Skip to main content

Advertisement

Log in

Comparing Oil Degradation Efficiency and Bacterial Communities in Contaminated Soils Subjected to Biostimulation Using Different Organic Wastes

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

The use of organic wastes in bioremediation of oil-contaminated desert soils has received little attention, although their use is cost-effective. We evaluated the use of spent mushroom compost (SMC), poultry manure (PM), and urea in the stimulation of respiration activities and oil degradation in a polluted desert soil. Moreover, we followed post treatment shifts in bacterial community structure using MiSeq sequencing. The addition of SMC and PM resulted in a significant increase in the evolved CO2 from 8.7 ± 1.9 to 25.7 ± 1.6 and to 23.4 ± 1.2 mg CO2 g−1 soil after 96 days of incubation, respectively. In contrast, changes in respiration activities after the addition of urea were insignificant. Gas chromatography–mass spectrometry (GC-MS) analysis revealed that most of the alkanes (C14-C30) were degraded in all biostimulated soils at a rate of 0.12–0.19 mg g−1 soil day−1, which was significantly higher than in the untreated soil (P < 0.05). Bacterial community analysis showed that 87–94 % of total sequences in the original soil belonged to Firmicutes, Actinobacteria, and Proteobacteria. While the relative abundance of Firmicutes remained unchanged after the addition of PM (37–48 % of total sequences), it increased in the urea treatment (44–87 %) and dramatically decreased in the SMC treatment (0.5–4.5 %). The remaining bacterial groups were still detectable after the treatments, although no clear treatment-related shifts could be observed, due to the large difference in the relative abundance of the same bacterial groups among the same replicates. We conclude that the use of organic wastes could be one of the ways of combating petroleum pollution in desert soils.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abed, R. M. M., Al-Kindi, S., & Al-Kharusi, S. (2015). Diversity of bacterial communities along a petroleum contamination gradient in desert soils. Microbial Ecology, 69, 95–105.

    Article  CAS  Google Scholar 

  • Abioye, P. O., Abdul Aziz, A., & Agamuthu, P. (2010). Enhanced biodegradation of used engine oil in soil amended with organic wastes. Water, Air, & Soil Pollution, 209, 173–179.

    Article  CAS  Google Scholar 

  • Adesodun, J. K., & Mbagwu, J. S. C. (2008). Biodegradation of waste-lubricating petroleum oil in a tropical alfisol as mediated by animal droppings. Bioresource Technology, 99, 5659–5665.

    Article  CAS  Google Scholar 

  • Agarry, S. E., Owabor, C. N., & Yusuf, R. O. (2010). Bioremediation of soil artificially contaminated with petroleum hydrocarbon oil mixtures: evaluation of the use of animal manure and chemical fertilizer. Bioremediation Journal, 14, 189–195.

    Article  CAS  Google Scholar 

  • AlonsoGutirrez, J., Costa, M. M., Figueras, A., Albaigs, J., Vias, M., Solanas, A. M., & Novoa, B. (2008). Alcanivorax strain detected among the cultured bacterial community from sediments affected by the “Prestige” oil spill. Marine Ecology Progress Series, 362, 25–36.

    Article  Google Scholar 

  • Aspray, T. J., Carvalho, D. J. C., & Philp, J. C. (2007). Application of soil slurry respirometry to optimise and subsequently monitor ex situ bioremediation of hydrocarbon-contaminated soils. International Biodeterioration & Biodegradation, 60, 279–284.

    Article  CAS  Google Scholar 

  • Atagana, H. I. (2004). Co-composting of PAH-contaminated soil with poultry manure. Letters in Applied Microbiology, 39, 163–168.

    Article  CAS  Google Scholar 

  • Ayotamuno, J. M., Okparanma, R. N., Davis, D. D., & Allagoa, M. (2010). PAH removal from Nigerian oil-based drill-cuttings with spent oyster mushroom (Pleurotus ostreatus) substrate. Journal of Food, Agriculture and Environment, 8, 914–919.

    Google Scholar 

  • Ball, A. S., & Jackson, A. M. (1995). The recovery of lignocellulose degrading enzymes from spent mushroom compost. Bioresource Technology, 54, 311–314.

    Article  CAS  Google Scholar 

  • Belnap, J., Phillips, S., Duniway, M., & Reynolds, R. (2003). Soil fertility in deserts: a review on the influence of biological soil crusts and the effect of soil surface disturbance on nutrient inputs and losses. Leiden: A a Balkema Publishers.

