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Kinetics of nickel bioaccumulation and its relevance to selected cellular processes in leaves of Elodea canadensis during short-term exposure

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Abstract

Elodea canadensis is an aquatic macrophyte used widely as a bioindicator for the monitoring of water quality and in the phytoremediation of metal-contaminated waters. This study considers the kinetics of nickel bioaccumulation and changes in accompanying metabolic and stress-related physiological parameters. These include photosynthetic activity, pigment content, the accumulation of thiol-containing compounds, thiobarbituric acid-reactive substance (TBARS) products, and the activity of selected antioxidant enzymes (catalase, glutathione reductase, superoxide dismutase). Elodea leaves accumulated nickel according to pseudo-second-order kinetics, and the protective responses followed a time sequence which was related to the apparent rates of nickel accumulation. The applicability of second-order kinetics to the Ni uptake by Elodea leaves during the first 8 h of exposure to the metal suggested that the passive binding of metal ions (chemisorption) was a rate-limiting step at the initial phase of Ni accumulation. This phase was accompanied by an increase in photosynthetic activity together with elevated photosynthetic pigments and protein synthesis, the enhanced activity of antioxidant enzymes, and increased thiol concentration. In contrast, there was a decrease in metabolic activity upon the accumulation of TBARS, and the decline in enzyme activity was observed in the saturation phase of Ni accumulation (8–24 h). These results show that a correlation exists between the protective response and the apparent kinetic rate of Ni uptake. Thus, the time of exposure to the toxicant is a crucial factor in the activation of specific mechanisms of Ni detoxification and stress alleviation.

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References

  • Aebi H (1971) Catalases. Methods Enzym Anal 3:273–286

    Google Scholar 

  • Bishop PL, Eighmy TT (1989) Aquatic wastewater treatment using Elodea nuttallii. J Water Pollut Cont Fed 61:641–648

    Google Scholar 

  • Bondareva L, Vlasova I, Mogilnaya O, Bolsunovsky A, Kalmykov S (2010) Microdistribution of 241Am in structures of submerged macrophyte Elodea canadensis growing in the Yenisei River. J Environ Radioact 101:16–21

    Article  CAS  PubMed  Google Scholar 

  • Calabrese EJ (1999) Evidence that hormesis represents an “overcompensation” response to a disruption in homeostasis. Ecotoxicol Environ Saf 42:135–137. doi:10.1006/eesa.1998.1729

    Article  Google Scholar 

  • Calabrese EJ, Blain RB (2009) Hormesis and plant biology. Environ Pollut 157:42–48. doi:10.1016/j.envpol.2008.07.028

    Article  CAS  PubMed  Google Scholar 

  • Cempel M, Nikel G (2006) Nickel: a review of its sources and environmental toxicology. Pol J Environ Stud 15:375–382. doi:10.1109/TUFFC.2008.827

    CAS  Google Scholar 

  • Chen C, Huang D, Liu J (2009) Functions and toxicity of nickel in plants: recent advances and future prospects. Clean 37(4–5):304–313

    CAS  Google Scholar 

  • Chorom M, Parnian A, Jaafarzadeh N, Cultures AS (2012) Nickel removal by the aquatic plant (Ceratophyllum demersum L.). Int J Environ Sci Dev 3:4–7

    Google Scholar 

  • Chukina NV, Borisova GG (2010) Structural and functional parameters of higher aquatic plants from habitats differing in levels of anthropogenic impact. Inland Water Biol 3(1):44–50. doi:10.1134/S1995082910010062

    Article  Google Scholar 

  • Combroux I, Baumberger T, Viglione J, Laffont-Schwob I (2015) Selection of wild macrophytes for use in constructed wetlands for phytoremediation of contaminant mixtures. J Environ Manag 147:108–123

    Article  Google Scholar 

  • Demirezen D, Aksoy A, Uruc K (2007) Effect of population density on growth, biomass and nickel accumulation capacity of Lemna gibba (Lemnaceae). Chemosphere 66:553–557

