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Mutual effects of crude oil and plants in contaminated soil: a field study

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Abstract

The effect of oil contamination on growth of mono- and dicotyledonous plants (clover and ryegrass), on the one hand, and the effect of plants on oil biodegradation in soil, on the other hand, were studied in a long-term field experiment. It was found that plants respond differently to oil contamination of soddy-podzolic soil. Clover was more resistant to oil than ryegrass. Biosynthesis of photosynthetic pigments (chlorophylls and carotenoids) was not disturbed in clover, and the plant yield was fully restored by the end of the third growing season. The content of oxidative enzymes in clover leaves was 2–10 times higher than in ryegrass. Biological activity of soil planted with clover was 1.5–2 times higher correlating with the biochemical parameters of plants. Higher basal respiration in soil planted with clover corresponded to the enhanced oil biodegradation. The differences in the carbon of oil products between soils planted with clover and ryegrass appeared at the end of the third growing season at high doses of oil (5 and 10 L m−2).

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References

  • Ahmad, A. A., Muhammad, I., Shah, T., Kalwar, Q., Zhang, J., Liang, Z., et al. (2020). Remediation methods of crude oil contaminated soil. World Journal of Agriculture and Soil Science, 4(3), 8.https://irispublishers.com/wjass/fulltext/remediation-methods-ofcrude-oil-contaminated.ID.000595.php

    Google Scholar 

  • Alef, K., & Nannipieri, P. (1995). Soil respiration. In B. methods in soil microbiology and biochemistry (pp. 214–215). Academic Press Inc.

    Google Scholar 

  • Aniefiok, E., & Ibok, U. J. (2019). Role of plants and microbes in bioremediation of petroleum hydrocarbons contaminated soils. International Journal of Environmental Bioremediation & Biodegradation, 7(1), 1–19.

    Google Scholar 

  • Arellano, P., Tansey, K., Balzter, H., & Tellkamp, M. (2017). Plant family-specific impacts of petroleum pollution on biodiversity and leaf chlorophyll content in the Amazon rainforest of Ecuador. PLoS ONE, 12(1), e0169867. https://doi.org/10.1371/journal.pone.0169867

    Article  CAS  Google Scholar 

  • Arellano, P., Tanseya, K., Balzter, H., & Boyd, D. S. (2015). Detecting the effects of hydrocarbon pollution in the Amazon forest using hyperspectral satellite images. Environmental Pollution, 205, 225–239.

    Article  CAS  Google Scholar 

  • Arinushkina, E. V. (1970). Manual on chemical analysis of soils. Publishing House of Moscow State University. (in Russian).

    Google Scholar 

  • Aristovskaya, T. V. (1980). Microbiology of soil formation processes. Nauka. (in Russian).

    Google Scholar 

  • Bakina, L. G. (2012). The role of fractions of humic substances in soil-ecological processes (Doctoral dissertation). Retrieved from Russian State Library (Accession No. FB 9 12-1/3098) (in Russian).

  • Bakina, L. G., Chugunova, M. V., Polyak, Y. M., Mayachkina, N. V., & Gerasimov, A. O. (2020). Bioaugmentation: Possible scenarios due to application of bacterial preparations for remediation of oil contaminated soil. Environmental Geochemistry and Health. https://doi.org/10.1007/s10653-020-00755-4

    Article  Google Scholar 

  • Balba, M. T., Al-Awadhi, N., & Al-Daher, R. (1998). Bioremediation of oil-contaminated soil: Microbiological methods for feasibility assessment and field evaluation. Journal of Microbiological Methods, 32(2), 155–164.

