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Bioaugmentation and Biostimulation of Total Petroleum Hydrocarbon Degradation in a Petroleum-contaminated Soil with Fungi Isolated from Olive Oil Effluent

  • Abduelbaset M. A. Essabri
  • Nur Pasaoglulari AydinlikEmail author
  • Ndifreke Etuk Williams
Article
  • 117 Downloads

Abstract

In degradation of total petroleum hydrocarbon, 35 isolates belonging to 11 genera were sanitized and 3 isolates as well as their consortium were initiated to be able to raise in association with petroleum hydrocarbon as sole source of carbon under in vitro circumstances. The isolated strains were grounded on internal transcribed spacer (ITS) rDNA sequence analysis. The fungal strains with the utmost potentiality to reduce petroleum hydrocarbon without emerging antagonistic activities were Aspergillus niger, Penicillium ochrochloron, and Trichodema viride. For fungal growth on petroleum hydrocarbon, P. ochrocholon gained weight of 44%, A. niger 49%, and T. viride 39% within the first 30–40 days. As compared to the controls, these fungi accumulated significantly higher biomass, produced extracellular enzymes, and degraded total petroleum hydrocarbon and A. niger strongly degraded total petroleum hydrocarbon with a degradation of about 71.19%. These observations with GC-MS data confirm that these isolates displayed rapid total petroleum hydrocarbon biodegradation within a period of 60 days and the half-life showed that A. niger was the shortest with t1/2 = 21.280 day−1 corresponding to the highest percent degradation of 71.19% and first-order kinetic fitted into the present study. By multivariate analysis, five main factors were identified by factor analysis (FA). The first factor (F1) of the fungi species accounts for 20.0% which signifies that fungi species controls the degradation of petroleum variability and hierarchical cluster analysis (HCA) as a dendrogram with five observations and three variables shows two predominant clusters order cluster 1 > 2.

Keywords

Petroleum Contamination Biodegradation Soil BSM Fungi 

Notes

Acknowledgements

The authors sincerely acknowledge Environmental Research Centre, Cyprus International University’s (North Cyprus, Mersin 10, Turkey) facilities for the research.

