Sub-surface oil-polluted soils are frequently subjected to temporal groundwater table fluctuations during which the biological and chemical properties of the soil are expected to change in response to hydrological variations. In this study, we investigated the influence of decreasing groundwater levels on soil enzymatic activities, microbial community and total hydrocarbon dynamics. The changes in enzymatic activities, hydrocarbon removal efficiencies and bacterial community structure in the petroleum polluted soil were monitored by routine collection and testing of soil samples every 20 days over a period of 80 days in a laboratory column setup. Polymerase chain reaction and high-throughput sequencing of soil microbial DNA were used to determine the compositions of microorganisms, alpha and beta diversity in the polluted soil while the soil enzymatic activities and total petroleum hydrocarbon were measured using spectrophotometry and gas chromatography–mass spectrometry, respectively. The results showed that experimental decreases in groundwater levels over 80 days led to increased soil alkalinity, modulated enzymatic activities and enhanced total petroleum hydrocarbon attenuation in sub-surface soil. The findings from this study will be very useful in designing and optimizing bioremediation strategies for petroleum polluted soils from cold temperate regions.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Price includes VAT (USA)
Tax calculation will be finalised during checkout.
Availability of data and materials
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Alef, K., & Nannipieri, P. (1995). Enzyme activities. In K. Alef & P. Nannipieri (Eds.), Methods in applied soil microbiology and biochemistry (pp. 23–30). Academic Press.
Baran, S., Bielińska, J. E., & Oleszczuk, P. (2004). Enzymatic activity in an airfield soil polluted with polycyclic aromatic hydrocarbons. Geoderma, 118, 221–232.
Barnett, S. E., Youngblut, N. D., & Buckley, D. H. (2019). Soil characteristics and land use drive bacterial community assembly patterns. FEMS Microbiology Ecology, 96(1), 1–11.
Buddhadasa, C., Barone, S., Bigger, S., & Orbell, J. (2001). Extraction of hydrocarbons from clay soils by sonication and Soxhlet techniques. Sekiyu Gakkaishi Journal of the Japan Petroleum Institute, 44(6), 378–383.
Caporaso, J., Kuczynsk, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5), 335–336.
Chu, H. Y., Sun, H. B., Tripathi, B. M., Adams, J. M., Huang, R., Zhang, Y. J., & Shi, Y. (2016). Bacterial community dissimilarity between the surface and subsurface soils equals horizontal differences over several kilometers in the western Tibetan Plateau. Environmental Microbiology, 18, 1523–1533.
Cisneros-de la Cueva, S., Martinez-Prado, M., Lopez-Miranda, J., Rojas-Contreras, J., & Medrano-Roldan, H. (2016). Aerobic degradation of diesel by a pure culture of Aspergillus terreus KP862582. Revista Mexicana De Ingenieria Quimica, 15(2), 347–360.
Dong, N., Yu, Z., Yang, C., Yang, M., & Wang, W. (2019). Hydrological impact of a reservoir network in the upper Gan River Basin, China. Hydrological Processes, 33, 1709–1723.
Dzionek, A., Dzik, J., Wojcieszyńska, D., & Guzik, U. (2018). Fluorescein diacetate hydrolysis using the whole biofilm as a sensitive tool to evaluate the physiological state of immobilized bacterial cells. Catalysts, 8, 434–440.
Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., & Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27(16), 2194–2200.
Eilers, K. G., Debenport, S., Anderson, S., & Fierer, N. (2012). Digging deeper to find unique microbial communities: the strong effect of depth on the structure of bacterial and archaeal communities in soil. Soil Biology and Biochemistry, 50, 58–65.
Ekundayo, E. O., Emede, T. O., & Osayande, D. J. (2001). Effects of crude oil spillage on growth and yield of maize (Zea mays L.) in soil of Midwestern Nigeria. Plant Food for Human Nutrition (formerly Qualitas Plantum), 56(4), 313–324.