    Article  CAS  Google Scholar 

  • Banks, M. K., Schwab, A. P., Liu, B., Kulakow, P., Smith, J. S., & Kim, R. (2003). The effect of plants on the degradation and toxicity of petroleum contaminants in soil: A field assessment. Advances in Biochemical Engineering/Biotechnology, 78, 75–96. https://doi.org/10.1007/3-540-45991-X_3

    Article  CAS  Google Scholar 

  • Bansal, N., & Kanwar, Sh. S. (2013). Peroxidase(s) in environment protection. The Scientific World Journal, 1, 9. https://doi.org/10.1155/2013/714639

    Article  CAS  Google Scholar 

  • Baruah, P., Saikia, R. R., Baruah, P. P., & Deka, S. (2014). Effect of crude oil contamination on the chlorophyll content and morpho-anatomy of Cyperus brevifolius (Rottb.). Environment Science and Pollution Research International, 21(21), 12530–12538. https://doi.org/10.1007/s11356-014-3195-y

    Article  CAS  Google Scholar 

  • Belovezhets, L. A., Makarova, L. E., Tretyakova, M. S., Markova, Yu. A., Dudareva, L. V., & Semenova, N. V. (2017). Possible pathways for destruction of polyaromatic hydrocarbons by some oil-degrading bacteria isolated from plant endosphere and rhizosphere. Applied Biochemistry and Microbiology, 53, 68–72.

    Article  CAS  Google Scholar 

  • Binet, Ph., Portal, J. M., & Leyval, C. (2000). Dissipation of 3–6-ring polycyclic aromatic hydrocarbons in the rhizosphere of ryegrass. Soil Biology and Biochemistry, 32(14), 2011–2017. https://doi.org/10.1016/S0038-0717(00)00100-0

    Article  CAS  Google Scholar 

  • Chaineau, C. H., Yepremian, C., Vidalie, J. F., Ducreux, J., & Ballerini, D. (2003). Bioremediation of a crude oil-polluted soil: Biodegradation, leaching and toxicity assessments. Water, Air & Soil Pollution, 144(1–4), 419–440.

    Article  CAS  Google Scholar 

  • Chibuike, G. U. (2013). Use of mycorrhiza in soil remediation: A review. Scientific Research and Essays, 8(35), 1679–1687. https://doi.org/10.5897/SRE2013.5605

    Article  CAS  Google Scholar 

  • Dospekhov, B. A. (1985). A field experiment technique (with the basics of statistical processing of research results). Agropromizdat.

    Google Scholar 

  • Dubrovskaya, E. V., Pozdnyakova, N. N., Muratova, AYu., Golubev, S. N., Bondarenkova, A. D., & Turkovskaya, O. V. (2019). Influence of oil pollution on plants in conditions of low humidity. Ecobiotech, 2(3), 391–401. https://doi.org/10.31163/2618-964X-2019-2-3-391-401

    Article  Google Scholar 

  • Dzhura, N., Romanyuk, O., Oshchapovsky, I., Tsvilynyuk, O., Terek, O., Turovsky, A., & Zaikov, G. (2008). Using plants for recultivation of oil-polluted soils. Journal of Environmental Protection and Ecology, 9(1), 55–59. in Russian.

    CAS  Google Scholar 

  • Ermakov, A. I. (1987). Biochemical research methods of plants. Agropromizdat. in Russian.

    Google Scholar 

  • Gamzaeva, R. S. (2019). Application of the Bak-Verad biodestructor on sod-podzolic soil contaminated with oil products. Bulletin of the St. Petersburg State Agrarian University, 2(55), 38–45. in Russian.

    Google Scholar 

  • Garcia Sánchez, M., Košnář, Z., Mercl, F., Aranda, E., & Tlustoš, P. (2017). A comparative study to evaluate natural attenuation, mycoaugmentation, phytoremediation, and microbial-assisted phytoremediation strategies for the bioremediation of an aged PAH-polluted soil. Ecotoxicology Environmental Safety, 147, 165–174. https://doi.org/10.1016/j.ecoenv.2017.08.012

    Article  CAS  Google Scholar 

  • Gaskin, S., Soole, K., & Bentham, R. (2008). Screening of Australian native grasses for rhizoremediation of aliphatic hydrocarbon-contaminated soil. International Journal of Phytoremediation, 10(5), 378–389. https://doi.org/10.1080/15226510802100465