References

  1. Abdulkadir, E., Abdulaziz, Y., AlKindi, S. A.-B., & Charles Bakheit, S. N. (2007). Biodegradation of crude oil and n-alkanes by fungi isolated from Oman. Marine Pollution Bulletin, 54, 1692–1696.Google Scholar
  2. Acevedoa, F., Pizzul, L., Castillo, M. P., Cuevas, R., & Diez, M. C. (2011). Degradation of polycyclic aromatic hydrocarbons by the Chilean white-rot fungus Anthracophyllum discolor. Journal of Hazardous Materials, 185, 212–219.Google Scholar
  3. Adnan, B., Jialong, Z., Shue, L., Jiashu, L., Hussein, B., Xiaoyu, Z., & Fuying, M. (2018). Biodegradation of n-hexadecane by Aspergillus sp. RFC-1 and its mechanism. Ecotoxicology and Environmental Safety, 164, 398–408.Google Scholar
  4. Agarry, S. E., & Oghenejoboh, K. M. (2015). Enhanced aerobic biodegradation of naphthalene in soil: kinetic modelling and half-life study. International Journal of Environmental Bioremediation & Biodegradation, 3(2), 48–53.Google Scholar
  5. Agarry, S. E., Aremu, M. O., & Aworanti, O. A. (2013). Kinetic modelling and half-life study on enhanced soil bioremediation of bonny light crude oil amended with crop and animal-derived organic wastes. Journal of Petroleum & Environmental Biotechnology, 4, 137.  https://doi.org/10.4172/2157-7463.1000137.Google Scholar
  6. Agarry, S. E., Oghenejoboh, K. M., & Solomon, B. O. (2015). Kinetic modelling and half-life study of adsorptive bioremediation of soil artificially contaminated with bonny light crude oil. Journal of Ecological Engineering, 16(3), 1–13.Google Scholar
  7. Al-Nasrawi, H. (2012). Biodegradation of crude oil by fungi isolated from Gulf of Mexico. Journal of Bioremediation & Biodegradation, 3, 147.  https://doi.org/10.4172/2155-6199.1000147.Google Scholar
  8. Amechi, S. N., & Chukwudi, O. O. (2017). Bioremediation of gasoline contaminated agricultural soil by bioaugmentation. Environmental Technology & Innovation., 7, 1–11.Google Scholar
  9. Anna, K., Ewa, B., Jarosław, L., Agnieszka, K., & Piotr, W. (2015). Influence of oil contamination on physical and biological properties of forest soil after chainsaw use. Water, Air, and Soil Pollution, 226, 389.  https://doi.org/10.1007/s11270-015-2649-2.Google Scholar
  10. Barathi, S., & Vasudevan, N. (2003). Bioremediation of crude oil contaminated soil by bioaugmentation of Pseudomonas fluorescens NS1. Journal of Environmental Science and Health, Part A: Toxic/Hazardous Substances and Environmental Engineering, 38(9), 1857–1866.Google Scholar
  11. Behnood, M., Nasernejad, B., & Nikazar, M. A. (2014). Biodegradation of crude oil from saline waste water using white rot fungus Phanerochaete chrysosporium. Journal of Industrial and Engineering Chemistry, 20, 1879–1885.Google Scholar
  12. Bovio, E., Gnavi, G., Prigione, V., Spina, F., Denaro, R., Yakimov, M., Calogero, R., Crisafi, F., & Varese, G. C. (2017). The culturable mycobiota of a Mediterranean marine site after an oil spill: isolation, identification and potential application in bioremediation. Science of the Total Environment, 576, 310–318.  https://doi.org/10.1016/j.scitotenv.2016.10.064.Google Scholar
  13. Caliz, J., Genoveva, M., Esther, M., Jordi, S., Robert, C., Garau, M. A., Xavier, T. M., & Xavier, V. (2012). The exposition of a calcareous Mediterranean soil to toxic concentrations of Cr, Cd and Pb produces changes in the microbiota mainly related to differential metal bioavailability. Chemosphere, 89, 494–504.Google Scholar
  14. Calvo, C., Manzanera, M., Silva-Castro, G., Uad, I., & González-López, J. (2009). Application of bioemulsifiers in soil oil bioremediation processes. Future prospects. Sci Total Environ., 407(12), 3634–3640.Google Scholar
  15. Chaillan, F., Fleche, A. L., & Bury, E. (2004). Identification and biodegradation potential of tropical aerobic hydrocarbon degrading microorganisms. Research in Microbiology, 155, 587–595.Google Scholar
  16. Chikere, C. B., Okpokwasili, G. C., & Chikere, B. O. (2011). Monitoring of microbial hydrocarbon remediation in the soil. Review article. 3 Biotech, 1, 117–138.Google Scholar