Geoffry, K., & Achur, R. N. (2018). Screening and production of lipase from fungal organisms. Biocatalysis and Agricultural Biotechnology, 14, 241–253.
Gianfreda, L., Antonietta-Rao, M., Piotrowska, A., Palumbo, G., & Colombo, C. (2005). Soil enzyme activities as affected by anthropogenic alterations: intensive agricultural practices and organic pollution. Science of the Total Environment, 341(1–3), 265–279.
Ginige, M. P., Kaksonen, A. H., Morris, C., Shackelton, M., & Patterson, B. M. (2013). Bacterial community and groundwater quality changes in an anaerobic aquifer during groundwater recharge with aerobic recycled water. FEMS Microbiology Ecology, 85(3), 553–567.
Guwy, A. J., Martin, S. R., Hawkes, F. R., & Hawkes, D. L. (1999). Catalase activity measurements in suspended aerobic biomass and soil samples. Enzyme and Microbial Technology, 25, 669–676.
Jia, J., Liu, Y., & Li, G. (2009). Contamination characteristics and its relationship with physicochemical properties of oil polluted soils in oilfields of China. Chemical Industry and Engineering Society of China, 60(3), 726–732. (In Chinese).
Jia, J., Zong, S., Hu, L., Shi, S., Zhai, X., & Wang, B. (2017). The dynamic change of microbial communities in crude oil-contaminated soils from oilfields in China. Soil Sediment Contamination, 17, 1–30.
Kaushal, J., Mehandia, S., Singh, G., Raina, A., & Arya, S. K. (2018). Catalase enzyme: application in bioremediation and food industry. Biocatalysis and Agricultural Biotechnology, 16, 192–199.
Klamerus-Iwan, A., Błońska, E., Lasota, J., Kalandyk, A., & Waligórski, P. (2015). Influence of oil contamination on physical and biological properties of forest soil after chainsaw use. Water, Air, and Soil Pollution, 226(11), 389–400.
Kong, J., Xin, P., Hua, G. F., Luo, Z. Y., Shen, C. J., Chen, D., & Li, L. (2015). Effects of vadose zone on groundwater table fluctuations in unconfined aquifers. Journal of Hydrology, 528, 397–407.
Kuang, S., Su, Y., Wang, H., Yu, W., Lang, Q., & Matangi, G. (2018). Soil microbial community structure and diversity around the aging oil sludge in Yellow River Delta as determined by high-throughput sequencing. Archaea, 2018, 1–10.
Lai, X., Wen, J., Cen, S., Huang, X., Tian, H., & Shi, X. (2016). Spatial and temporal soil moisture variations over China from simulations and observations. Advances in Meteorology, 2016, 1–14.
Lekiah, P. P., Lelesi, K. J., & Simeon, A. T. K. (2020). Transport and degradation of hydrocarbons in a simulated crude oil contaminated vadose zone due to nutrient percolation. Singapore Journal of Scientific Research, 10, 425–437.
Lin, X., Li, X., Sun, T., Li, P., Zhou, Q., Sun, L., & Hu, X. (2009). Changes in microbial populations and enzyme activities during the bioremediation of oil-contaminated soil. Bulletin of Environmental Contamination and Toxicology, 83, 542–547. https://doi.org/10.1007/s00128-009-9838-x
Lipińska, A., Kucharski, J., & Wyszkowska, J. (2014). Activity of arylsulphatase in soil contaminated with polycyclic aromatic hydrocarbons. Water Air Soil Pollution, 225(9), 2097–2104.
Liu, Q., Tang, J., Gao, K., Gurav, R., & Giesy, J. P. (2017). Aerobic degradation of crude oil by microorganisms in soils from four geographic regions of China. Scientific Reports, 7, 1–12.
Margesin, R. (2005). Determination of enzyme activities in contaminated soil. In R. Margesin & F. Schinner (Eds.), Soil Biology: manual for soil analysis (Vol. 5, pp. 309–320). Springer.