    Article  CAS  Google Scholar 

  • Ghaffari, Z., Shademan, S., Sobhani-Damavandifar, Z., & Minai, D. (2015). Root and shoot peroxidase activity in Festuca arundinacea in light oil-contaminated soil. In  M. Öztürk, M. Ashraf, A. Aksoy, M. Ahmad (Eds.) Phytoremediation for Green Energy (pp. 185–191). Springer, Dordrecht. https://doi.org/10.1007/978-94-007-7887-0_13

  • Gkorezis, P., Daghio, M., Franzetti, A., van Hamme, J. D., Sillen, W., & Vangronsveld, J. (2016). The interaction between plants and bacteria in the remediation of petroleum hydrocarbons: An environmental perspective. Frontiers in Microbiology, 7, 1836. https://doi.org/10.3389/fmicb.2016.01836

    Article  Google Scholar 

  • Grigoriadi, A. S., Sotnikova, Yu. M., Novoselova, E. I., & Sattarova, L. R. (2019). Assessment of the influence of oil pollution and biological product on the biochemical parameters of a plant-phytoremediant. Scientific life, 14(11), 1705–1713.

    Article  Google Scholar 

  • Han, G., Cui, B. X., Zhang, X. X., & Li, K. R. (2016). The effects of petroleum-contaminated soil on photosynthesis of Amorpha fruticosa seedlings. International Journal of Environmental Science and Technology, 13(10), 2383–2392. https://doi.org/10.1007/s13762-016-1071-7

    Article  CAS  Google Scholar 

  • Hazaimeha, M., Almansooryb, F., Abd Mutalibc, S., & Kanaand, B. (2019). Effects of plant density on the bioremediation of soils contaminated with polyaromatic hydrocarbons. Emerging Contaminants, 5(1), 123–127. https://doi.org/10.1016/j.emcon.2019.03.001

    Article  Google Scholar 

  • Heba, M. I., Aly, A. A., & Omar, M. R. (2014) Use of phenols, peroxidase and polyphenoloxidase of seed to quantify resistance of cotton genotypes to damping-off incited by Fusarium oxysporum. Journal of Stress Physiology & Biochemistry, 10(1), 37–44. http://www.jspb.ru/issues/2014/N1/JSPB_2014_1_37-44.pdf

  • Hussain, I., Puschenreiter, M., Gerhard, S., Abbas, S. G., Sani, Sh., Khan, W., & Reichenauer, T. G. (2019). Differentiation between physical and chemical effects of oil presence in freshly spiked soil during rhizoremediation trial. Environmental Science and Pollution Research, 26(18), 18451–18464. https://doi.org/10.1007/s11356-019-04819-6

    Article  CAS  Google Scholar 

  • Ikeura, H., Kawasaki, Yu., Kaimi, E., Nishiwaki, Ju., Noborio, K., & Tamaki, M. (2016). Screening of plants for phytoremediation of oil-contaminated soil. International Journal of Phytoremediation, 18(5), 460–466. https://doi.org/10.1080/15226514.2015.1115957

    Article  CAS  Google Scholar 

  • Joner, E. J., & Leyval, C. (2003). Phytoremediation of organic pollutants using mycorrhizal plants: A new aspect of rhizosphere interactions. Agronomie, 23, 495–502. https://doi.org/10.1051/agro:2003021

    Article  CAS  Google Scholar 

  • Kirk, J. L., Klironomos, J. N., Lee, H., & Trevors, J. T. (2005). The effects of perennial ryegrass and alfalfa on microbial abundance and diversity in petroleum contaminated soil. Environmental Pollution, 133(3), 455–465. https://doi.org/10.1016/j.envpol.2004.06.002

    Article  CAS  Google Scholar 

  • Kirkpatrick, W. D., White, P. M., Wolf, D. C., Thoma, G. J., & Reynolds, C. M. (2008). Petroleum-degrading microbial numbers in rhizosphere and non-rhizosphere crude oil-contaminated soil. International Journal of Phytoremediation, 10(3), 208–219. https://doi.org/10.1080/15226510801997648

    Article  CAS  Google Scholar 

  • Korchagina, L. E. (2015). Functional features of upland bog plants in conditions of oil pollution on the territory of the Middle Ob’ region. Bulletin of Nizhnevartovsk State University, 1, 14–21. in Russian.