  17. Chima, C. W., Ndifreke, E. W., Edidiong, A. E., Emmanuel, U. E., & Akhayere, E. (2016). Modelling changes in soil chemical parameters of Obio-Akpor, Rivers state, Nigeria using geographic information system. Journal of Scientific and Engineering Research, 3(6), 207–221.Google Scholar
  18. Chouhan, S., Garg, R. K., Sairkar, P., atav, N., Silawat, N., Sharma, R., Singh, R. K., & Mehrotra, N. N. (2014). Characterization of genetic variance within and among five populations of Sperata seenghala (Skyes, 1839) revealed by random amplified polymorphic DNA markers. Journal of Genetic Engineering and Biotechnology, 12(1), 7–14.Google Scholar
  19. David, T. T., Otilio, A. S., Blanca, R. R. P., & Martha, G. C. (2017). Phylogeny and polycyclic aromatic hydrocarbons degradation potential of bacteria isolated from crude oil-contaminated site. Journal of Environmental Science and Health, Part A, 0(0), 1–8.Google Scholar
  20. de Amorim, R. C., Makarenkov, V., & Mirkin, B. (2016). A-Wardpb effective hierarchical clustering using the Minkowski metric and a fast k-means initialization. Information Sciences, 370–371, 343–354.Google Scholar
  21. Dobler, R., Matthias, S., & Reinhard, B. (2000). Population changes of soil microbial communities induced by hydrocarbon and heavy metal contamination. Bioremediation Journal, 4, 41–56.Google Scholar
  22. Eman, K., Esmaeil, S., Arturo, A., Mohamed, T., Nagalakshmi, H., Tanvi, H., Paul, D., & Andrew, S. (2016). Bioremediation potential of diesel-contaminated Libyan soil. Ecotoxicology and Environmental Safety, 133, 297–305.Google Scholar
  23. Eman, K., Esmaeil, S., Arturo, A.-M., Mohamed, T., Nagalakshmi, H., Tanvi, H. M., Morrison, P. D., & Ball, A. S. (2017). Bioremediation potential of diesel-contaminated Libyan soil. Ecotoxicology and Environmental Safety, 133, 297–305.Google Scholar
  24. Environmental Protection Agency, U. S. (1986). Test method for evaluating solid waste, SW-846, third ed (p. 1A). Washington: U.S. EPA.Google Scholar
  25. Fritsche, W., & Hofrichter, M. (2008). Aerobic degradation by microorganisms. In J. Klein (Ed.), Environmental processes soil decontamination (pp. 146–155). Weinheim: Wiley- VCH.Google Scholar
  26. Hadibarata, T., Tachibana, S., & Itoh, K. (2009). Biodegradation of chrysene, an aromatic hydrocarbon by Polyporus sp. S133 in liquid medium. Journal of Hazardous Materials, 164, 911–917.Google Scholar
  27. Hasan, I. (2014). Biodegradation of kerosene by Aspergillus niger and Rhizopus stolonifer. Applied and Environmental Microbiology, 2, 31–36.Google Scholar
  28. Hasan, S. W., Ghannam, M. T., & Esmail, N. (2010). Heavy crude oil viscosity reduction and rheology for pipe line transportation. Fuel, 89(5), 1095–1100.Google Scholar
  29. Hassan, G., Hamid, M., & Seyed, M. D. (2018). Evaluation of heavy petroleum degradation using bacterial-fungal mixed cultures. Ecotoxicology and Environmental Safety, 164, 434–439.Google Scholar
  30. Hung, S., Pius, M., Makoto, S., & Chae, G. (2008). Bioremediation of oil-contaminated soil using Candida catenulate and food waste. Environmental Pollution., 156, 891–896.Google Scholar
  31. Hwanhwi, L., Yeongseon, J., Young, M., Hanbyul, L., Gyu-Hyeok, K., & Jae-Jin, K. (2015). Enhanced removal of PAHs by Peniophora incarnata and ascertainment of its novel ligninolytic enzyme genes. Journal of Environmental Management, 164, 10–18.Google Scholar
  32. Kanaly, R. A., & Harayama, S. (2010). Advances in the field of high-molecular-weight polycyclic aromatic hydrocarbon biodegradation by bacteria. Microbial Biotechnology, 3, 136–164.Google Scholar
  33. Kauppi, S., Sinkkonen, A., & Romantschuk, M. (2011). Enhancing bioremediation of diesel-fuel-contaminated soil in a boreal climate: comparison of biostimulation and bioaugmentation. International Biodeterioration and Biodegradation, 65(2), 359–368.Google Scholar