    Google Scholar 

  • Bento, F. M., Camargo, F. A. O., Okeke, B. C., & Frankenberger, W. T. (2005). Comparative bioremediation of soils contaminated with diesel oil by natural attenuation, biostimulation and bioaugmentation. Bioresource Technology, 96, 1049–1055.

    Article  CAS  Google Scholar 

  • Chaillan, F., Chaîneau, C. H., Point, V., Saliot, A., & Oudot, J. (2006). Factors inhibiting bioremediation of soil contaminated with weathered oils and drill cuttings. Environmental Pollution, 144, 255–265.

    Article  CAS  Google Scholar 

  • Chiu, S.-W., Gao, T., Chan, C. S.-S., & Ho, C. K.-M. (2009). Removal of spilled petroleum in industrial soils by spent compost of mushroom Pleurotus pulmonarius. Chemosphere, 75, 837–842.

    Article  CAS  Google Scholar 

  • Couto, M. N. P. F. S., Pinto, D., Basto, M. C. P., & Vasconcelos, T. S. D. (2012). Role of natural attenuation, phytoremediation and hybrid technologies in the remediation of a refinery soil with old/recent petroleum hydrocarbons contamination. Environmental Technology, 33, 2097–2104.

    Article  CAS  Google Scholar 

  • Dados, A., Omirou, M., Demetriou, K., Papastephanou, C., & Ioannides, I. M. (2015). Rapid remediation of soil heavily contaminated with hydrocarbons: a comparison of different approaches. Annals of Microbiology, 65, 241–251.

    Article  CAS  Google Scholar 

  • Das, N., & Chandran, P. (2010). Microbial degradation of petroleum hydrocarbon contaminants: an overview. Biotechnology Research International, 2011.

  • DeSantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., et al. (2006). Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology, 72, 5069–5072.

    Article  CAS  Google Scholar 

  • Doyle, R. C., Kaufman, D. D., & Burt, G. W. (1978). Effect of dairy manure and sewage sludge on 14C-pesticide degradation in soil. Journal of Agricultural and Food Chemistry, 26, 987–989.

    Article  CAS  Google Scholar 

  • Dumas, M. D., Polson, S. W., Ritter, D., Ravel, J., Gelb, J., Jr, Morgan, R., & Wommack, K. E. (2011). Impacts of poultry house environment on poultry litter bacterial community composition. PLoS ONE, 6

  • El-Fadel, M., Findikakis, A. N., & Leckie, J. O. (1997). Environmental impacts of solid waste landfilling. Journal of Environmental Management, 50, 1–25.

    Article  Google Scholar 

  • Eneje, R., Nwagbara, C., & Uwumarongie-Ilori, E. G. (2012). Amelioration of chemical properties of crude oil contaminated soil using compost from Calapoigoniummucunoides and poultry manure. International Research Journal of Agricultural Science and Soil Science, 2, 246–251.

    Google Scholar 

  • Ezenne, G. I., Nwoke, O. A., Ezikpe, D. E., Obalum, S. E., & Ugwuishiwu, B. O. (2014). Use of poultry droppings for remediation of crude-oil-polluted soils: effects of application rate on total and poly-aromatic hydrocarbon concentrations. International Biodeterioration & Biodegradation, 92, 57–65.

    Article  CAS  Google Scholar 

  • Fallgren, P. H., & Jin, S. (2008). Biodegradation of petroleum compounds in soil by a solid-phase circulating bioreactor with poultry manure amendments. Journal of Environmental Science and Health, 43, 125–131.

    Article  CAS  Google Scholar 

  • Gallardo, A., & Schlesinger, W. H. (1992). Carbon and nitrogen limitations of soil microbial biomass in desert ecosystems. Biogeochemistry, 18, 1–17.

    Article  CAS  Google Scholar 

  • García-Delgado, C., D’Annibale, A., Pesciaroli, L., Yunta, F., Crognale, S., Petruccioli, M., & Eymar, E. (2015). Implications of polluted soil biostimulation and bioaugmentation with spent mushroom substrate (Agaricus bisporus) on the microbial community and polycyclic aromatic hydrocarbons biodegradation. Science of the Total Environment, 508, 20–28.