Margesin, R., Feller, G., Hämmerle, M., Stegner, U., & Schinner, F. (2002). A colorimetric method for the determination of lipase activity in soil. Biotechnology Letters, 24, 27–33.
Michael, K., Wasswa, J., & Kasozi, G. (2016). Removal efficiency of total petroleum hydrocarbons from water by Pseudomonas aeruginosa: a case of Lake Albert, Uganda. Journal of Bioremediation and Biodegradation, 7, 337–341.
Okonkwo, C. J., Liu, N., Li, J., & Ahmed, A. (2021). Experimental thawing events enhance petroleum hydrocarbon attenuation and enzymatic activities in polluted temperate soils. International Journal Environment Science and Technology. https://doi.org/10.1007/s13762-021-03175-8
Osuji, C., & Adesiyan, S. O. (2005). The Isiokpo oil-pipeline leakage: total organic carbon/organic matter contents of affected soils. Chemistry & Biodiversity, 2(8), 1079–1085.
Peng, M., Zi, X., & Wang, Q. (2015). Bacterial community diversity of oil-contaminated soils assessed by high throughput sequencing of 16S rRNA genes. International Journal of Environmental Research and Public Health, 12(10), 12002–12015.
Popp, N., Schlomann, M., & Mau, M. (2006). Bacterial diversity in the active stage of a bioremediation system for mineral oil hydrocarbon-contaminated soils. Microbiology, 152, 3291–3304.
Prosser, J. A., Speir, T. W., Stott, D. E., & Dick, R. P. (2011). Soil oxidoreductases and FDA hydrolysis. Methods of Soil Enzymology, 6, 118.
Sannino, F., & Gianfred, L. (2001). Pesticide influence on soil enzymes activities. Chemosphere, 22, 1–9.
Schnurer, J., & Rosswall, T. (1982). Fluorescein diacetate hydrolysis as a measure of total microbial activity in soil and litter. Applied Environment Microbiology, 43, 1256–1261.
Shankar, V., Agans, R., & Paliy, O. (2017). Advantages of phylogenetic distance based constrained ordination analyses for the examination of microbial communities. Scientific Reports, 7, 1–10. https://doi.org/10.1038/s41598-017-06693-z
Sheng, Y., Wang, G., Hao, C., Xie, Q., & Zhang, Q. (2016). Microbial community structures in petroleum contaminated soils at an oil field, Hebei, China. Clean, 44(7), 829–839.
Siles, J. A., & Margesin, R. (2018). Insights into microbial communities mediating the bioremediation of hydrocarbon-contaminated soil from an Alpine former military site. Applied Microbiology and Biotechnology, 102, 4409–4421.
Silva, D., de Lima Cavalcanti, D., de Melo, E. J. V., dos Santos, P. N. F., da Luz, E. L. P., de Gusmão, N. B., & de Queiroz Sousa, F. V. (2015). Bio-removal of diesel oil through a microbial consortium isolated from a polluted environment. International Biodeterioration and Biodegradation, 97, 85–89.
Sun, W., Dong, Y., Gao, P., Fu, M., Ta, K., & Li, J. (2015). Microbial communities inhabiting oil contaminated soils from two major oilfields in Northern China: implications for active petroleum degrading capacity. Journal of Microbiology, 53(6), 371–378.
Wang, D. Y., Ma, W., Niu, Y. H., Chang, X. X., & Wen, Z. (2007a). Effects of cyclic freezing and thawing on mechanical properties of Qinghai-Tibet clay. Cold Region Science and Technology, 48, 34–43.
Wang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. (2007b). Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied Environment Microbiology, 73(16), 5261–5267.
Wang, X. Y., Feng, J., & Zhao, J. M. (2010). Effects of crude oil residuals on soil chemical properties in oil sites, Momoge Wetland, China. Environmental Monitoring and Assessment, 161(1), 271–280.
