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Removing of Benzo[a]pyrene using the Isolated Fungi from Petroleum-polluted Soils

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Abstract

Objective

Benzo[a]pyrene, belonging to polycyclic aromatic hydrocarbons, is one of the most important industrial pollutants. This research was aimed to evaluate some fungal strains, with petroleum removing potency, for degradation of BaP from BaP-polluted media and also evaluation of Enzyme activity and protein content in the fungi growing in BaP-polluted media.

Methods

In a field study seven fungal specie were isolated from Tehran oil refinery and cultured in potato dextrose agar (PDA) media containing 30, 60 and 90 (mg/kg) BaP for adaptation of the fungal strains. Removing of BaP was measured after 45 days growth of the fungal colonies under different concentrations of BaP pollution in PDA media and soil. Peroxidase and catalase activity, and protein content were compared in the fungi growing in BaP-polluted media and control ones.

Results

The results showed that all the isolated fungi were able to growth in the BaP containing media and could remove BaP from the media. The highest removal efficiency was determined for Fusarium acuminatum (93%). Similar data obtained when the fungus used for bioremediation of BaP-polluted soil (91%). Total protein content and enzymatic activity (Peroxidase and Catalase) were increased with increasing of BaP pollution. The highest catalase activity was measured in F. acuminatum growing in the media containing 90 mg/kg BaP (2.2×10-2 unit/mg protein) and the highest (5× 10-3 unit/mg protein) peroxidase activity for Alternaria alternata. Protein content in the fungi was increased with increasing of BaP pollution. In F. acuminatum, the lowest amount of total protein was observed in the control sample (1×10-3 mg/g FW) and the highest amount was belonging to the group treated by 90 mg/kg BaP (7.5×10-3 mg/g FW).

Conclusion

It concluded that F. acuminatum showed the highest catalase activity, highest total protein content and also the highest BaP removal efficiency from both BaP-polluted media and soils.

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References

  1. Gary, J. H. & Handwerk, G. E. Petroleum refining technology and economics. (Marcel Dekker Inc., USA, 2001).

    Google Scholar 

  2. Mohsenzadeh, F. et al. Phytoremediation of petroleumpolluted soils: application of Polygonum aviculare and its root-associated (penetrated) fungal strains for biore mediation of petroleum-polluted soils. Ecotoxicol. Environ. Safe. 73, 613–619 (2010).

    Article  CAS  Google Scholar 

  3. Chehregani, A. & Kouhkan, F. Diesel exhaust particles and allergenicity of pollen grains of Lilium martagon. Ecotoxicol. Environ. Safe. 69, 567–573 (2008).

    Article  CAS  Google Scholar 

  4. Hagemann, R., Virelizier, H., Gaudin, D. & Pesneau, A. Polycyclic aromatic hydrocarbons in exhaust particles emitted from gasoline and diesel automobile. Toxicol. Environ. Chem. 5, 227–236 (1982).

    Article  CAS  Google Scholar 

  5. Environmental Protection Agency. National Air Pollutant Emission Trends Procedures Document, https://www.epa.gov/sites/production/files/2015-07/documents/trends_procedures_old.pdf (1998).

  6. Sverdrup, E. L., Hagen, B. S. Krogh, P. H. & Van Gestel, C. Benzo[a]pyrene shows low toxicity to three species of terrestrial plants, two soil invertebrates, and soil-nitrifying bacteria. Ecotoxicol. Environ. Safe. 66, 362–368 (2007).

    Article  CAS  Google Scholar 

  7. Fawell, J. K. & Hunt, S. The polycyclic aromatic hydrocarbons. In: Environmental toxicology: organic pollutants. (eds Fawell, J. K., Hunt, S.) 241–269 (Ellis Horwood, West Susex, 1988).

  8. IARC (International Agency for Research on Cancer). IARC Monographs on the evaluation of carcinogenic risks of humans. https://monographs.iarc.fr/ENG/Monographs/vol83/mono83.pdf (2004).

  9. Bhatt, T. S. & Coombs, M. M. The carcinogenicity of Cyclopenta[a]phenanhrene and chrysene derivatives in the sencar mouse. Polycyclic Arom. Comp. Online published (2006).

    Google Scholar 

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

    Article  CAS  Google Scholar 

  11. IARC (International Agency for Research on Cancer). Some non-heterocyclic polycyclic aromatic hydrocarbons and some related exposures. IARC Monographs on the evaluation of carcinogenic risks of humans, Vol 92: 1–835. https://monographs.iarc.fr/ENG/Monographs/vol92/mono92.pdf (2010).

  12. Baghali, Z. et al. Cytotoxic effect of Benzo[a]pyrene on development and protein pattern of sunflower pollen grains. Environ. Toxicol. Chem. 93, 665–677 (2011).

    Article  CAS  Google Scholar 

  13. ATSDR (Agency for toxic substances and disease registry). ATSDR Fact Sheet on Polycyclic Aromatic Hydrocarbons, on-line version, available on: http://www.atsdr.cdc.gov/tfacts69.pdf (2006).

