Skip to main content
SpringerLink
Log in

Tree seedlings suffer oxidative stress but stimulate soil enzyme activity in oil sludge-contaminated soil in a species-specific manner

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

The impact of plants on soil enzymatic activity and their potential for remediation of oil-contaminated soil has been widely studied but information about tree species is scarce. Here, we used seedlings of four tree species (Ailanthus altissima Mill, Fraxinus rotundifolia Mill, Melia azedarach L. and Robinia pseudoacacia L.) to investigate rhizosphere effects on key soil enzymes (dehydrogenase, urease, alkaline and acid phosphatase) and to evaluate oxidative stress in response to oil sludge-contaminated soil (0, 100, 200, 400 g kg−1). We observed a large species-specific stimulation of soil enzyme activity often far exceeding the figures in unplanted soil with peaks mostly occurring under low oil contamination (100 g kg−1). The strongest stimulatory effect on dehydrogenase and urease activity produced R. pseudoacacia at the low and intermediate and F. rotundifolia at the highest contamination level. No clear pattern emerged for acid phosphatase activity, which was equally stimulated by all species at the highest contamination level. Alkaline phosphatase stimulation was dominated by F. rotundifolia at the low and by R. pseudoacacia at the higher oil contamination levels. Foliar H2O2 rose significantly in a species-specific manner in response to oil contamination, triggering an upregulation of the antioxidant defence, which began to show signs of exhaustion at the highest pollution level and revealed that oxidative stress was highest in A. altissima. Our results imply that phytoremediation efforts can be optimized through carefully designed plant species assemblages aligning stimulatory effects on soil enzyme activity and oxidative stress tolerance with the severity of the oil pollution.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Acosta-Martinez V, Tabatabai M (2000) Enzyme activities in a limed agricultural soil. Biol Fertil Soils 31:85–91

    CAS  Google Scholar 

  • Aebi H (1974) Catalase. In: Methods of enzymatic analysis. Elsevier, pp 673–684

  • Ahmadvand H, Amiri H, Dehghani Elmi Z, Bagheri S (2014) Chemical composition and antioxidant properties of Ferula-assa-foetida leaves essential oil. Iran J Pharmacol Therap 12:52–50

    Google Scholar 

  • Banks M, Schwab P, Liu B, Kulakow P, Smith J, Kim R (2003) The effect of plants on the degradation and toxicity of petroleum contaminants in soil: a field assessment. In: Phytoremediation. Springer, pp 75–96

  • Beškoski VP, Gojgić-Cvijović G, Milić J, Ilić M, Miletić S, Šolević T, Vrvić MM (2011) Ex situ bioremediation of a soil contaminated by mazut (heavy residual fuel oil): a field experiment. Chemosphere 83:34–40

    PubMed  Google Scholar 

  • Blaylock M, Huang J (2000) Phytoextraction of metals in phytoremediation of toxic metals: using plants to clean up the environment, Raskin, BD Ensley. John Wiley and Sons Inc, New York

    Google Scholar 

  • Bouazizi H, Jouili H, El Ferjani E (2007) Effects of copper excess on growth, H, O, production and peroxidase activities in maize seedlings (Zea mays L.). Pak J Biol Sci 10:751–756

    CAS  PubMed  Google Scholar 

  • Bouyoucos GJJAj (1962) Hydrometer method improved for making particle size analyses of soils 1 54:464–465

  • Brakorenko NN, Korotchenko TV (2016) Impact of petroleum products on soil composition and physical-chemical properties. In: IOP conference series: earth and environmental science, 2016. IOP Publishing, p 012028

  • Burns RG (1982) Enzyme activity in soil: location and a possible role in microbial ecology. Soil Biol Biochem 14:423–427

    CAS  Google Scholar 

  • Burt R (2004) Soil survey laboratory methods manual

  • Casida L Jr, Klein D (1964) Santoro TJSs. Soil dehydrogenase activity 98:371–376

    CAS  Google Scholar 

  • Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53

    Google Scholar 

  • Das SK, Varma A (2010) Role of enzymes in maintaining soil health. In: Soil enzymology. Springer, pp 25–42

  • Dick R, Kandeler E (2005) Enzymes in soils/reference module in earth systems and environmental sciences. Encyclop Soils Environ

  • Dindar E, Şağban FOT, Başkaya HS (2015) Variations of soil enzyme activities in petroleum-hydrocarbon contaminated soil. Int Biodeterior Biodegradation 105:268–275

    CAS  Google Scholar 

  • Grossman R, Reinsch TJMosaPpm (2002) 2.1 Bulk density and linear extensibility:201–228