    Article  CAS  PubMed  Google Scholar 

  • Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77

    Article  CAS  PubMed  Google Scholar 

  • Ermachenko LA, Ermachenko VM (1999) Atomic-absorption analysis with a graphite furnace [in Russian]. Podunova L.G. (Ed.). PAIMS, Moscow, 220 p

  • Fernández-Luqueño F, López-Valdez F, Gamero-Melo P, Luna-Suarez SS, Aguilera-González EN, Martínez AI, Garcia-Guillemo MS, Hernández-Martínez G, Herrera-Mendoza R, Álvarez-Garza MA, Pérez-Velázquez IR (2013) Heavy metal pollution in drinking water—a global risk for human health: a review. Afr J Environ Sci Technol 7:567–584. doi:10.5897/AJEST12.197

    Google Scholar 

  • Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 13:21–25

    Article  Google Scholar 

  • Hadad HR, Maine MA, Bonetto CA (2006) Macrophyte growth in a pilot-scale constructed wetland for industrial wastewater treatment. Chemosphere 63:1744–1753

  • Hadad HR, Maine MA, Mufarrege MM, Del Sastre MV, Di Luca GA (2011) Bioaccumulation kinetics and toxic effects of Cr, Ni and Zn on Eichhornia crassipes. J Hazard Mater 190:1016–1022. doi:10.1016/j.jhazmat.2011.04.044

    Article  CAS  PubMed  Google Scholar 

  • Hanif MA, Nadeem R, Bhatti HN, Ahmad NR, Ansari TM (2007) Ni (II) biosorption by Cassia fistula (Golden Shower) biomass. J Hazard Mater 139:345–355. doi:10.1016/j.jhazmat.2006.06.040

    Article  CAS  PubMed  Google Scholar 

  • Ho YS (2004) Pseudo-isotherms using a second order kinetic expression constant. Adsorption 10:151–158. doi:10.1023/B:ADSO.0000039870.28835.09

    Article  CAS  Google Scholar 

  • Ho YS (2005) Comments on “Chitosan functionalized with 2[-bis-(pyridylmethyl) aminomethyl]4-methyl-6-formyl-phenol: equilibrium and kinetics of copper (II) adsorption”. Polymer 46:1451–1452. doi:10.1016/j.polymer.2004.11.109

    Article  CAS  Google Scholar 

  • Ho YS, Wase DAJ, Forster CF (1996) Kinetic studies of competitive heavy metal adsorption by sphagnum moss peat. Environ Technol 17:71–77

    Article  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circular 347, University of California, College of Agriculture, Berkeley

  • Hossain MA, Piyatida P, Teixeira da Silva JA, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot Article ID 872875, 37 p http://dx.doi.org/10.1155/2012/872875

  • Järup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182. doi:10.1093/bmb/ldg032

    Article  PubMed  Google Scholar 

  • Kadlec RH, Wallace SD (2009) Treatment Wetlands, 2nd edn. CRC Press, Boca Raton, FL, USA, 1016 p

    Google Scholar 

  • Kadlec RH, Zmarthie LA (2010) Wetland treatment of leachate from a closed landfill. Ecol Eng 36:946–957

    Article  Google Scholar 

  • Kähkönen MA, Kairesalo T (1998) The effects of nickel on the nutrient fluxes and on the growth of Elodea canadensis. Chemosphere 37:1521–1530

    Article  Google Scholar 

  • Kähkönen MA, Manninen PKG (1998) The uptake of nickel and chromium from water by Elodea canadensis at different nickel and chromium exposure levels. Chemosphere 36:1381–1390

    Article  Google Scholar 

  • Kara Y, Basaran D, Kara I, Zeytunluoglu A, Genc H (2003) Bioaccumulation of nickel by aquatic macrophyta Lemna minor (Duckweed). Int J Agric Biol 5:281–283

