Abstract
In this study, we focused on soil contaminated by polycyclic aromatic hydrocarbons (PAHs) at typical coking-polluted sites in Beijing, conducted research on enhanced PAH bioremediation and methods to evaluate remediation effects based on toxicity testing, and examined changes in pollutant concentrations during ozone preoxidation coupled with biodegradation in test soil samples. The toxicity of mixed PAHs in soil was directly evaluated using the Ames test, and the correlation between mixed PAH mutagenicity and benzo(a)pyrene (BaP) toxicity was investigated in an effort to establish a carcinogenic risk assessment model based on biological toxicity tests to evaluate remediation effects on PAH-contaminated soil. This study provides a theoretical and methodological foundation for evaluating the effect of bioremediation on PAH-contaminated soil at industrially contaminated sites. The results revealed that the removal rate of PAHs after 5 min of O3 preoxidation and 4 weeks of soil reaction with saponin surfactants and medium was 83.22%. The soil PAH extract obtained after remediation had a positive effect on the TA98 strain at a dose of 2000 μg·dish−1, and the carcinogenic risk based on the Ames toxicity test was 8.98 times greater than that calculated by conventional carcinogenic PAH toxicity parameters. The total carcinogenic risk of the remediated soil samples was approximately one order of magnitude less than that of the original soil samples.
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References
Alabi, O. A. (2023). Comparative chemical analysis, mutagenicity, and genotoxicity of Petroleum refinery wastewater and its contaminated river using prokaryotic and eukaryotic assays. Protoplasma, 260(1), 89–101. https://doi.org/10.1007/s00709-022-01763-0
Bell, S. M., Phillips, J., Sedykh, A., Tandon, A., Sprankle, C., Morefield, S. Q., et al. (2017). An integrated chemical environment to support 21st-century toxicology. Environmental Health Perspectives, 124(10), 1616–1621. https://doi.org/10.1289/EHP1759
Brookes, P. (1975). Chemical basis for relationship between mutagenesis and carcinogenesis. British Journal of Cancer, 32(2), 253–254. https://doi.org/10.1038/bjc.1975.199
Cai, Y., Zhang, D., Jiang, L., Zhong, M., Xia, T., Yao, J., et al. (2014). Combined ozone pretreatment and biodegradation for remediation of PAHs-contaminated soil. Research of Environmental Sciences, 27(12), 1493–1498.
Chakravarty, P., Chowdhury, D., & Deka, H. (2022). Ecological risk assessment of priority PAHs pollutants in crude oil contaminated soil and its impacts on soil biological properties. Journal of Hazardous Materials, 437, 129325. https://doi.org/10.1016/j.jhazmat.2022.129325
Chen, G., & White, P. A. (2004). The mutagenic hazards of aquatic sediments: A review. Mutation Research/reviews in Mutation Research, 567(2–3), 151–225. https://doi.org/10.1016/j.mrrev.2004.08.005
Clerge, A., Le Goff, J., Brotin, E., Abeillard, E., Vaudorne, I., Denoyelle, C., et al. (2023). In vitro genotoxicity potential investigation of 7 oxy-PAHs. Environmental and Molecular Mutagenesis, 64(3), 176–186. https://doi.org/10.1002/em.22531
Courty, B., Le Curieux, F., Belkessam, L., Laboudigue, A., & Marzin, D. (2008). Mutagenic potency in Salmonella typhimurium of organic extracts of soil samples originating from urban, suburban, agricultural, forest and natural areas. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 653, 1–5. https://doi.org/10.1016/j.mrgentox.2008.01.011
da Silva, F., Felipe, M., de Castro, D., Araujo, S., Sisenando, H., & de Medeiros, S. (2021). A look beyond the priority: A systematic review of the genotoxic, mutagenic, and carcinogenic endpoints of non-priority PAHs. Environmental Pollution. https://doi.org/10.1016/j.envpol.2021.116838
EPA. (1999). Guidance for Conducting Health Risk Assessment of Chemical Mixtures. Available: https://cfpub.epa.gov/ncea/risk/recordisplay.cfm?deid=29260. Retrieved April 5, 1999.
