Skip to main content
Log in

Combined effects of cadmium and oil sludge on sorghum: growth, physiology, and contaminant removal

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The physiological and biochemical responses of Sorghum bicolor (L.) Moench. to cadmium (Cd) (30 mg kg−1) and oil sludge (OS) (16 g kg−1) present in soil both separately and as a mixture were studied in pot experiments. The addition of oil sludge as a co-contaminant decreased Cd entry into the plant by almost 80% and simultaneously decreased the stimulation of superoxide dismutase (SOD) and peroxidase. The decrease in glutathione reductase (GR) activity and the increase in glutathione-S-transferase (GST) activity under the influence of oil sludge indicated that its components were detoxified by conjugation with glutathione. Cd additionally activated the antioxidant and detoxifying potential of the plant enzymatic response to stress. This helped to enhance the degradation rate of oil sludge in the rhizosphere, in which the participation of the root-released enzymes in the degradation could be possible. Cd increased the extent of soil clean-up from oil sludge, mainly owing to the elimination of paraffins, naphthenes, and mono- and bicyclic aromatic hydrocarbons. The mutual influence of the pollutants on the biochemical responses of sorghum and on soil clean-up was evaluated. The results are important for understanding the antistress and detoxification responses of the remediating plant to combined environmental pollution.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Al-Hawas GHS, Sukry WM, Azzoz MM, Al-Moaik RMS (2012) The effect of sublethal concentrations of crude oil on the metabolism of Jojoba (Simmodsia chinensis) seedlings. Int Res J Plant Sci 3:54–62

    Google Scholar 

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341

    CAS  Google Scholar 

  • Babu TS, Tripuranthakam S, Greenberg BM (2005) Biochemical responses of the aquatic higher plant Lemna gibba to a mixture of copper and 1,2-dihydroxyanthraquinone: synergistic toxicity via reactive oxygen species. Environ Toxicol Chem 24:3030–3036

    CAS  Google Scholar 

  • Baldrian P, Gabriel J (2002) Copper and cadmium increase laccase activity in Pleurotus ostreatus. FEMS Microbiol Lett 206:69–74

    CAS  Google Scholar 

  • Banks MK, Kulakow P, Schwab AP, Chen Z, Rathbone K (2003) Degradation of crude oil in the rhizosphere of Sorghum bicolor. Int J Phytoremediation 5:225–234

    CAS  Google Scholar 

  • Baruah P, Saikia RR, Baruah PP, Deka S (2014) Effect of crude oil contamination on the chlorophyll content and morpho-anatomy of Cyperus brevifolius (Rottb.) Hassk. Environ Sci Pollut Res 21:12530–12538

    CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  Google Scholar 

  • Cristaldi A, Conti GO, Jho EH, Zuccarello P, Grasso A, Copat C, Ferrante M (2017) Phytoremediation of contaminated soils by heavy metals and PAHs. A brief review. Environ Technol Innov 8:309–326

    Google Scholar 

  • Dazy M, Jung V, Férard JF, Masfaraud JF (2008) Ecological recovery of vegetation on a coke-factory soil: role of plant antioxidant enzymes and possible implications in site restoration. Chemosphere 74:57–63

    CAS  Google Scholar 

  • Dubrovskaya E, Pozdnyakova N, Golubev S, Muratova A, Grinev V, Bondarenkova A, Turkovskaya O (2017) Peroxidases from root exudates of Medicago sativa and Sorghum bicolor: catalytic properties and involvement in PAH degradation. Chemosphere 169:224–232

    CAS  Google Scholar 

  • Dubrovskaya EV, Polikarpova IO, Muratova AY, Pozdnyakova NN, Chernyshova MP, Turkovskaya OV (2014) Changes in physiological, biochemical, and growth parameters of sorghum in the presence of phenanthrene. Russ J Plant Physiol 61:529–536

    CAS  Google Scholar 

  • Elavarthi S, Martin B (2010) Spectrophotometric assays for antioxidant enzymes in plants. In: Sunkar R (ed) Plant stress tolerance, Methods in molecular biology, vol 639. Springer Science+Buisness Media, LCC, pp 273–280

  • Gali NK, Kotteazeth S (2012) Isolation, purification, and characterization of thermophilic laccase from the xerophytes Cereus pterogonus. Chem Nat Compd 48:451–456