  14. Turusov, V. S., Nikonova, T. V. & Parfenov, Yu. D. Increased multiplicity of lung adenomas in five generations of mice treated with benzo(a)pyrene when pregnant. Cancer Lett. 55, 227–231 (1990).

    Article  PubMed  CAS  Google Scholar 

  15. Alarcon, A., Delgadillo, J., Franco-Ramirez, A., Davies, F. & Ferrera-Cerrato, R. Influence of two polycyclic aromatic hydrocarbons on spore germination, and phytoremediation potential of Gigaspora margarita-Echynochloa polystachys symbiosis in Benzo[a]pyrene-polluted substrate. Revista Intern. de Contamin. Ambien. 22, 39–47 (2006).

    CAS  Google Scholar 

  16. Kang, H. G., Jeong, S. H., Cho, M. H. & Cho, J. H. Changes of biomarkers with oral exposure to benzo[a]pyrene, phenanthrene and pyrene in rats. J. Veter. Sci. 8, 361–368 (2010).

    Article  Google Scholar 

  17. Kummerov, M., Slovak, L. & Holoubek, I. Phytotoxicity studies of benzo[a]pyrene with Lactuca sativa. Toxicol. Environ. Chem. 51, 197–203 (1995).

    Article  Google Scholar 

  18. Aina, R., Plain, L. & Citterio, S. Molecular evidence for benzo[a]pyrene and naphthalene genotoxicity in Trifolium repens L. Chemosphere 65, 666–673 (2006).

    Article  PubMed  CAS  Google Scholar 

  19. Shah, U. K. et al. A comparison of the genotoxicity of benzo[a]pyrene in four cell lines with differing metabolic capacity. Mutation Research - Gen. Toxicol. Environ. Mutagenesis 808, 8–19 (2016).

    Article  CAS  Google Scholar 

  20. Mrozik, A., Piotrowska-Seget, Z. & Labuzek, S. Bacterial degredation and bioremediation of polycyclic aromatic hydrocarbons. Polish J. Environ. Studies 12, 15–25 (2013).

    Google Scholar 

  21. Sayara, T. A. S. Bioremediation of polycyclic aromatic hydrocarbons (PAHs)-contaminated soil: process evaluation through composting and anaerobic digestion approach. (University of Autonoma de Barcelona, Spain, 2010).

    Google Scholar 

  22. Cerniglia, C. E. Biodegradation of polycyclic aromatic hydrocarbons. Curr. Opin. Biotech. 4, 331–338 (1993).

    Article  CAS  Google Scholar 

  23. Dan, S., Pei-jun, L., Stagnitti, F. & Xian-zhe, X. Biodegradation of benzo[a]pyrene in soil by Mucor sp. SF06 and Bacillus sp. SB02 co-immobilized on vermiculite. J. Environ. Sci. 18, 1204–1209 (2006).

    Article  Google Scholar 

  24. Mohsenzadeh, F. & Shirkhani, Z. Removing of crude oil from polluted areas using the isolated fungi from Tehran oil refinery. Soil Sediment Contam. 25, 536–551 (2016).

    Article  CAS  Google Scholar 

  25. Nelson, P. E., Tousooun, T. A. & Marasas, W. F. O. Fusarium species: An illustrated manual for identification. (The Pennsylvania State University Press, USA, 1983).

    Google Scholar 

  26. Watanabe, T. Pictorial atlas of soil and seed fungi: Morphology and key to species. (CRC Press, New Delhi, 2002).

    Book  Google Scholar 

  27. Boonchan, S., Britz, M. L. & Stanley, G. A. Surfactantenhanced biodegradation of high molecular weight polycyclic aromatic hydrocarbons by Stenotrophomonas maltophilia. Biotech. Bioeng. 59, 482–494 (1998).

    Article  CAS  Google Scholar 

  28. Wyszkowski, M. & Wyszkowska, L. Effect of enzymatic activity of diesel oil contaminated soil on chemical composition of oat (Avena sativa L.) and maize (Zea mays L.). Plant, Soil Environ. 51, 360–367 (2005).

    Article  CAS  Google Scholar 

  29. Chance, B. & Maehly, A. Assay of catalases and peroxidases, Methods Biochem. Analysis 11, 746–775 (1995).

    Google Scholar 

  30. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254 (1976).

    Article  PubMed  CAS  Google Scholar 

  31. Chehregani, A., Eshghi Malayeri, B., Mohsenzadeh, F & Shirkhani, Z. Screening for plants and rhizospheral fungi with bioremediation potency of petroleum-polluted soils in a Tehran oil refinery area. Toxicol. Environ. Chem. 96, 84–93 (2014).

    Article  CAS  Google Scholar 

  32. Ogbe, M. E., Okhuoya, J. A. & Anaziah, O. C. Effect of different levels of spent lubricating oil on the growth of Pleurotus tuber-regium Fries Singer. Niger. J. Bot. 19, 266–270 (2006).

    Google Scholar 

  33. Mohsenzadeh, F. et al. Phytoremediation of petroleumcontaminated soils: Pre-screening for suitable plants and rhizospheral fungi. J. Toxicol. Environ. Chem. 91, 1443–1453 (2009).