  34. Kiran, G. S., Hema, T. A., Gandhimathi, R., Selvin, J., Thomas, T. A., Ravji, T. R., & Natarajaseenivasan, K. (2009). Optimization and production of a biosurfactant from the sponge-associated marine fungus Aspergillus ustus MSF3. Colloids and Surfaces B: Biointerfaces, 73(2), 250–256.Google Scholar
  35. Kriti, S., & Subhash, C. (2014). Treatment of petroleum hydrocarbon polluted environment through bioremediation: a review. Pakistan Journal of Biological Sciences, 17, 1–8.  https://doi.org/10.3923/pjbs.2014.1.8.Google Scholar
  36. Lee, H., Yeong, Y., Seo, J., Seokyoon, K., Gyu-Hyeok, K., & Jae, J. (2015). Bioremediation of polycyclic aromatic hydrocarbons in creosote-contaminated soil by Peniophora incarnata KUC8836. Bioremediation Journal, 19, 1–8.Google Scholar
  37. Li, Y., Liu, H., Tian, Z., Zhu, L., Wu, Y., & Tang, H. (2008). Diesel pollution biodegradation: synergetic effect of mycobacterium and filamentous fungi. Biomedical and Environmental Sciences, 21, 181–187.Google Scholar
  38. Maletic, S., Dalmacija, B., Roncevic, S., 2013. Petroleum hydrocarbon biodegradability in soil—implications for bioremediation. INTECH,  https://doi.org/10.5772/50108.
  39. Manli, W., Warren, A. D., Wei, L., Xiaochang, W., Qian, Y., Tingting, W., Limei, M., & Liming, C. (2016). Bioaugmentation and biostimulation of hydrocarbon degradation and the microbial community in a petroleum-contaminated soil. International Biodeterioration & Biodegradation., 107, 158–164.Google Scholar
  40. Marquez-Rocha, F. J., Olmos-Soto, J., & Rosano-Hernandez, M. C. (2005). Determination of the hydrocarbon-degrading metabolic capabilities of tropical bacterial isolates. International Biodeterioration and Biodegradation, 55, 17–23.Google Scholar
  41. McGenity, T. J., Folwell, B. D., McKew, B. A., & Sanni, G. O. (2012). Marine crude-oil biodegradation: a central role for interspecies interactions. Aquatic Biosystems, 8(10), 10–1186.Google Scholar
  42. Montagnolli, R. N., Lopes, P. R., & Bidoia, E. D. (2015). Screening the toxicity and biodegradability of petroleum hydrocarbons by a rapid colorimetric method. Archives of Environmental Contamination and Toxicology, 68, 342–353.Google Scholar
  43. Naga R. M., Ricardo, B., Venkateswarlu, K., Andrea, R. C., Manjunatha, B (2016). Removal of petroleum hydrocarbons from crude oil in solid and slurry phase by mixed soil microorganisms isolated from Ecuadorian oil fields. International Biodeterioration & Biodegradation 108, 85–90.  https://doi.org/10.1016/j.ibiod.2015.12.015.
  44. Naga, R. M., Laura, S., & Kadiyala, V. (2017). Microbial degradation of total petroleum hydrocarbons in crude oil: a field-scale study at the low-land rainforest of Ecuador. Environmental Technology, 38(20), 2543–2550.  https://doi.org/10.1080/09593330.2016.1270356.Google Scholar
  45. Nilanjana, D., & Preethy, C. (2011). Microbial degradation of petroleum hydrocarbon contaminants: an overview. Biotechnology Research International, 941810, 1–13.  https://doi.org/10.4061/2011/941810.Google Scholar
  46. Olga, M., Ewa, K., Dorota, W., & Tadeusz, A. (2015). Biodegradation of diesel oil hydrocarbons enhanced with Mucor circinelloides enzyme preparation. International Biodeterioration & Biodegradation, 104, 142–148.Google Scholar
  47. Onojake, M. C., Omokheyeke, O., & Osakwe, J. O. (2014). Petroleum hydrocarbon contamination of the environment: a case study. Bulletin of Earth Sciences of Thailand, 6(1), 67–79.Google Scholar
  48. Oriomah, C., Olufemi, A., Olawale, A., & Abimbola, O. (2014). Bacteria from spent engine-oil-contaminated soils possess dual tolerance to hydrocarbon and heavy metals, and degrade spent oil in the presence of copper, lead, zinc and combinations thereof. Annales de Microbiologie, 65, 207–215.Google Scholar
  49. Palanisamy, N., Ramya, J., Kumar, S., Vasanthi, N., Chandran, P., & Khan, S. (2014). Diesel biodegradation capacities of indigenous bacterial species isolated from diesel contaminated soil. Journal of Environmental Health Science and Engineering, 12, 142.Google Scholar