    CAS  Google Scholar 

  • Khan S, Ahmad I, Shah MT, Rehman S, Khaliq A (2009) Use of constructed wetland for the removal of heavy metals from industrial wastewater. J Environ Manag 90:3451–3457

    Article  CAS  Google Scholar 

  • Kumar PS, Kirthika K (2009) Equilibrium and kinetic study of adsorption of nickel from aqueous solution onto bael tree leaf powder. Int J Eng Sci Technol 4:351–363

    Google Scholar 

  • Kumar GP, Prasad MNV (2004) Photosynthetic pigments and gaseous exchange in cadmium exposed Ceratophyllum demersum L. (a freshwater macrophyte) – a model for hormesis. J Plant Biology 31:1–8

  • Kumar B, Singla-Pareek SL, Sopory SK (2010) Glutathione homeostasis: crucial for abiotic stress tolerance in plants. In: Pareek A, Sopory SK, Bohnert HJ, Govindjee (eds) Abiotic stress adaptation in plants, physiological, molecular and genomic foundation. Springer, Netherlands, pp 263–282

  • Küpper H, Kroneck PMH (2007) Nickel in the environment and its role in the metabolism of plants and cyanobacteria. Met Ions Life Sci 2:31–62

    Google Scholar 

  • Leshem YY, Kuiper PJC (1996) Is there a GAS (general adaptation syndrome) response to various types of environmental stress? Biol Plant 38:1–18

    Article  Google Scholar 

  • Lichtenthaler H (1987) Chlorophylls and carotenoid: pigments of photosynthetic membranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Liu Y, Shen L (2008) From Langmuir kinetics to first- and second-order rate equations for adsorption. Langmuir 24:11625–11630. doi:10.1021/la801839b

    Article  CAS  PubMed  Google Scholar 

  • Lone MI, He Z, Stoffella PJ, Yang X (2008) Phytoremediation of heavy metal polluted soils and water: progresses and perspectives. J Zhejiang Univ Sci B 9:210–220. doi:10.1631/jzus.B0710633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mal TK, Adorjan P, Corbett AL (2002) Effect of copper on growth of an aquatic macrophyte, Elodea canadensis. Environ Pollut 120:307–311

    Article  CAS  PubMed  Google Scholar 

  • Malec P, Maleva MG, Prasad MNV, Strzałka K (2009a) Identification and characterization of Cd-induced peptides in Egeria densa (water weed): putative role in Cd detoxification. Aquat Toxicol 95:213–221

    Article  CAS  PubMed  Google Scholar 

  • Malec P, Maleva MG, Prasad MNV, Strzałka K (2009b) Copper toxicity in leaves of Elodea canadensis Michx. Bull Environ Contam Toxicol 82:627–632

    Article  CAS  PubMed  Google Scholar 

  • Malec P, Maleva MG, Prasad MNV, Strzałka K (2010) Responses of Lemna trisulca (Duckweed) exposed to low doses of cadmium: thiols, metal binding complexes, and photosynthetic pigments as sensitive biomarkers of ecotoxicity. Protoplasma 240:69–74

    Article  CAS  PubMed  Google Scholar 

  • Malec P, Myśliwa-Kurdziel B, Prasad MNV, Waloszek A, Strzałka K (2011) Role of aquatic macrophytes in biogeochemical cycling of heavy metals, relevance to soil-sediment continuum detoxification and ecosystem health. In: Sherameti I, Varma A (eds) Detoxification of heavy metals. Springer, Berlin, pp 345–368

    Chapter  Google Scholar 

  • Maleva MG, Nekrasova GF, Malec P, Prasad MNV, Strzałka K (2009) Ecophysiological tolerance of Elodea canadensis to nickel exposure. Chemosphere 77:393–398

    Article  Google Scholar 

  • Martins RJE, Vilar VJP, Boaventura RAR (2014) Kinetic modelling of cadmium and lead removal by aquatic mosses. Braz J Chem Eng 31:229–242

