Uptake and bioaccumulation of diverse hydrocarbon compounds by selected food plants artificially exposed to bioremediated crude oil-contaminated soils

Victoria Tovo Jason-Ogugbue, Prince Chinedu Mmom, Ibisime Etela, Joesph Amadi Orluchukwu


Article Details: Received: 2020-12-15 | Accepted: 2021-02-15 | Available online: 2021-09-30 https://doi.org/10.15414/afz.2021.24.03.185-201


Assessment of the uptake and bioaccumulation of diverse hydrocarbon compounds within internal tissues by selected food plants artificially exposed to bioremediated crude oil-contaminated soils was carried out. Three bioremediated crude-oil contaminated soils of different fallow ages (6-, 12-, and 18- months after certified remediation protocols) and an uncontaminated soil were collected and designated as 6m-AB, 12m-AB, 18m-AB and control respectively. Total petroleum hydrocarbons (TPH) and intermediate metabolites of degradation in soil samples were determined in the dry and wet seasons using Gas Chromatography – Mass Spectrophotometer. Telfairia occidentalis, Zea mays, Cucumis sativus, and Abelmoschus esculentus were used to assess safety of crops grown on test soils by monitoring the bioaccumulation of chemical residues in their tissues. Baseline TPH contents in various soil samples were 161.25 mg Kg-1 (6m-AB), 51.72 mg Kg-1 (12m-AB), 91.50 mg Kg-1 (18m-AB) and below detectable level in the control soil. A myriad of organic compounds emanating from degradation of petroleum compounds and including toxic and carcinogenic metabolic intermediates like trifluoromethyltrimethylsilane, phthalate esters and halogenated aliphatics were detected in bioremediated soil and also in tissues of the plants grown on the bioremediated soils. Higher bioconcentration factors for accumulated organic compounds were obtained during the wet season for all plants with Telfairia occidentalis having the highest bioconcentration factor in both wet and dry seasons. Results obtained provide evidence of contaminant transfer from these bioremediated soils to plant tissues and suggest the need for adequate evaluation of chemical residues in remediated soils before utilizing such sites for farming to ensure safe crop production.

Keywords: crude oil-contaminated soil, bioremediation, bioconcentration, plants, TPH



Abbasian, F. et al. (2015).  A Comprehensive review of aliphatic hydrocarbon biodegradation by bacteria. Appl. Biochem. Biotechnol., 176(3), 670–699.

Adesuyi, A.A. et al. (2015). Assessment of heavy metals pollution in soils and vegetation around selected industries in Lagos State, Nigeria. J. Geosci. Environ. Prot., 3, 11–19.

Alburquerque, J.A. et al. (2011). Improvement of soil quality after ‘‘alperujo’’ compost application to two contaminated soils characterized by differing heavy metal solubility. J. Environ. Manage., 92, 733–741.

Alimba, C.G. et al. (2016). Chemical characterization of simulated landfill soil leachates from Nigeria and India and their cytotoxicity and DNA damage inductions on three human cell lines. Chemosphere, 164, 469–479.

ATSDR. (1997). CERCLA. Priority List of Hazardous Substances that Will Be the Subjects of Toxicological Profiles and Support Document. U.S. Department of Health and Human Services.

Bartha, R. (1986). Biotechnology of crude oil pollutant biodegradation. Microb. Ecol., 12, 155–172.

Bento, F.M. et al. (2005). Comparative bioremediation of soils contaminated with diesel oil by natural attenuation, bio-stimulation and bioaugmentation. Bioresour. Technol., 96(9), 1049–105.

Chung, N., & Alexander, M. (2002). Effect of soil properties on bioavailability and extractability of phenanthrene and atrazine sequestered in soil. Chemosphere, 48, 109–115. CIA. (2012). World Factbook. In Nigeria. CIA (pp. 1–15). Retrieved 14 April, 2012 from https://www.cia. gov/library/publications/the‐world‐factbook/geos/ countrytemplate_ni.html

Collier, T.K. et al. (2012). Biomarkers currently used in environmental monitoring. In Ecological biomarkers: Indicators of ecotoxicological effects. CRC Press: Boca Raton pp. 385–410.

Declercq, I., Cappuyns, V., & Duclos, Y. (2012). Monitored natural attenuation (MNA) of contaminated soils: state of the art in Europe – a critical evaluation. Sci. Total. Environ., 426, 393–405.