    CAS  Google Scholar 

  • Gautam A, Dubey RS (2018) Metal toxicity in plants: induction of oxidative stress, antioxidative defence system, metabolic alterations and phytoremrdiation. In: Hemantaranjan A (ed) Molecular physiology of abiotic stresses in plant productivity. Scientific Publishers, Jodhpur, pp 256–291

    Google Scholar 

  • Garifzyanov AR, Zhukov NN, Ivanishchev VV (2011) Formation and physiological reactions of oxygen active forms in plants cells. Modern Problems of Science and Education 2:2 (In Russian)

    Google Scholar 

  • Christou A, Antoniou C, Christodoulou C, Hapeshi E, Stavrou I, Michael C, Fatta-Kassinos D, Fotopoulos V (2016) Stress-related phenomena and detoxification mechanisms induced by common pharmaceuticals in alfalfa (Medicago sativa L.) plants. Sci Total Environ 557-558:652–664

    CAS  Google Scholar 

  • Gramss G, Rudeschko O (1998) Activities of oxidoreductase enzymes in tissue extracts and sterile root exudates of three crop plants and some properties of the peroxidase component. New Phytol 138:401–409

    CAS  Google Scholar 

  • Gronwald JW, Plaisance KL (1998) Isolation and characterization of glutathione S-transferase isozymes from Sorghum. Plant Physiol 117:877–892

    CAS  Google Scholar 

  • Hammami H, Alaie E, Mohammad S, Dastgheib M (2018) The ability of Silybum marianum to phytoremediate cadmium and/or diesel oil from the soil. Int J Phytoremediation 20:756–763

    CAS  Google Scholar 

  • Huang X-D, Babu ST, Marwood C, Gensemer R, Solomon K, Greenberg BM (1997) Inhibition of photosynthesis as an endpoint for photoinduced toxicity of PAHs. In: Dwyer TR, Doane ML, Hinman FJ (eds) Environmental toxicology and risk assessment: modeling and risk assessment, vol 6, pp 443–454

    Google Scholar 

  • Jeelani N, WenY XL, Qiao Y, An S, Xin L (2017) Phytoremediation potential of Acorus calamus in soils co-contaminated with cadmium and polycyclic aromatic hydrocarbons. Sci Rep UK 7:8028

    Google Scholar 

  • 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 Phytoremediation 20:773–779

    CAS  Google Scholar 

  • Khan S, Hesham EL, Gu Q, Shuang L, He J (2009) Biodegradation of pyrene and catabolic genes in contaminated soils cultivated with Lolium multiflorum L. J Soils Sediments 9:482–491

    CAS  Google Scholar 

  • Kvesitadze G (2013) Degradation of anthropogenic contaminants by higher plants. Biotechnol Acta 6:132–143

    Google Scholar 

  • Kvesitadze GI, Khatisashvili GA, Sadunishvili TA, Evstigneev ZG (2005) Metabolizm antropogennykh toksikantov v vysshikhr asteniyakh (metabolism of anthropogenic toxicants in higher plants). Nauka, Moscow (In Russian)

    Google Scholar 

  • Lin Q, Shen KL, Zhao HM, Li WH (2008) Growth response of Zea mays L. in pyrene-copper co-contaminated soil and the fate of pollutants. J Hazard Mater 150:515–521

    CAS  Google Scholar 

  • Lux A, Martinka M, Vaculik M, White PJ (2010) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37

    Google Scholar 

  • Martí MC, Camejo D, Fernández-García N, Rellán-Álvarez R, Marques S, Sevilla F, Jiménez A (2009) Effect of oil refinery sludges on the growth and antioxidant system of alfalfa plants. J Hazard Mater 171:879–885

    Google Scholar 

  • Mendoza-Cózatl DG, Jobe TO, Hauser F, Schroeder JI (2011) Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic. Curr Opin Plant Biol 14:554–562

    Google Scholar 

  • Morozova OV, Shumakovich GP, Shleev SV, Yaropolov YI (2007) Laccase-mediator systems and their applications: a review. Appl Biochem Microbiol 43:523–535

    CAS  Google Scholar 

  • Muratova A, Lyubun Y, German K, Turkovskaya O (2015) Effect of cadmium stress and inoculation with a heavy-metal-resistant bacterium on the growth and enzyme activity of Sorghum bicolor. Environ Sci Pollut Res 22:16098–16109

    CAS  Google Scholar 

  • Muratova AY, Dmitrieva TV, Panchenko LV, Turkovskaya OV (2008) Phytoremediation of oil-sludge-contaminated soil. Int J Phytoremediation 10:486–502