  • Habiba U et al (2015) EDTA enhanced plant growth, antioxidant defense system, and phytoextraction of copper by Brassica napus L. Environ Sci Pollut Res 22:1534–1544

    CAS  Google Scholar 

  • Helal HM, Dressler A (1989) Mobilization and turnover of soil phosphorus in the rhizosphere. Zeitschrift für Pflanzenernährung und Bodenkunde 152:175–180

    CAS  Google Scholar 

  • Hernández-Ortega HA, Alarcón A, Ferrera-Cerrato R, Zavaleta-Mancera HA, López-Delgado HA, Mendoza-López MR (2012) Arbuscular mycorrhizal fungi on growth, nutrient status, and total antioxidant activity of Melilotus albus during phytoremediation of a diesel-contaminated substrate. J Environ Manag 95:S319–S324

    Google Scholar 

  • Huang S, Jia X, Zhao Y, Chang Y (2016) Response of Robinia pseudoacacia L. rhizosphere microenvironment to Cd and Pb contamination and elevated temperature. Appl Soil Ecol 108:269–277

    Google Scholar 

  • IR of Iran Meteorological Org (IRIMO) (2014) The meteorology of the khoram abad Township https://www.irimo.ir/english/. Accessed April 2014

  • Jeelani N, Yang W, Qiao Y, Li J, An S, Leng X (2018) Individual and combined effects of cadmium and polycyclic aromatic hydrocarbons on the phytoremediation potential of Xanthium sibiricum in co-contaminated soil. Int J Phytoremed 20:773–779

    CAS  Google Scholar 

  • Khan S, Afzal M, Iqbal S, Khan QM (2013) Plant–bacteria partnerships for the remediation of hydrocarbon contaminated soils. Chemosphere 90:1317–1332

    CAS  PubMed  Google Scholar 

  • Kord B, Mataji A, Babaie SJ (2010) Pine (Pinus Eldarica Medw.) needles as indicator for heavy metals pollution 7:79–84

  • Kriksunov E (2011) Marine oil spills: the causes, environmental impact, prevention methods, response operations. Water Resour 38:684–685

    CAS  Google Scholar 

  • Lai J, Yu Z, Song X, Cao X, Han X (2011) Responses of the growth and biochemical composition of Prorocentrum donghaiense to different nitrogen and phosphorus concentrations. J Exp Mar Biol Ecol 405:6–17

    CAS  Google Scholar 

  • Lemanowicz J (2018) Dynamics of phosphorus content and the activity of phosphatase in forest soil in the sustained nitrogen compounds emissions zone. Environ Sci Pollut Res 25:33773–33782

    CAS  Google Scholar 

  • Li Y et al (2018) Biochar reduces soil heterotrophic respiration in a subtropical plantation through increasing soil organic carbon recalcitrancy and decreasing carbon-degrading microbial activity. Soil Biol Biochem 122:173–185

    CAS  Google Scholar 

  • Liu F, Ying G-G, Tao R, Zhao J-L, Yang J-F, Zhao L-F (2009) Effects of six selected antibiotics on plant growth and soil microbial and enzymatic activities. Environ Pollut 157:1636–1642

    CAS  PubMed  Google Scholar 

  • Marschner P (2012) Rhizosphere biology. In: Marschner's mineral nutrition of higher plants (Third Edition). Elsevier, pp 369–388

  • Martinez-Salgado M, Gutiérrez-Romero V, Jannsens M, Ortega-Blu R (2010) Biological soil quality indicators: a review. Curr Res Technol Educ Topics Appl Microbiol Microb Biotechnol 1:319–328

    Google Scholar 

  • Mithöfer A, Schulze B (2004) Biotic and heavy metal stress response in plants: evidence for common signals. FEBS Lett 566:1–5

    PubMed  Google Scholar 

  • Mohsenzadeh F (2018) Removing of benzo [a] pyrene using the isolated fungi from petroleum-polluted. Soils Toxicol Environ Health Sci 10:123–131

    Google Scholar 

  • Movafagh S, Crook S, Vo K (2015) Regulation of hypoxia-inducible factor-1a by reactive oxygen species: new developments in an old debate. J Cell Biochem 116:696–703

    CAS  PubMed  Google Scholar 

  • Nakano Y, Asada KJP (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Namli S, Akbas F, Isikalan C, Tilkat EA, Basaran D (2010) The effect of different plant hormones (PGRs) on multiple shoots of hypericum retusum aucher. Plant Omics 3:12

    CAS  Google Scholar 

  • Nanekar S, Dhote M, Kashyap S, Singh S, Juwarkar AA (2015) Microbe assisted phytoremediation of oil sludge and role of amendments: a mesocosm study. Int J Environ Sci Technol 12:193–202