Wang Y, Feng J, Lin Q, Lyu X, Wang X, Wang G. (2013). Effects of crude oil contamination on soil physical and chemical properties in momoge wetland of China. Chinese Geographical Science, 23(6), 708–715. https://doi.org/10.1007/s11769-013-0641-6.
White, T., Bruns, T. D., Lee, S. B., & Taylor, J. W. (1990). Amplification and direct sequencing of fungal ribosomal RNA Genes for phylogenetics. Academic Press, pp 315–321.
Wu, M., Dick, W. A., Li, W., Wang, X., Yang, Q., Wang, T., & Chen, L. (2016). Bioaugmentation and biostimulation of hydrocarbon degradation and the microbial community in a petroleum-contaminated soil. International Biodeterioration and Biodegradation, 107, 58–164.
Xin, P., Kong, J., Li, L., & Barry, D. A. (2013). Modelling of groundwater–vegetation interactions in a tidal marsh. Advances in Water Resources, 57, 52–68.
Yang, M., Yang, Y. S., Du, X., Cao, Y., & Lei, Y. (2013). Fate and transport of petroleum hydrocarbons in vadose zone: compound-specific natural attenuation. Water Air Soil Pollution, 224(3), 1439–1453.
Zhang, Y., Wang, J., Jing, J., & Sun, J. (2014). Response of groundwater to climate change under extreme climate conditions in North China Plain. Journal of Earth Science, 25(3), 612–618.
Zhang, H., Wang, E., Zhou, D., Luo, Z., & Zhang, Z. (2016). Rising soil temperature in China and its potential ecological impact. Scientific Reports, 6(1), 1–8.
Zhang, L., Zhang, G., & Sun, G. (2017). Variation trend of dry-wet climatic factors and correlation with wetlands in Western Jilin Province, China. Carpathian Journal of Earth and Environmental Science, 12(1), 1–8.
Zheng, Z., Zhang, Y., Su, X., & Cui, X. (2016). Responses of hydrochemical parameters, community structures, and microbial activities to the natural biodegradation of petroleum hydrocarbons in a groundwater–soil environment. Environmental Earth Sciences, 75(21), 1400–1413.
Zhong, Q., Chen, H., Liu, L., He, Y., Zhu, D., Jiang, L., Zhan, W., & Hu, J. (2017). Water table drawdown shapes the depth-dependent variations in prokaryotic diversity and structure in Zoige peatlands. FEMS Microbiology Ecology, 93(49), 1–11.
Zhou. Y., Dong. D., & Liu, J. (2013). Upgrading a regional groundwater level monitoring network for Beijing Plain, China. Geoscience Frontiers, 4, 127–138.
Zhou, Y., Wei, A., Li, J., Yan, L., & Li, J. (2016). Groundwater quality evaluation and health risk assessment in the Yinchuan Region, Northwest China. Expo Health, 8, 443–456.
The first author is grateful to the Petroleum Technology Development Fund, Nigeria for the doctoral scholarship award. This work was supported by the National Water Pollution Control and Treatment Science and Technology Major Project (No. 2018ZX07109-003) of China.
This work was supported by the National Water Pollution Control and Treatment Science and Technology Major Project (No. 2018ZX07109-003) of China. The first author is grateful to the Petroleum Technology Development Fund for the doctoral scholarship award.
Conflict of interest
The authors have no conflicts of interest to declare that are relevant to the content of this article.
This article does not contain any studies with human participants performed by any of the authors.
Below is the link to the electronic supplementary material.
About this article
Cite this article
Okonkwo, C.J., Liu, N. & Li, J. Impacts of experimental decreasing groundwater levels on bacterial community composition and hydrocarbon attenuation in oil-polluted soil from Northern China. Int J Energ Water Res 5, 447–460 (2021). https://doi.org/10.1007/s42108-021-00143-3
- Water table draw-down
- Petroleum hydrocarbons
- Soil enzymes