    Google Scholar 

  • Krivobochek, V. G., Statsenko, A. P., Gural, D. M., & Kuryshev, I. A. (2016). Variability of metabolic processes in wheat plants under stress. Agrarian Scientific Journal, 6, 20–23. in Russian.

    Google Scholar 

  • Mariano, A. P., Tomasella, R. C., Di Martino, C., Morais, E. B., Maciel Filho, R., Seleghim, M. H. R., Contiero, J., de Tornisielo, S. M. T., & Angelis, D. D. F. (2010). Aerobic biodegradation of butanol and diesel oil blends. African journal of biotechnology, 9(42), 7094–7101.

    CAS  Google Scholar 

  • Methods for determining the toxicity of water and water extracts from soils, sewage sludge, waste using mortality and fertility changes in Daphnia. FR.1.39.2007.03222. (2007). Moscow: Akvaros (in Russian).

  • Method of measurement of seed germination and root length of seedlings of higher plants to determine the toxicity of technogenic contaminated soils. FR.1.39.2006.02264. (2009). St. Petersburg (in Russian).

  • Mohsenzadeh, F., Naseri, S., Mesdaghinia, A., Nabizadeh, R., Rad, ACh., & Zafari, D. (2009). Identification of petroleum resistant plants and rhizospheral fungi for phytoremediation of petroleum contaminated soils. Journal of the Japan Petroleum Institute, 52(4), 198–204. https://doi.org/10.1627/jpi.52.198

    Article  CAS  Google Scholar 

  • Nadtochiy, P. P., & Myslyva, T. N. (2014). Reference values of the acid-basic buffer of sody-podzolic soils for background monitoring. Agrochemistry, 3, 83–89. (in Russian).

    Google Scholar 

  • Njoku, K., Akinola, M., & Oboh, B. (2016). Phytoremediation of crude oil contaminated soil using Glycine max (Merril); through phytoaccumulation or rhizosphere effect? Journal of Biological & Environmental Sciences, 10(30), 115–124.

    Google Scholar 

  • Nkereuwem, M. E., Fagbola, O., Okon, I. E., Adeleye, A. O., & Nzamouhe, M. (2020). Bioremediation potential of mycorrhiza fungi in crude oil contaminated soil planted with Costus lucanusianus. Amazonian Journal of Plant Research, 4(1), 441–455. https://doi.org/10.26545/ajpr.2020.b00053x

    Article  Google Scholar 

  • Odjegba, V. J., & Sadiq, A. O. (2002). Effects of spent engine oil on the growth parameters, chlorophyll and protein levels of Amaranthus hybridus L. The Environmentalist, 22, 23–28.

    Article  Google Scholar 

  • Osuagwu, A. N., Okigbo, A. U., Ekpo, I. A., Chukwurah, P. N., & Agbor, R. B. (2013). Effect of crude oil pollution on growth parameters, chlorophyll content and bulbils yield in air potato (Dioscorea bulbifera L.). International Journal of Applied Science and Technology, 3(4), 37–42.

    Google Scholar 

  • Polyak, Y. M., Bakina, L. G., Chugunova, M. V., Mayachkina, N., Gerasimov, A. O., & Bure, V. M. (2018). Effect of remediation strategies on biological activity of oil-contaminated soil: A field study. International Biodeterioration & Biodegradation., 126, 57–68. https://doi.org/10.1016/j.ibiod.2017.10.004

    Article  CAS  Google Scholar 

  • Polyak, Y., Bakina, L., Mayachkina, N., & Polyak, M. (2020). The possible role of toxigenic fungi in ecotoxicity of two contrasting oil-contaminated soils: A field study. Ecotoxicology and Environmental Safety, 202, 110959. https://doi.org/10.1016/j.ecoenv.2020.110959

    Article  CAS  Google Scholar 

  • Polyak, Y. M., & Sukcharevich, V. I. (2019). Allelopathic interactions between plants and microorganisms in soil ecosystems. Biology Bulletin Reviews, 9(6), 562–574. https://doi.org/10.1134/S2079086419060033

    Article  Google Scholar 

  • Rogozina, E. A., & Kalimullina, G. M. (2009). Balance side and dynamics of utilization of soil oil pollution by microorganisms. Oil and gas geology. Theory and practice. 4(2), 1–13. http://www.ngtp.ru/rub/7/19_2009.pdf (in Russian).