    CAS  Google Scholar 

  • Nannipieri P, Grego S, Ceccanti B, Bollag J (1990) Ecological significance of the biological activity in soil. Soil Biochem 6:1

    Google Scholar 

  • Norouzi Haroni N, Badehian Z, Zarafshar M, Bazot S (2019) The effect of oil sludge contamination on morphological and physiological characteristics of some tree species. Ecotoxicology 28:507–519

    Google Scholar 

  • Oliveira F, Grossmann IE, Hamacher S (2014) Accelerating Benders stochastic decomposition for the optimization under uncertainty of the petroleum product supply chain. Comput Oper Res 49:47–58

    Google Scholar 

  • Osse M, Hamel J-F, Mercier A (2018) Markers of oil exposure in cold-water benthic environments: insights and challenges from a study with echinoderms. Ecotoxicol Environ Saf 156:56–66

    CAS  PubMed  Google Scholar 

  • Panchenko L, Muratova A (2017) Comparison of the phytoremediation potentials of Medicago falcata L. and Medicago sativa L. in aged oil-sludge-contaminated soil. Environ Sci Pollut Res 24:3117–3130

    CAS  Google Scholar 

  • Patidar K, Chouhan A, Thakur LS (2017) Removal of heavy metals from water and waste water by electrocoagulation process: a review. Int Res J Eng Technol 4:16–25

    Google Scholar 

  • Qiu L, Zhang X, Cheng J, Yin X (2010) Effects of black locust (Robinia pseudoacacia) on soil properties in the loessial gully region of the Loess Plateau China. Plant Soil 332:207–217

    CAS  Google Scholar 

  • Rosselli W, Keller C, Boschi K (2003) Phytoextraction capacity of trees growing on a metal contaminated soil. Plant Soil 256:265–272

    CAS  Google Scholar 

  • Roy AS et al (2014) Bioremediation potential of native hydrocarbon degrading bacterial strains in crude oil contaminated soil under microcosm study. Int Biodeterior Biodegradation 94:79–89

    CAS  Google Scholar 

  • Sajna KV, Sukumaran RK, Gottumukkala LD, Pandey A (2015) Crude oil biodegradation aided by biosurfactants from Pseudozyma sp. NII 08165 or its culture broth. Bioresour Technol 191:133–139

    CAS  PubMed  Google Scholar 

  • Sharma A, Kumar V, Kanwar M, Thukral A (2017a) Ameliorating imidacloprid induced oxidative stress by 24-epibrassinolide in Brassica juncea L. Environ Sci Pollut Res 64:509–517

    CAS  Google Scholar 

  • Sharma A, Kumar V, Thukral AK, Bhardwaj RJ (2016) Epibrassinolide-imidacloprid interaction enhances non-enzymatic antioxidants in Brassica juncea L. Environ Sci Pollut Res 21:70–75

    Google Scholar 

  • Sharma A, Kumar V, Yuan H, Kanwar MK, Bhardwaj R, Thukral AK (2018) Jasmonic acid seed treatment stimulates insecticide detoxification in Brassica juncea L. Front Plant Sci 9:1–17

    Google Scholar 

  • Sharma A, Thakur S, Kumar V, Kesavan AK, Thukral AK (2017b) 24-epibrassinolide stimulates imidacloprid detoxification by modulating the gene expression of Brassica juncea L. BMC Plant Biol 17:56

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 1:1

    Google Scholar 

  • Tabatabai M (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307

    CAS  Google Scholar 

  • Tabatabai M, Bremner JJSB (1972) Assay of urease activity in soils. Soil Biol Biochem 4:479–487

    CAS  Google Scholar 

  • Tauqeer HM et al (2016) Phytoremediation of heavy metals by Alternanthera bettzickiana: growth and physiological response. Ecotoxicol Environ Saf 126:138–146

    CAS  PubMed  Google Scholar 

  • Thomson B, Robson A, Abbott L (1986) Effects of phosphorus on the formation of mycorrhizas by Gigaspora calospora and Glomus fasciculatum in relation to root carbohydrates. New Phytol 103:751–765

    Google Scholar 

  • Tyśkiewicz K et al (2019) Characterization of bioactive compounds in the biomass of black locust, poplar and willow. Trees 1:1–29

    Google Scholar 

  • Uselman SM, Qualls RG, Thomas RB (1999) A test of a potential short cut in the nitrogen cycle: the role of exudation of symbiotically fixed nitrogen from the roots of a N-fixing tree and the effects of increased atmospheric CO2 and temperature. Plant Soil 210:21–32

    CAS  Google Scholar 

  • Varjani SJ, Upasani VN (2017) A new look on factors affecting microbial degradation of petroleum hydrocarbon pollutants. Int Biodeterior Biodegradation 120:71–83