    CAS  Google Scholar 

  • Nehnevajova E, Lyubenova L, Herzig R, Schröder P, Schwitzguébel J-P, Schmülling T (2012) Metal accumulation and response of antioxidant enzymes in seedlings and adult sunflower mutants with improved metal removal traits on a metal-contaminated soil. Environ Exp Bot 76:39–48

    CAS  Google Scholar 

  • Osuagwu AN, Okigbo AU, Ekpo IA, Chukwurah PN, Agbor RB (2013) Effect of crude oil pollution on growth parameters, chlorophyll content and bulbils yield in air potato (Dioscorea bulbifera L.). Int J Appl Sci Technol 3:37–42

    Google Scholar 

  • Panda S, Chaudhury I, Khan M (2003) Heavy metals induce lipid peroxidation and affect antioxidants in wheat leaves. Biol Plant 46:289–294

    CAS  Google Scholar 

  • Pašková V, Hilscherová K, Smutná M, Blaha L (2006) Toxic effects and oxidative stress in higher plants exposed to polycyclic aromatic hydrocarbons and their N‐heterocyclic derivatives. Environmental Toxicology and Chemistry. 25. 3238-3245

  • Pierattini EC, Francini A, Huber C, Sebastiani L, Schröder P (2018) Poplar and diclofenac pollution: a focus on physiology, oxidative stress and uptake in plant organs. Sci Total Environ 636:944–952

    CAS  Google Scholar 

  • Pilon-Smits EAH, Zhu YL, Sears T, Terry N (2000) Overexpression of glutathione reductase in Brassica juncea: effects on cadmium accumulation and tolerance. Physiol Plant 110:455–460

    CAS  Google Scholar 

  • Pinto AP, Mota AM, de Varennes A, Pinto FC (2004) Influence of organic matter on the uptake of cadmium, zinc, copper and iron by sorghum plants. Sci Total Environ 326:239–247

    CAS  Google Scholar 

  • Prasad MNV (1995) Cadmium toxicity and tolerance in vascular plants. Environ Exp Bot 35:525–545

    CAS  Google Scholar 

  • Romero-Puertas MC, Corpas FJ, Rodríguez-Serrano M, Gómez M, del Río LA, Sandalio LM (2007) Differential expression and regulation of antioxidative enzymes by cadmium in pea plants. J Plant Physiol 164:1346–1357

    CAS  Google Scholar 

  • Roy S, Pellinen J, Sen CK, Hänninen O (1994) Benzo(a)anthracene and benzo(a)pyrene exposure in the aquatic plant Fontinalis antipyretica: uptake, elimination and the responses of biotransformation and antioxidant enzymes. Chemosphere 29:1301–1311

    Google Scholar 

  • Rusin M, Gospodarek J, Barczyk G, Nadgórska-Socha A (2018) Antioxidant responses of Triticum aestivum plants to petroleum-derived substances. Ecotoxicology 27:1353–1367

    CAS  Google Scholar 

  • Saini S, Dhania G (2020) Cadmium as an environmental pollutant: ecotoxicological effects, health hazards, and bioremediation approaches for its detoxification from contaminated sites. In: Bioremediation of industrial waste for environmental safety. Springer, Singapore, pp 357–387

    Google Scholar 

  • Schröder P, Lyubenova L, Huber C (2009) Do heavy metals and metalloids influence the detoxification of organic xenobiotics in plants? Environ Sci Pollut Res 16:795–804

    Google Scholar 

  • Schröder P (2007) Exploiting plant metabolism for the phytoremediation of organic xenobiotics. In: Willey N (ed) Methods in biotechnology, Phytoremediation: methods and reviews, vol 23. Humana Press Inc., Totowa, pp 251–263

    Google Scholar 

  • Somtrakoon K, Chouychai W (2018) Removal of phenanthrene and cadmium from co-contaminated alkaline soil by carpet grass, Siam weed and winged bean. J Environ Biol 39:558–564

    CAS  Google Scholar 

  • Soudek P, Petrová Š, Vaňková R, Song J, Vaněk T (2014) Accumulation of heavy metals using Sorghum sp. Chemosphere 104:15–24

    CAS  Google Scholar 

  • Stiborová M, Anzenbacher P (1991) What are the principal enzymes oxidizing the xenobiotics in plants: cytochromes p-450 or peroxidases? (a hypothesis). Gen Physiol Biophys 10:209–216

