology, 60, 258–263.

    CAS  Google Scholar 

  18. 18.

    Lang, S., Gilbon, A., Syldatk, C., & Wagner, F. (1984). In K. L. Mittal, & B. Lindman (Eds.) Surfactants in solutions p. 1985. New York: Plenum.

    Google Scholar 

  19. 19.

    Drews, J. (2000). Science, 287, 1960–1964.

    Article  CAS  Google Scholar 

  20. 20.

    Suresh, P. S, Kumar, A., Kumar, R., & Singh, V. P. (2007). An in silico approach to bioremediation: Laccase as a case study. Journal of Molecular Graphics & Modelling. DOI 10.1016/j.jmgm.2007.05.005.

  21. 21.

    Steffen, K. T., Hofritchter, M., & Hatakka, A. (2005). Applied Microbiology and Biotechnology, 54, 819–825.

    Article  Google Scholar 

  22. 22.

    Bodour, A. A., & Miller-Maier, R. M. (1998). Journal of Microbiological and Methods, 32, 273–280.

    Article  CAS  Google Scholar 

  23. 23.

    Boochan, S., Britz, M. L., & Stanley, G. A. (2000). Applied and Environmental Microbiology, 66(3), 1007–1019.

    Article  Google Scholar 

  24. 24.

    Holt, J. G., Krieg, N. R., Sneath, P. H. A., Staley, J. T., & Williams, S. T. (1994). Bergey’s manual of determinative bacteriology (9th ed.). Baltimore: Williams & Wilkins.

    Google Scholar 

  25. 25.

    Vijaya, Ch., & Singaracharya, M. A. (2005). Indian Journal of Microbiology, 45, 75–77.

    CAS  Google Scholar 

  26. 26.

    MarioCarlous, N. S., Martinez, M. J., Cabello, M. N., & Arambarri, A. M. (2002). Revista Iberica de Micologia, 19, 181–185.

    Google Scholar 

  27. 27.

    Leonowicz, A., Trojanowski, J., & Olicz, B. (1978). Acta Biochimica Polonica, 25, 369–377.

    CAS  Google Scholar 

  28. 28.

    Steffen, K. T., Hofritchter, M., & Hatakka, A. (2002). Applied Microbiology and Biotechnology, 60, 212–217.

    Article  CAS  Google Scholar 

  29. 29.

    Mulligan, C. N., Cooper, D. G., & Neufeld, R. J. (1984). Journal of Fermentation Technology, 62(4), 311–314.

    CAS  Google Scholar 

  30. 30.

    Marcia, N., Ferraz, C., & Pastore, M. G. (2004). Brazilian Journal of Microbiology, 35, 81–85.

    Google Scholar 

  31. 31.

    Morikawa, M., Hirata, Y., & Imanaka, T. (2000). Biochimica et Biophysica Acta, 1488, 211–218.

    CAS  Google Scholar 

  32. 32.

    Cooper, D. G., & Goldenberg, B. G. (1987). Applied Microbiology and Biotechnology, 53, 224–229.

    CAS  Google Scholar 

  33. 33.

    Gornall, A. G., Bardawill, C. S., & David, M. M. (1949). Journal of Biological Chemistry, 177, 751–756.

    CAS  Google Scholar 

  34. 34.

    Steffen, K. T., Hofritchter, M., & Hatakka, A. (2002). Enzyme and Microbial Technology, 30, 550–555.

    Article  CAS  Google Scholar 

  35. 35.

    Yuan, S. Y., Wei, S. H., & Chang, B. V. (2000). Chemosphere, 41, 1463–1468.

    Article  CAS  Google Scholar 

  36. 36.

    Deziel, E., Paquettle, G., Villemur, R., Lepine, F., & Besaillion, J. G. (1996). Applied and Environmental Microbiology, 62(6), 1908–1912.

    CAS  Google Scholar 

  37. 37.

    Kanaly, R. A., & Haryama, S. (2000). Journal of Bacteriology, 182, 2059–2067.

    Article  CAS  Google Scholar 

  38. 38.

    Doong, R., & Lei, W. G. (2003). Journal of Hazardous Materials, 96, 15–27.

    Article  CAS  Google Scholar 

  39. 39.

    Bumpus, J. A. (1989). Applied and Environmental Microbiology, 55(1), 154–158.

    CAS  Google Scholar 

  40. 40.

    Pozzdnyakova, N. N., Nowak, J. R., Turkovskaya, O., & Haber, J. (2006). Enzyme and Microbial Technology, 39(6), 1242–1249.