    CAS  Google Scholar 

  • Velikova V, Yordanov I (2000) Edreva AJPs Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66

    CAS  Google Scholar 

  • Vig K, Megharaj M, Sethunathan N, Naidu R (2003) Bioavailability and toxicity of cadmium to microorganisms and their activities in soil: a review. Adv Environ Res 8:121–135

    CAS  Google Scholar 

  • Wang J, Zhang Z, Su Y, He W, He F, Song H (2008) Phytoremediation of petroleum polluted soil Petroleum Science 5:167–171

    CAS  Google Scholar 

  • Wyszkowska J, Wyszkowski M (2010) Activity of soil dehydrogenases, urease, and acid and alkaline phosphatases in soil polluted with petroleum. J Toxicol Environ Health Part A 73:1202–1210

    CAS  PubMed  Google Scholar 

  • Wyszkowska J, Wyszkowski MJJOT (2010) Activity of soil dehydrogenases, urease, and acid and alkaline phosphatases in soil polluted with petroleum. J Toxicol Environ Health 73:1202–1210

    CAS  Google Scholar 

  • Xie W et al (2018) Different responses to soil petroleum contamination in monocultured and mixed plant systems. Ecotoxicol Environ Saf 161:763–768

    CAS  PubMed  Google Scholar 

  • Xun W, Huang T, Zhao J, Ran W, Wang B, Shen Q, Zhang R (2015) Environmental conditions rather than microbial inoculum composition determine the bacterial composition, microbial biomass and enzymatic activity of reconstructed soil microbial communities. Soil Biol Biochem 90:10–18

    CAS  Google Scholar 

  • Yang Y, Han X, Liang Y, Ghosh A, Chen J, Tang MJPO (2015) The combined effects of arbuscular mycorrhizal fungi (AMF) and lead (Pb) stress on Pb accumulation, plant growth parameters, photosynthesis, and antioxidant enzymes in Robinia pseudoacacia L. PLoS ONE 10:e0145726

    PubMed  PubMed Central  Google Scholar 

  • Yang Y, Zhang N, Xue M, Lu S (2011) Effects of soil organic matter on the development of the microbial polycyclic aromatic hydrocarbons (PAHs) degradation potentials. Environ Pollut 159:591–595

    CAS  PubMed  Google Scholar 

  • Zarafshar M et al (2020) Do tree plantations or cultivated fields have the same ability to maintain soil quality as natural forests? Appl Soil Ecol 151:103536

    Google Scholar 

  • Zhang F-Q, Wang Y-S, Lou Z-P, Dong J-D (2007) Effect of heavy metal stress on antioxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Chemosphere 67:44–50

    CAS  PubMed  Google Scholar 

  • Zhang Z, Qu W (1990) Experiment guide of plant physiology. High Education Press, China

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Forestry, Faculty of Agriculture and Natural Resources, Lorestan University, Khorramabad, Islamic Republic of Iran

    Naser Norouzi Haroni

  2. Natural Resources Department, Fars Agricultural and Natural Resources Research and Education Center, AREEO, Shiraz, Islamic Republic of Iran

    Mehrdad Zarafshar

  3. Department of Forestry, Faculty of Agriculture and Natural Resources, Lorestan University, Khorramabad, Islamic Republic of Iran

    Ziaedin Badehian

  4. State Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Hangzhou, China

    Anket Sharma

  5. Institute for Applied Ecology, School of Science, Auckland University of Technology, 34 St. Paul Street, Auckland, 1010, New Zealand

    Martin Karl-Friedrich Bader

  6. Swiss Federal Institute of Forest, Snow and Landscape Research (WSL), Zürcherstrasse 111, 8903, Birmensdorf, Switzerland

    Martin Karl-Friedrich Bader

Authors
  1. Naser Norouzi Haroni
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mehrdad Zarafshar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ziaedin Badehian
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anket Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Martin Karl-Friedrich Bader
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

NNH, MZ, and ZB designed the experiments; NNH performed the experiments; MZ and MB analyzed the data and wrote the paper; ZB and AS revised the first draft of the manuscript and then MB grammatically improved the paper. All authors read and approved the final version of the manuscript.

Corresponding authors

Correspondence to Mehrdad Zarafshar or Ziaedin Badehian.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by DesRochers.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Haroni, N.N., Zarafshar, M., Badehian, Z. et al. Tree seedlings suffer oxidative stress but stimulate soil enzyme activity in oil sludge-contaminated soil in a species-specific manner. Trees 34, 1267–1279 (2020). https://doi.org/10.1007/s00468-020-01996-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-020-01996-7

Keywords

Search

Navigation