    Google Scholar 

  • Tabassum S, Shahid N, Wang J, Shafiq M, Mumtaz M, Arslan M (2016) The oxidative stress response of Mirabilis jalapa to exhausted engine oil (EEO) during phytoremediation. Pol J Environ Stud 25:2581–2587

    CAS  Google Scholar 

  • Tamás L, Bočová B, Huttová J, Mistrík I, Ollé M (2006) Cadmium-induced inhibition of apoplastic ascorbate oxidase in barley roots. Plant Growth Regul 48:41–49

    Google Scholar 

  • Titov AF, Kaznina NM, Talanova VV (2014) Tyazhelye metally i resteniya (heavy metals and plants). Karelian Research Centre of the RAS, Petrozavodsk (In Russian)

    Google Scholar 

  • Tran TA, Popova LP (2013) Functions and toxicity of cadmium in plants: recent advances and future prospects. Turk J Bot 37:1–13

    CAS  Google Scholar 

  • Ugrekhelidze D, Korte F, Kvesitadze G (1997) Uptake and transformation of benzene and toluene by plant leaves. Ecotoxicol Environ Saf 37:24–29

    CAS  Google Scholar 

  • von Wettstein D (1957) Chlorophyll-letale und der submicroskoposche Formwechsel der Plastiden. Exp Cell Res 12:427–506

    Google Scholar 

  • Wang J, Liu X, Zhang X, Liang X, Zhang W (2011) Growth response and phytoremediation ability of Reed for diesel contaminant. In: 2nd International Conference on Environmental Science and Technology IPCBEE, vol 6. IACSIT Press, Singapore, pp V1–V233 http://www.ipcbee.com/vol6/no1/53-F00105.pdf

    Google Scholar 

  • Wang K, Zhu Z, Huang H, Li T, He Z, Yang X, Alva A (2012) Interactive effects of cd and PAHs on contaminants removal from co-contaminated soil planted with hyperaccumulator plant Sedum alfredii. J Soils Sediments 12:556–564

    CAS  Google Scholar 

  • Wang W, Zhang X, Huang J, Yan C, Zhang Q, Lu H, Liu J (2014) Interactive effects of cadmium and pyrene on contaminant removal from co-contaminated sediment planted with mangrove Kandelia obovata (S., L.) Yong seedlings. Mar Pollut Bull 84:306–313

    CAS  Google Scholar 

  • Wintermans JF, de Mots A (1965) Spectrophotometric characteristics of chlorophylls a and b and their pheophytins in ethanol. Biochim Biophys Acta 109:448–453

    CAS  Google Scholar 

  • Wong K-K, Quilty B, Surif S (2013) Degradation of crude oil in the presence of lead (Pb) and cadmium (Cd) by a metal-adapted consortium culture. Adv Environ Biol 7:577–585

    CAS  Google Scholar 

  • Yang Y-J, Cheng L-M, Liu Z-H (2007) Rapid effect of cadmium on lignin biosynthesis in soybean roots. Plant Sci 172:632–639

    CAS  Google Scholar 

  • Zengin FK, Munzuroglu O (2005) Effects of some heavy metals on content of chlorophyll, proline and some antioxidant chemicals in bean (Phaseolus vulgaris L.) seedlings. Acta Biol Cracov Ser Bot 47:157–164

    Google Scholar 

  • Zhang H, Dang Z, Zheng LC, Yi XY (2009) Remediation of soil co-contaminated with pyrene and cadmium by growing maize (Zea mays L.). Int J Environ Sci Technol 6:249–258

    Google Scholar 

  • Zukauskaite A, Jakubauskaite V, Belous O, Ambrazaitiene D, Stasiskiene Z (2008) Impact of heavy metals on the oil products biodegradation process. Waste Manag Res 26:500–507

    CAS  Google Scholar 

Download references

Funding

This study was supported in part by the Russian Foundation for Basic Research (project no. 18-29-05062\18).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yelena Lyubun.

Additional information

Responsible Editor: Gangrong Shi

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

Lyubun, Y., Muratova, A., Dubrovskaya, E. et al. Combined effects of cadmium and oil sludge on sorghum: growth, physiology, and contaminant removal. Environ Sci Pollut Res 27, 22720–22734 (2020). https://doi.org/10.1007/s11356-020-08789-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-08789-y

Keywords

Navigation