Escher, B. I., Bramaz, N., Mueller, J. F., Quayle, P., Rutishauser, S., & Vermeirssen, E. L. M. (2008). Toxic equivalent concentrations (TEQs) for baseline toxicity and specific modes of action as a tool to improve interpretation of ecotoxicity testing of environmental samples. Journal of Environmental Monitoring, 10(5), 612–621. https://doi.org/10.1039/b800949j
Gabelova, A., Polakova, V., Prochazka, G., Kretova, M., Poloncova, K., Regendova, E., et al. (2013). Sustained induction of cytochrome P4501A1 in human hepatoma cells by co-exposure to benzo[a]pyrene and 7H-dibenzo[c, g]carbazole underlies the synergistic effects on DNA adduct formation. Toxicology and Applied Pharmacology, 271(1), 1–12. https://doi.org/10.1016/j.taap.2013.04.016
Gan, S., Lau, E. V., & Ng, H. K. (2009). Remediation of soils contaminated with polycyclic aromatic hydrocarbons (PAHs). Journal of Hazardous Materials, 172(2–3), 532–549. https://doi.org/10.1016/j.jhazmat.2009.07.118
Goi, A., Kulik, N., & Trapido, M. (2006). Combined chemical and biological treatment of oil contaminated soil. Chemosphere, 63(10), 1754–1763. https://doi.org/10.1016/j.chemosphere.2005.09.023
Haapea, P., & Tuhkanen, T. (2006). Integrated treatment of PAH contaminated soil by soil washing, ozonation and biological treatment. Journal of Hazardous Materials, 136(2), 244–250. https://doi.org/10.1016/j.jhazmat.2005.12.033
HAC. (2018). The federal contaminated site risk assessment in Canada, Part I: Guidance on human health preliminary quantitative risk assessment (PQRA). Available: http://www.hc-sc.gc.ca/ewh-semt/pubs/contamsite/part-partie_i/index-eng.php. Retrieved July 19, 2018.
Hughes, N., & Phillips, D. (1991). Covalent binding of the dibenzpyrenes and benzo[a]pyrene to DNA-evidence for synergistic and inhibitory interactions when applied in combination to mouse skin. Mutation Research, 252(2), 190. https://doi.org/10.1016/0165-1161(91)90065-G
Jiang, L., Zhong, M., Zhang, D., & Xia, T. (2011). Health risk assessment based on the bioaccessibile concentration of PAHs in soil. Ecology and Environment Sciences, 20(6–7), 1168–1175.
Kanaly, R., & Harayama, S. (2000). Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by bacteria. Journal of Bacteriology, 182(8), 2059–2067. https://doi.org/10.1128/jb.182.8.2059-2067.2000
Kenyon, M. O., Cheung, J. R., Dobo, K. L., & Ku, W. W. (2007). An evaluation of the sensitivity of the Ames assay to discern low-level mutagenic impurities. Regulatory Toxicology and Pharmacology, 48(1), 75–86. https://doi.org/10.1016/j.yrtph.2007.01.006
Krzyszczak, A., & Czech, B. (2021). Occurrence and toxicity of polycyclic aromatic hydrocarbons derivatives in environmental matrices. Science of the Total Environment, 788(20), 147738. https://doi.org/10.1016/j.scitotenv.2021.147738
Kulik, N., Goi, A., Trapido, M., & Tuhkanen, T. (2006). Degradation of polycyclic aromatic hydrocarbons by combined chemical pre-oxidation and bioremediation in creosote contaminated soil. Journal of Environmental Management, 78, 382–391. https://doi.org/10.1016/j.jenvman.2005.05.005
Laha, T., Gope, M., Datta, S., Masto, R. E., & Balachandran, S. (2023). Oral bioaccessibility of potentially toxic elements (PTEs) and related health risk in urban playground soil from a medieval bell metal industrial town Khagra, India. Environmental Geochemistry and Health, 45(8), 5619–5637. https://doi.org/10.1007/s10653-020-00715-y
Mccann, J., & Ames, B. (1976). Detection of carcinogens as mutagens in Salmonella/microsome test: assay of 300 chemicals: Discussion. Proceedings of the National Academy of Sciences of the United States of America, 73(3), 950-954. https://doi.org/10.1073/pnas.73.3.950
MEE. (2016a). Soil and sediment-Extraction of organic compounds-Pressurized fluid extraction (PFE). Available: https://www.mee.gov.cn/ywgz/fgbz/bz/bzwb/jcffbz/201602/W020160217517923190981.pdf. Retrieved March 1, 2016.
MEE. (2016b). Soil and Sediment-Determination of polycyclic aromatic hydrocarbon by gas chromatography-mass spectrometry method. Available: https://www.mee.gov.cn/ywgz/fgbz/bz/bzwb/jcffbz/201606/W020160701543192146985.pdf. Retrieved August 1, 2016.
MEE. (2018). Soil environmental quality Risk control standard for soil contamination of development land. Available: https://www.mee.gov.cn/ywgz/fgbz/bz/bzwb/trhj/201807/W020190626596188930731.pdf. Retrieved August 1, 2018.
MEE. (2019). Technical guidelines for risk assessment of soil contamination of land for construction. Available: https://www.mee.gov.cn/ywgz/fgbz/bz/bzwb/trhj/201912/W020191224560850148092.pdf. Retrieved December 5, 2019.