    Article  CAS  Google Scholar 

  34. Hong, H. H., Chong, Y. S., Choi, S. D. & Park, V. Degradation of dibenzofuran by Pseudomonas putida. Water Res. 34, 2404–2407 (2000).

    Article  CAS  Google Scholar 

  35. Pandey, B. & Fulekar, M. H. Bioremediation technology: A new horizon for environmental clean-up. Biol. Med. 4, 51–59 (2012).

    Google Scholar 

  36. Capotorti, G., Digianvincenzo, P., Cesti, P., Bernardi, A. & Guglielmetti, G. Pyrene and benzo[a]pyrene metabolism by an Aspergillus terreus strain isolated from a polycyclic aromatic hydrocarbons polluted soil. Biodeg. 15, 79–85 (2004).

    Article  PubMed  CAS  Google Scholar 

  37. Joner, E. J. & Leyval, C. Influence of arbuscular mycorrhizal on clover and ryegrass grown together in a soil spiked with polycyclic aromatic hydrocarbons. Mycorrhiza 10, 155–159 (2001).

    Article  CAS  Google Scholar 

  38. Mohsenzadeh, F., Chehregani Rad, A. & Akbari, M. Evaluation of oil removal efficiency and enzymatic activity in some fungal strains for bioremediation of petroleum-polluted soils. Iran. J. Environ. Health Sci. Engin. 9, 1–8 (2012).

    Article  CAS  Google Scholar 

  39. Adekunle, A. A. & Adebambo, O. A. Petroleum hydrocarbon utilization by fungi isolated from Detarium senegalense (J. F. Gmelin) seeds. J. Amer. Sci. 3, 69–76 (2007).

    Google Scholar 

  40. Gong, Z. P. et al. Bioslurry remediation of soil contaminated with polycyclic aromatic hydrocarbons. Huan Jing KeXue (China Environ. Sci.) 22, 112–116 (2001).

    CAS  Google Scholar 

  41. Husaini, A., Roslan, H. A., Hii, K. S. Y. & Ang, C. H. Biodegradation of aliphatic hydrocarbon by indigenous fungi isolated from used motor oil contaminated sites. World J. Microb. Biotechnol. 24, 2789–2797 (2008).

    Article  CAS  Google Scholar 

  42. Iheanacho, C. C., Okerentugba, P. O., Orji, F. A. & Atalkiru, T. L. Hydrocarbon degradation potentials of indigenous fungal isolates from a petroleum hydrocarbon contaminated soil in Sakpenwa community, Niger Delta. Glob. Advan. Res. J. Environ. Sci. Toxicol. 3, 6–11 (2014).

    Google Scholar 

  43. Wunder, T., Kremer, S., Sterner, O. & Anke, H. Metabolism of the polycyclic aromatic hydrocarbon pyrene by Aspergilus niger SK9317. App. Microb. Biotech. 42, 636–641 (1994).

    Article  CAS  Google Scholar 

  44. Atagana, H. I., Haynes, R. J. & Wallis, F. W. Fungal bioremediation of creosote-contaminated soil: A laboratory scale bioremediation study using indigenous soil fungi. Water, Air Soil Poll. 172, 201–219 (2006).

    Article  CAS  Google Scholar 

  45. Bhattacharya, S., Das, A., Prashanthi, K., Palaniswamy, M. & Angayarkanni, J. Mycoremediation of benzo[a] pyrene by Pleurotus ostreatus in the presence of heavy metals and mediators. 3Biotec 4, 205–211 (2014).

    Google Scholar 

  46. Romero, M. C., Urrutia, M. I., Reinoso, H. E. & Kiernan, M. M. Benzo[a]pyrene degradation by soil filamentous fungi. J. Yeast Fung. Res. 1, 025–029 (2010).

    CAS  Google Scholar 

  47. Silva, I. S., Grossman, M. & Durranta, L. Degradation of polycyclic aromatic hydrocarbons (2e7 rings) under microaerobic and very-low-oxygen conditions by soil fungi. Inter. Biodeter. Biodeg. 63, 224–229 (2009).

    Article  CAS  Google Scholar 

  48. Alrumman, S. A., Standing, D. B. & Paton, G. I. Effects of hydrocarbon contamination on soil microbial community and enzyme activity. J. King Saud Univ. Sci. 27, 31–41 (2015).

    Article  Google Scholar 

  49. Balaji, V., Arulazhagan, P. & Ebenezer, P. Enzymatic bioremediation of polyaromatic hydrocarbons by fungal consortia enriched from petroleum contaminated soil and oil seeds. J. Environ. Biol. 35, 521–529 (2014).

    PubMed  CAS  Google Scholar 

  50. Messias, J. M. et al. Screening Botryosphaeria species for lipases: Production of lipase Botryosphaeriaribis EC-01 grown on soybean oil and other carbon sources. Enzym. Microb. Technol. 45, 426–431 (2009).

    Article  CAS  Google Scholar 

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Mohsenzadeh, F. Removing of Benzo[a]pyrene using the Isolated Fungi from Petroleum-polluted Soils. Toxicol. Environ. Health Sci. 10, 123–131 (2018). https://doi.org/10.1007/s13530-018-0355-3

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