Devanathan, G. et al. (2012). Brominated flame retardants and polychlorinated biphenyls in human breast milk from several locations in India: potential contaminant sources in a municipal dumping site. Environ. Int., 39, 87–95.

DPR. (2002). Environmental guidelines and standards for crude oil industry in Nigeria.

Eggen, T., Moeder, M., & Arukwe, A. (2010) Municipal landfill leachates: a significant source for new and emerging pollutants. Sci. Total. Environ., 408, 5147–5157.

Federal Register. (2012). Incentives for Nondiscriminatory Wellness Programs in Group Health Plans. Washington, D.C. Proposed Rule: 77 Fed. Reg, 70620–70642.

Heitkamp, M.A., Franklin, W., & Cerniglia, C.E. (1988). Microbial metabolism of polycyclic aromatic hydrocarbons: isolation and characterization of a pyrene-degrading bacterium. Appl. Environ. Microbiol., 54, 2549–2555.

IARC. (2000). Some Industrial Chemicals. In Monographs on the Evaluation of the Carcinogenic Risk of Some Industrial Chemicals to Humans, (vol. 77IARC). Lyon, France (pp. 15–22).

IUCN. (2013). Sustainable remediation and rehabilitation of biodiversity and habitats of oil spill sites in the Niger Delta: main report including recommendations for the future. Report to Shell Crude oil Development Company Ltd of Nigeria, by the Independent IUCN–Niger Delta Panel (IUCN–NDP). Gland, Switzerland.

Jason-Ogugbue, V.T. et al. (2019). Evaluation of plant growth performance in bioremediated petroleum contaminated soil in Rivers State, Nigeria. Scientia Africana, 18(3), 75–96.

Khan, S. et al. (2008). Accumulation of polycyclic aromatic hydrocarbons and heavy metals in lettuce grown in the soils contaminated with long-term wastewater irrigation. J. Hazard. Mat., 152, 506–515.

Kleinsasser, N.H. et al. (2000). Phthalates demonstrate genotoxicity on human mucosa of the upper aerodigestive tract. Environ. Mol. Mutagen., 35, 9–12.

Kostka, J.E. et al. (2011). Hydrocarbon-degrading bacteria and the bacterial community response in Gulf of Mexico beach sands impacted by the deep-water horizon oil spill. Appl. Environ. Microbiol., 77, 7962–7974.

Lee, S. et al. (2013). Genotoxic potentials and related mechanisms of bisphenol A and other bisphenol compounds: a comparison study employing chicken DT40 cells. Chemosphere, 93, 434–440.

Lindén, O., & Pålsson, J. (2013). Oil contamination in Ogoni, Niger Delta. Ambio, 42, 685–701.

Little, D. I. et al. (2018). Sediment hydrocarbons in former mangrove areas, Southern Ogoni, Eastern Niger Delta, Nigeria In C. Makowski, C. W. Finkl (eds.), Threats to Mangrove Forests, Coastal Research Library. Springer International Publishing (pp. 323−342).

Lotfinasabasl, S., Gunale, V.R., & Rajurkar, N.S. (2013). Crude oil hydrocarbons pollution in soil and its bioaccumulation in mangrove species, Avicennia marina from Alibaug Mangrove Ecosystem, Maharashtra, India. Int. J. Adv. Res. Technol., 2(2), 1−7.

McElroy, A.E., Farrington, J.W., & Teal, J.M. (1989). Bioavailability of polycyclic aromatic hydrocarbons in the aquatic environment. In U. Varanasi (Ed.),  Metabolism of polycyclic aromatic hydrocarbons in the aquatic environment. Boca Raton, CRC Press (pp. 1–39).

Melnyk, A. et al. (2014). Chemical pollution and toxicity of water samples from stream receiving leachate from controlled municipal solid waste (MSW) landfill. Environ. Res., 135, 253–261.

Miller, R., & Bartha, R. (1989). Evidence from tiposome encapsulation for transport-limited microbial metabolism of solid alkanes. Appl. Environ. Microbiol., 55, 268–274.

Mmom, P.C., & Deekor, T. (2010). Assessing the effectiveness of land farming in the remediation of hydrocarbon polluted soils in the Niger Delta, Nigeria. Res. J. Appl. Sci. Eng. Technol., 2(7), 654–660.