Mohan, S. V., Kisa, T., Ohkuma, T., Kanaly, R. A., & Shimizu, Y. (2006). Bioremediation technologies for treatment of PAH-contaminated soil and strategies to enhance process efficiency. Reviews in Environmental Science and Bio/technology, 5(4), 347–374. https://doi.org/10.1007/s11157-006-0004-1
Nam, K., & Kukor, J. (2000). Combined ozonation and biodegradation for remediation of mixtures of polycyclic aromatic hydrocarbons in soil. Biodegradation, 11(1), 1–9. https://doi.org/10.1023/A:1026592324693
Pohren, R.D.S., Rocha, J.A.V., Leal, K.A., & Vargas, V.M.F. (2012). Soil mutagenicity as a strategy to evaluate environmental and health risks in a contaminated area. Environment International, 44, 40–52. https://doi.org/10.1016/j.envint.2012.01.008
Richardson, S. D., Lebron, B. L., Miller, C. T., & Aitken, M. D. (2011). Recovery of phenanthrene-degrading bacteria after simulated in situ persulfate oxidation in contaminated soil. Environmental Science & Technology, 45(2), 719–725. https://doi.org/10.1021/es102420r
Russo, L., Rizzo, L., & Belgiorno, V. (2010). PAHs contaminated soils remediation by ozone oxidation. Desalination and Water Treatment, 23(1–3), 161–172. https://doi.org/10.5004/dwt.2010.1990
Siddens, L. K., Larkin, A., Krueger, S. K., Bradfield, C. A., Waters, K. M., Tilton, S. C., et al. (2012). Polycyclic aromatic hydrocarbons as skin carcinogens: Comparison of benzo[a]pyrene, dibenzo[def, p]chrysene and three environmental mixtures in the FVB/N mouse. Toxicology and Applied Pharmacology, 264(3), 377–386. https://doi.org/10.1016/j.taap.2012.08.014
Sleight, T. W., Sexton, C. N., Mpourmpakis, G., Gilbertson, L. M., & Ng, C. A. (2021). A classification model to identify direct-acting mutagenic polycyclic aromatic hydrocarbon transformation products. Chemical Research in Toxicology, 34(11), 2273–2286. https://doi.org/10.1021/acs.chemrestox.1c00187
Smolarek, T., Baird, W., Fisher, E., & Digiovanni, J. (1987). Benzo(e)pyrene-induced alterations in the binding of benzo(a)pyrene and 7,12-dimethylbenz(a)anthracene to DNA in sencar mouse epidermis. Cancer Research, 47(14), 3701–3706.
Tarantini, A., Maitre, A., Lefebvre, E., Marques, M., Marie, C., Ravanat, J. L., & Douki, T. (2009). Relative contribution of DNA strand breaks and DNA adducts to the genotoxicity of benzo[a]pyrene as a pure compound and in complex mixtures. Mutation Research/fundamental and Molecular Mechanisms of Mutagenesis, 671(1–2), 67–75. https://doi.org/10.1016/j.mrfmmm.2009.08.014
White, P. A., & Claxton, L. D. (2004). Mutagens in contaminated soil: A review. Mutation Research/reviews in Mutation Research, 567(2–3), 227–345. https://doi.org/10.1016/j.mrrev.2004.09.003
Xu, S., Liu, W., & Tao, S. (2006). Emission of polycyclic aromatic hydrocarbons in China. Environmental Science & Technology, 40(3), 702–708. https://doi.org/10.1021/es0517062
Zeng, J., Li, Y., Dai, Y., Wu, Y., & Lin, X. (2021). Effects of polycyclic aromatic hydrocarbon structure on PAH mineralization and toxicity to soil microorganisms after oxidative bioremediation by laccase. Environmental Pollution, 287, 117581. https://doi.org/10.1016/j.envpol.2021.117581
Zhang, H., Liu, X., Wang, Y., Duan, L., Liu, X., Zhang, X., et al. (2023). Deep relationships between bacterial community and polycyclic aromatic hydrocarbons in soil profiles near typical coking plants. Environmental Science and Pollution Research, 30(23), 64486–64498. https://doi.org/10.1007/s11356-023-26903-8
Acknowledgements
We thank all the study participants in this study, and this study would not be possible without their valuable contributions.
Funding
This study was supported by the Beijing Natural Science Foundation (8232037), Beijing Natural Science Foundation (8164055), and National Key Research and Development Plans of Special Project for Site Soil (2018YFC1801006).
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DZ: Conceptualization, Methodology, Formal analysis, Project administration, Writing-Original Draft, Writing-Review & Editing, Funding acquisition. JM: Methodology, Formal analysis, Investigation, Data Curation, Visualization, Writing-Original Draft. MQ: Conceptualization, Methodology, Writing-Review & Editing. YD: Formal analysis, Writing-Review & Editing. YW: Writing-Review, Data Curation.
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Zhang, D., Song, J., Cai, M. et al. Preliminary study on the enhanced bioremediation of PAH-contaminated soil in Beijing and assessment of remediation effects based on toxicity tests. Environ Geochem Health 46, 103 (2024). https://doi.org/10.1007/s10653-024-01913-8
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DOI: https://doi.org/10.1007/s10653-024-01913-8