  • Sambuu, G., Garetova, L. A., Imranova, E. L., Kirienko, O. A., Fischer, N. K., Gantumur, Kh., & Kharitonova, G. V. (2019). Biogeochemical characteristics of soils in the Dzunbayan oil-producing area (Eastern Mongolia). Biogeosystem Technique, 6(1), 46–58. (in Russian).

    Google Scholar 

  • Sharapova, I. E., Maslova, S. P., Tabalenkova, G. N., & Lapteva, E. M. (2011). Bioremediation of oil-contaminated soil in the cultivation of rhizomatous cereal of the reed canary grass. Environmental Protection in the Oil and Gas Complex, 11, 42–47.

    Google Scholar 

  • Shubina, A. G., Sinyutina, S. E., & Popova, E. D. (2012). Polyphenoxidase activity in the needles of blue spruce (Picea pungens) and potatoes (Solanium tuberosum) as a phytoindication marker of the state of the environment. Bulletin of the Tambov University, 17(1), 347–348. (in Russian).

    Google Scholar 

  • Statsenko, A. P., & Blinokhvatov, A. A. (2019). Variability of metabolic processes in wheat plants under stress. Innovative Technique and Technology, 2(19), 30–33.

    Google Scholar 

  • Syal, S., & Ramamurthy, V. (2003). Influence of plants on degradation of diesel in soil. Asian Journal of Microbiology Biotechnology and Environmental Sciences, 5(3), 353–358.

    CAS  Google Scholar 

  • Vavrek, M. C., & Campbell, W. J. (2002). Identification of plant traits that enhance biodegradation of oil. http://ipec.utulsa.edu/Ipec/conf/2002/vavrek_campbell_20.pdf

  • Vysotskaya, L. B., Arkhipova, T. N., Kuzina, E. V., Rafikova, G. F., Akhtyamova, Z. A., Ivanov, R. S., Timergalina, L. N., & Kudoyarova, G. R. (2019). Comparison of responses of different plant species to oil pollution. Biomics, 11(1), 86–100. https://doi.org/10.31301/2221-6197.bmcs.2019-06

    Article  Google Scholar 

  • Wei, Y., Wang, Y., Duan, M., Han, J., & Li, G. (2019). Growth tolerance and remediation potential of six plants in oil-polluted soil. Journal of Soils and Sediments, 19(2), 3773–3785. https://doi.org/10.1007/s11368-019-02348-w

    Article  CAS  Google Scholar 

  • Yavari, S., Malakahmad, A., & Sapari, N. B. (2015). A review on phytoremediation of crude oil spills. Water Air and Soil Pollution, 226, 279. https://doi.org/10.1007/s11270-015-2550-z

    Article  CAS  Google Scholar 

  • Zilberman, M. V., Poroshina, E. A., & Zyryanova, E. V. (2005). Bioassay of soils contaminated with oil and oil products. Publishing house of the Perm State Technical University. (in Russian).

    Google Scholar 

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Funding

This work was financially supported by the Ministry of Science and Higher Education of the Russian Federation (research topic No AAAA-A19-119020190122-6).

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LB contributed to study conception and design, analysis and interpretation of results, draft manuscript preparation; YP helped in analysis and interpretation of results, draft manuscript preparation; AG contributed to analysis and interpretation of results; NM helped in data collection, analysis of results; MC contributed to data collection, analysis and interpretation of results; YK contributed to data collection, analysis of results; VV contributed to data collection, analysis of results.

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Correspondence to Y. M. Polyak.

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Bakina, L.G., Polyak, Y.M., Gerasimov, A.O. et al. Mutual effects of crude oil and plants in contaminated soil: a field study. Environ Geochem Health 44, 69–82 (2022). https://doi.org/10.1007/s10653-021-00973-4

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