  50. Passarini, M. R., Sette, L. D., & Rodrigues, M. V. (2011). Improved extraction method to evaluate the degradation of selected PAHs by marine fungi grown in fermentative medium. Journal of the Brazilian Chemical Society, 22(3), 564–570.Google Scholar
  51. Rhodes, C. J. (2010). Seaweeds and their role in globally changing environments, cellular origin, life in extreme. Habitats and Astrobiology, 15, 229–248.Google Scholar
  52. Saowakon, S., Thanaphorn, R., Tewan, Y., Poonsuk, P., & Kanokphorn, S. (2017). The production of biodiesel using residual oil from palm oil mill effluent and crude lipase from oil palm fruit as an alternative substrate and catalyst. Fuel, 195, 82–87.Google Scholar
  53. Saravanan, R., & Sivakumar, T. (2013). Biodiversity and biodegradation potentials of fungi isolated from marine systems of East Coast of Tamil Nadu, India. International Journal of Current Microbiology and Applied Sciences, 2, 192–201.Google Scholar
  54. Sayara, T., Sarra, M., & Sanchez, A. (2010). Effects of compost stability and contaminant concentration on the bioremediation of PAHs-contaminated soil through composting. Journal of Hazardous Materials, 179, 999–1006.Google Scholar
  55. Sayara, T., Borras, E., Caminal, G., Sarra, M., & Sanchez, A. (2011). Bioremediation of PAHs-contaminated soil through composting: influence of bioaugmentation and biostimulation on contaminant biodegradation. International Biodeterioration and Biodegradation, 65, 859–865.Google Scholar
  56. Shaieb, F. M., Elghazawani, A. H., & Issa, A. (2015). Studies on crude oil degrading bacteria isolated from Libyan desert. International Journal of Current Microbiology and Applied Sciences, 4(2), 920–927.Google Scholar
  57. Sheppard, P. J., Adetutu, E. M., Makadia, T. H., & Ball, A. S. (2011). Microbial community and ecotoxicity analysis of bioremediated, weathered hydrocarbon contaminated soil. Soil Research, 49(3), 261–269.Google Scholar
  58. Tahhan, R. A., Ammari, T. G., Goussous, S. J., & Al-Shdaifat, H. I. (2011). Enhancing the biodegradation of total petroleum hydrocarbons in oily sludge by a modified bioaugmentation strategy. International Biodeterioration and Biodegradation, 65, 130–134.Google Scholar
  59. Toshio, M., Masashi, W., Hisato, T., Tasuku, K., & Ichiro, K. (2015). Degradation of chlorinated dioxins and polycyclic aromatic hydrocarbons (PAHs) and remediation of PAH-contaminated soil by the entomopathogenic fungus, Cordyceps militaris. Journal of Environmental Chemical Engineering, 3, 2317–2322.Google Scholar
  60. Varjani, S. J. (2017). Microbial degradation of petroleum hydrocarbons. Bioresource Technology, 223, 277–286.Google Scholar
  61. Weiwei, C., Junde, L., Xiangnan, S., Jun, M., & Xiaoke, H. (2017). High efficiency degradation of alkanes and crude oil by a salt-tolerant bacterium Dietzia species CN-3. International Biodeterioration & Biodegradation, 118, 110–118.Google Scholar
  62. Yao, L., Teng, Y., Luo, Y., Christie, P., Ma, W., Liu, F., Wu, Y., Luo, Y., & Li, Z. (2015). Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by Trichoderma reesei FS10-C and effect of bioaugmentation on an aged PAH-contaminated soil. Bioremediation Journal, 19, 9–17.Google Scholar
  63. Zhao, D., Liu, C., Liu, L., Zhang, Y., Liu, Q., & Wu, W. M. (2011). Selection of functional consortium for crude oil-contaminated soil remediation. International Biodeterioration and Biodegradation, 65(8), 1244–1248.Google Scholar
  64. Zuzanna, S., Paweł, C., Wojciech, J., Jakub, C., Justyna, S., & Agnieszka, P. (2015). Antibacterial effect of the Trichoderma viride fungi on soil microbiome during PAH’s biodegradation. International Biodeterioration & Biodegradation, 104, 170–177.Google Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Abduelbaset M. A. Essabri
    • 1
    • 2
  • Nur Pasaoglulari Aydinlik
    • 1
    • 2
    Email author
  • Ndifreke Etuk Williams
    • 1
    • 2
  1. 1.Department of Environmental Engineering, Faculty of EngineeringCyprus International UniversityNicosiaTurkey
  2. 2.Environmental Research CentreCyprus International UniversityNicosiaTurkey

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