    Article  CAS  Google Scholar 

  41. 41.

    Kamada, F., Abe, S., Hiratsuka, N., Wariishi, H., & Tanaka, H. (2002). Microbiology, 148, 1939–1946.

    CAS  Google Scholar 

  42. 42.

    Pickard, M. A., Roman, R., Tinoco, R., & Duhalt, R. V. (1999). Applied and Environmental Microbiology, 65(9), 3805–3809.

    CAS  Google Scholar 

  43. 43.

    Steffen, K. T., Hofritchter, M., & Hatakka, A. (2003). Applied and Environmental Microbiology, 69(7), 3957–3964.

    Article  CAS  Google Scholar 

  44. 44.

    Launen, L., Pinto, L., Wiebe, C., Kiehlman, E., & Moore, M. (1995). Canadian Journal of Microbiology, 41, 477–488.

    CAS  Article  Google Scholar 

  45. 45.

    Brodkorb, T. S., & Legge, R. L. (1992). Applied and Environmental Microbiology, 58, 3117–3121.

    CAS  Google Scholar 

  46. 46.

    Carillo, P. G., Mardaraz, C., Pitta-Alvarez, S. J., & Giulietti, A. M. (1996). World Journal of Microbiology and Biotechnology, 12, 82–84.

    Article  Google Scholar 

  47. 47.

    Yonebayashi, H., Yoshida, S., Ono, K., & Enomoto, H. (2000). Sekiyu Gakkaishi, 43(1), 59–69.

    CAS  Google Scholar 

  48. 48.

    Makkar, R. E., & Cameotra, S. S. (1997). Journal of Industrial Microbiology and Biotechnology, 18, 37–42.

    Article  CAS  Google Scholar 

  49. 49.

    Parra, J. L., Guinea, J., Manresa, M. A., Robert, M., Merced, M. E., Comelles, F., et al. (1989). Journal of the American Oil Chemists’ Society, 66, 141–145.

    Article  CAS  Google Scholar 

  50. 50.

    Stringfellow, W. T., & Aitken, M. D. (1994). Canadian Journal of Microbiology, 40, 432–438.

    CAS  Article  Google Scholar 

  51. 51.

    Volkering, F., Breure, A. M., & Andel, J. G. Y. (1992). Applied Microbiology and Biotechnology, 40, 535–540.

    Google Scholar 

  52. 52.

    Clemente, A. R., Anazawa, T. A., & Durrant, L. R. (2001). Brazian Journal of Microbiology, 32, 255–261.

    CAS  Google Scholar 

  53. 53.

    Makkar, R. S., & Rockne, K. J. (2003). Environmental Toxicology and Chemistry, 22(10), 2280–2292.

    Article  CAS  Google Scholar 

  54. 54.

    Zhongming, Z., & Obbard, J. P. (2002). Journal of Environmental Quality, 31, 1842–1847.

    Article  Google Scholar 

  55. 55.

    Batista, S. R., Mounteer, A. H., Amorim, F. R., & Totola, M. R. (2006). Bioresource Technology, 97, 868–875.

    Article  CAS  Google Scholar 

  56. 56.

    Plaza, G. A., Zjawiony, I., & Banat, I. M. (2006). Journal of Petroleum Science and Engineering, 50, 71–77.

    Article  CAS  Google Scholar 

  57. 57.

    Carmichael, L. M., & Pfaender, F. K. (1997). Biodegradation, 8, 1–13.

    Article  CAS  Google Scholar 

  58. 58.

    Kanga, S. A., Bonner, J. S., Page, C. A., Mills, M. A., & Autenrieth, R. L. (1997). Environmental Science and Technology, 31, 556–561.

    Article  CAS  Google Scholar 

  59. 59.

    Willumsen, P. A., & Karlson, U. (1997). Biodegradation, 7, 415–423.

    Article  Google Scholar 

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Correspondence to A. Arun.

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Arun, A., Raja, P.P., Arthi, R. et al. Polycyclic Aromatic Hydrocarbons (PAHs) Biodegradation by Basidiomycetes Fungi, Pseudomonas Isolate, and Their Cocultures: Comparative In Vivo and In Silico Approach. Appl Biochem Biotechnol 151, 132–142 (2008). https://doi.org/10.1007/s12010-008-8160-0

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Keywords

  • PAHs
  • Biodegradation
  • Ligninolytic enzymes
  • Biosurfactant
  • In silico method
  • Docking