    Article  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Mkandawire M, Dudel EG (2007) Are Lemna spp. effective phytoremediation agents? Bioremed Biodiv Bioavail 1:56–71

    Google Scholar 

  • Murphy KJ (2002) Plant communities and plant diversity in softwater lakes of northern Europe. Aquat Bot 73:287–324

    Article  Google Scholar 

  • Nagalakshmi N, Prasad MNV (2001) Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160:291–299

    Article  CAS  PubMed  Google Scholar 

  • Neminen TM, Ukonmaanaho L, Rausch N, Shotyk W (2007) Biogeochemistry of nickel and its release into the environment. Met Ions Life Sci 2:1–30

    Google Scholar 

  • Paoletti F, Macali A (1990) Determination of superoxide dismutase activity by purely chemical system based on NAD (P) H oxidation. Meth Enzymol 186:209–220

    Article  CAS  PubMed  Google Scholar 

  • Prasad MNV, Malec P, Waloszek A, Bojko M, Strzałka K (2001) Physiological responses of Lemna trisulca L. (Duckweed) to cadmium and copper bioaccumulation. Plant Sci 161:881–889

    Article  CAS  Google Scholar 

  • Schiewer S, Wong MH (1999) Metal binding stoichiometry and isotherm choice in biosorption. Environ Sci Technol 33:3821–3828

    Article  CAS  Google Scholar 

  • Shakterle TR, Pollack RL (1973) A simplified method for the quantities assay of small amounts of protein in biological material. Analyt Biochem 51:654–655

    Article  Google Scholar 

  • Thiébaut G, Gross Y, Gierlinski P, Boiché A (2010) Accumulation of metals in Elodea canadensis and Elodea nuttallii: implications for plant–macroinvertebrate interactions. Sci Total Environ 408:5499–5505

    Article  PubMed  Google Scholar 

  • Uchiyama M, Mihara M (1978) Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Analyt Biochem 86:287–297

    Article  Google Scholar 

  • Vymazal J (2009) The use constructed wetlands with horizontal sub-surface flow for various types of wastewater. Ecol Eng 35:1–17

    Article  Google Scholar 

  • Vymazal J (2013) Emergent plants used in free water surface constructed wetlands: a review. Ecol Eng 61:501–504

    Article  Google Scholar 

Download references

Acknowledgments

MNVP gratefully acknowledges KS for hosting a 1-month visit in June 2014. MNVP is also thankful to the Ural Federal University (UrFU), Ekaterinburg, for the “Visiting Professorship.” The Faculty of Biochemistry, Biophysics and Biotechnology of Jagiellonian University is a partner of the Leading National Research Center (KNOW) supported by the Ministry of Science and Higher Education.

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The authors report no conflicts of interest.

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Authors and Affiliations

  1. Department of Plant Physiology and Biochemistry, Ural Federal University named after the first President of Russia B.N. Yeltsin, Lenin av. 51, Ekaterinburg, Russia, 620000

    Maria G. Maleva & Majeti Narasimha Vara Prasad

  2. Department of Plant Physiology and Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, ul. Gronostajowa 7, 30-387, Kraków, Poland

    Przemysław Malec & Kazimierz Strzałka

  3. Department of Plant Sciences, University of Hyderabad, Hyderabad, Telangana, 500 046, India

    Majeti Narasimha Vara Prasad

Authors
  1. Maria G. Maleva
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  2. Przemysław Malec
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  3. Majeti Narasimha Vara Prasad
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  4. Kazimierz Strzałka
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Corresponding author

Correspondence to Kazimierz Strzałka.

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Maleva, M.G., Malec, P., Prasad, M.N.V. et al. Kinetics of nickel bioaccumulation and its relevance to selected cellular processes in leaves of Elodea canadensis during short-term exposure. Protoplasma 253, 543–551 (2016). https://doi.org/10.1007/s00709-015-0832-3

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