    Article  CAS  Google Scholar 

  • Gargouri, B., Karray, F., Mhiri, N., Aloui, F., & Sayadi, S. (2014). Bioremediation of petroleum hydrocarbons-contaminated soil by bacterial consortium isolated from an industrial wastewater treatment plant. Journal of Chemical Technology & Biotechnology, 89, 978–987.

    Article  CAS  Google Scholar 

  • Hassanshahian, M., Zeynalipour, M. S., & Musa, F. H. (2014). Isolation and characterization of crude oil degrading bacteria from the Persian Gulf (Khorramshahr provenance). Marine Pollution Bulletin, 82, 39–44.

    Article  CAS  Google Scholar 

  • Hesnawi, R. M., & Mogadami, F. S. (2013). Bioremediation of Libyan crude oil-contaminated soil under mesophilic and thermophilic conditions. APCBEE Procedia, 5, 82–87.

    Article  CAS  Google Scholar 

  • Jadhav, V. V., Yadav, A., Shouche, Y. S., Aphale, S., Moghe, A., Pillai, S., et al. (2013). Studies on biosurfactant from Oceanobacillus sp. BRI 10 isolated from Antarctic sea water. Desalination, 318, 64–71.

    Article  CAS  Google Scholar 

  • Jin, S., & Fallgren, P. H. (2007). Site-specific limitations of using urea as a nitrogen source in biodegradation of petroleum wastes in soil. Soil and Sediment Contamination: An International Journal, 16, 497–505.

    Article  CAS  Google Scholar 

  • Klindworth, A., Pruesse, E., Schweer T, & Peplies J, Quast C, Horn M, Gloeckner FO. (2013). Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Research, 41

  • Kosaric, N. (2001). Biosurfactants and their application for soil bioremediation. Food Technology and Biotechnology, 39, 295–304.

    CAS  Google Scholar 

  • Lau, K. L., Tsang, Y. Y., & Chiu, S. W. (2003). Use of spent mushroom compost to bioremediate PAH-contaminated samples. Chemosphere, 52(9), 1539–1546.

    Article  CAS  Google Scholar 

  • Liu, J.-F., Sun, X.-B., Yang, G.-C., Mbadinga, S. M., Gu, J.-D., & Mu, B.-Z. (2015). Analysis of microbial communities in the oil reservoir subjected to CO2-flooding by using functional genes as molecular biomarkers for microbial CO2 sequestration. Frontiers in Microbiology, 6

  • Makut, M. D., & Ishaya, P. (2010). Bacterial species associated with soils contaminated with used petroleum products in Keffi town, Nigeria. African Journal of Microbiology Research, 4, 1698–1702.

    Google Scholar 

  • Mathew, M., Tan, L. R., Su, Q., Yang, X., Baxter, M., & Senior, E. (2006). Bioremediation of 6 % [w/w] diesel-contaminated mainland soil in Singapore: comparison of different biostimulation and bioaugmentation treatments. Engineering in Life Sciences, 6, 63–67.

    Article  CAS  Google Scholar 

  • Mnif, S., Chamkha, M., & Sayadi, S. (2009). Isolation and characterization of Halomonas sp. strain C2SS100, a hydrocarbon-degrading bacterium under hypersaline conditions. Journal of Applied Microbiology, 107, 785–794.

    Article  CAS  Google Scholar 

  • Ogboghodo, I. A., Erebor, E. B., Osemwota, I. O., & Isitekhale, H. H. (2004). The effects of application of poultry manure to crude oil polluted soils on maize (Zea mays) growth and soil properties. Environmental Monitoring and Assessment, 96, 153–161.

    Article  CAS  Google Scholar 

  • Oyetibo, G. O., Ilori, M. O., Obayori, O. S., & Amund, O. O. (2013). Biodegradation of petroleum hydrocarbons in the presence of nickel and cobalt. Journal of Basic Microbiology, 53, 917–927.

    Article  CAS  Google Scholar 

  • Prince, R. C., Gramain, A., & McGenity, T. J. (2010). Prokaryotic hydrocarbon degraders. In K. N. Timmis (Ed.), Handbook of hydrocarbon and lipid microbiology (pp. 1669–1692). Berlin, Heidelberg: Springer, Berlin Heidelberg.

    Chapter  Google Scholar 

  • Quinn, G., & Keough, M. (2002). Experimental design and data analysis for biologists

  • Ramirez, K. S., Craine, J. M., & Fierer, N. (2010). Nitrogen fertilization inhibits soil microbial respiration regardless of the form of nitrogen applied. Soil Biology and Biochemistry, 42, 2336–2338.