Mortelmans, K. et al. (1986). Salmonella mutagenicity test: II. Results from testing of 270 chemicals. Environ. Mutagen., 8(7), 1–119.

Onyeike, E.N., Ogbuja, I.S., & Nwinuka, N.M. (2002). Inorganic ion levels of soils and streams in some areas of Ogoni, Nigeria as affected by crude oil spillage. Environ. Monit. Assess., 73, 191–205.

Ortínez, B.O., Ize, L.I., & Gavilán, G.A. (2003). La restauración de lossuelos contaminados con hidrocarburosen México. Gacetaecológica, 69, 83–92.

Petts, G. E. et al. (2000). Longitudinal variations in exposed riverine sediments: a context for the ecology of the Fiume Tagliamento, Italy. Aquat. Conserv., 10(4), 249–266.

Phillips, T.M. et al. (2000). Monitoring bioremediation in creosote-contaminated soils using chemical analysis and toxicity tests. J. Ind. Microbiol. Biotechnol., 24, 132–139.

Reid, B.J., Jones, K.C., & Semple, K.T. (2000). Bioavailability of persistent organic pollutants in soils and sediments – a perspective on mechanisms, consequences and assessment. Environ. Pollut., 108, 103–112.

Rhykerd, R.L. et al. (1999). Impact of bulking agents, forced aeration, and tillage on remediation of oil-contaminated soil. Bioresour. Technol., 67, 279–285.

Rojo, F. (2009). Degradation of alkanes by bacteria. Environ. Microbiol., 11(10), 2477–2490.

Salanitro, J.P. et al. (1997). Crude oil hydrocarbon bioremediation and soil ecotoxicity assessment. Environ. Sci. Technol., 31, 1769–1776.

Shagal, M.H. et al. (2012). Bioaccumulation of trace metals concentration in some vegetables grown near refuse and effluent dumpsites along Rumude-Doubeli bye-pass in Yola North, Adamawa State. Global Adv. Res. J. Environ. Sci. Toxicol., 1, 18–22.

Shirani, M. et al. (2012), Biomarker responses in mudskipper (Periophthalmus waltoni) from the coastal areas of the Persian Gulf with oil pollution.  Environ. Toxicol. Pharmacol., 34(3), 705–713.

SNV. (2008). Tabell över generella riktvärden för förorenad mark. Naturvårdsverket/Environmental Protection Agency, Stockholm.

Someya, M. et al. (2010). Persistent organic pollutants in breast milkof mothers residing around an open dumping site in Kolkata, India: specific dioxin-like PCB levels and fish as a potential source. Environ. Int., 36, 27–35.

Thiergärtner, H., & Holtzmann, K. (2014). Modeling and preliminary assessment of crude oil-contaminated soil in Ogoni (Nigeria). Altlasten Spektrum, 2, 61–71.

Tinsley, A., & Farewell, T. (2015). Soil degradation: a growing concern. Dissecting Soil: Safeguarding an Invaluable Natural Resource. The Environmentalist. IEMA (pp. 14–17).

UNEP. (2011). Environmental Assessment of Ogoni. United Nations Environment Programme, Nairobi, Kenya retrieved 12 October, 2014 from http://www.unep.org/Nigeria

US EPA. (1988). Guidelines Establishing Test Procedures for the Analyses of Pollutants Under the Clean Water Act; Final Rule and Interim Final Rule and Proposed Rule. Federal Register, 40CFR, Part 136.

Vázquez-luna, D. (2012). Chapter 5. Environmental bases on the exploitation of crude oil in the World. In Mohamed Younes (Ed.), Crude Oil Exploration in the World. IntechOpen (pp. 89– 134). https://doi.org/10.5772/35706

Vidali, M. (2001). Bioremediation: an overview. Pure. Appl. Chem., (73), 1163–1172.

Yang, C. et al. (2012). Application of light crude oil biomarkers for forensic characterization and source identification of spilled light refined oils. Environ. Forensics, 13(4), 298–311.

Full Text:



  • There are currently no refbacks.

Copyright (c) 2021 Acta Fytotechnica et Zootechnica

© Slovak University of Agriculture in Nitra, Faculty of Agrobiology and Food Resources