    Article  CAS  Google Scholar 

  • Ros, M., Rodríguez, I., García, C., & Hernández, T. (2010). Microbial communities involved in the bioremediation of an aged recalcitrant hydrocarbon polluted soil by using organic amendments. Bioresource Technology, 101, 6916–6923.

    Article  CAS  Google Scholar 

  • Sasek, V., Bhatt, M., Cajthaml, T., Malachová, K., & Lednická, D. (2003). Compost-mediated removal of polycyclic aromatic hydrocarbons from contaminated soil. Archives of Environmental Contamination and Toxicology, 44, 336–342.

    Article  CAS  Google Scholar 

  • Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., et al. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 7537–7541.

    Article  CAS  Google Scholar 

  • Seo, J.-S., Keum, Y.-S., & Li, Q. X. (2009). Bacterial degradation of aromatic compounds. International Journal of Environmental Research and Public Health, 6, 278–309.

    Article  CAS  Google Scholar 

  • Shahsavari, E., Adetutu, E. M., Anderson, P. A., & Ball, A. S. (2013). Plant residues—a low cost, effective bioremediation treatment for petrogenic hydrocarbon-contaminated soil. Science of the Total Environment, 443, 766–774.

    Article  CAS  Google Scholar 

  • Sharma, D., Saharan, B. S., Chauhan, N., Procha, S., & Lal, S. (2015). Isolation and functional characterization of novel biosurfactant produced by Enterococcus faecium. SpringerPlus, 4

  • Sutton, N. B., Maphosa, F., Morillo, J. A., Abu Al-Soud, W., Langenhoff, A. A. M., Grotenhuis, T., et al. (2013). Impact of long-term diesel contamination on soil microbial community structure. Applied and Environmental Microbiology, 79, 619–630.

    Article  CAS  Google Scholar 

  • Tang, J., Lu, X., Sun, Q., & Zhu, W. (2012). Aging effect of petroleum hydrocarbons in soil under different attenuation conditions. Agriculture, Ecosystems & Environment, 149, 109–117.

    Article  CAS  Google Scholar 

  • Tao, X.-Q., Lu, G.-N., Dang, Z., Yang, C., & Yi, X.-Y. (2007). A phenanthrene-degrading strain Sphingomonas sp. GY2B isolated from contaminated soils. Process Biochemistry, 42, 401–408.

    Article  CAS  Google Scholar 

  • Volossiouk, T., Robb, E., & Nazar, R. (1995). Direct DNA extraction for PCR-mediated assays of soil organisms., 61, 3972–3976.

  • Vrijheid, M. (2000). Health effects of residence near hazardous waste landfill sites: a review of epidemiologic literature. Environmental health perspectives, 108

  • Yang, S., Wen, X., Zhao, L., Shi, Y., & Jin, H. (2014). Crude oil treatment leads to shift of bacterial communities in soils from the deep active layer and upper permafrost along the China-Russia crude oil pipeline route. PLoS ONE, 9

  • Yergeau, E., Sanschagrin, S., Beaumier, D., & Greer, C. W. (2012). Metagenomic analysis of the bioremediation of diesel-contaminated Canadian high arctic soils. PloS One, 7

  • Zhang, J., Lin, X., Liu, W., Wang, Y., Zeng, J., & Chen, H. (2012). Effect of organic wastes on the plant-microbe remediation for removal of aged PAHs in soils. Journal of Environmental Sciences, 24, 1476–1482.

    Article  CAS  Google Scholar 

  • Zuberi, M. J. S., & Ali, S. F. (2015). Greenhouse effect reduction by recovering energy from waste landfills in Pakistan. Renewable and Sustainable Energy Reviews, 44, 117–131.

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank Mr. Jamal Al-Sabahi for his assistance in the chemical analysis. We are also grateful for Gulf Mushroom Products Company (S.A.O.G.) in Barka, Oman, for their help in the collection of SMC. This research was financially supported by The Research Council (TRC) of Oman (grant RC/SCI/BIOL/11/01).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Raeid M. M. Abed.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Al-Kindi, S., Abed, R.M.M. Comparing Oil Degradation Efficiency and Bacterial Communities in Contaminated Soils Subjected to Biostimulation Using Different Organic Wastes. Water Air Soil Pollut 227, 36 (2016). https://doi.org/10.1007/s11270-015-2722-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-015-2722-x

Keywords

Navigation