Abstract
In order to study the bioaccumulation of Pb, Cr, Ni, and Zn and the stress response, the floating aquatic plant Limnobium laevigatum was exposed to increasing concentrations of a mixture of these metals for 28 days, and its potential use in the treatment of wastewater was evaluated. The metal concentrations of the treatment 1 (T1) were Pb 1 μg L−1, Cr 4 μg L−1, Ni 25 μg L−1, and Zn 30 μg L−1; of treatment 2 (T2) were Pb 70 μg L−1, Cr 70 μg L−1, Ni 70 μg L−1, and Zn 70 μg L−1; and of treatment 3 (T3) were Pb 1000 μg L−1, Cr 1000 μg L−1, Ni 500 μg L−1, and Zn 100 μg L−1, and there was also a control group (without added metal). The accumulation of Pb, Cr, Ni, and Zn in roots was higher than in leaves of L. laevigatum, and the bioconcentration factor revealed that the concentrations of Ni and Zn in the leaf and root exceeded by over a thousand times the concentrations of those in the culture medium (2000 in leaf and 6800 in root for Ni; 3300 in leaf and 11,500 in root for Zn). Thus, this species can be considered as a hyperaccumulator of these metals. In general, the changes observed in the morphological and physiological parameters and the formation of products of lipid peroxidation of membranes during the exposure to moderate concentrations (T2) of the mixture of metals did not cause harmful effects to the survival of the species within the first 14 days of exposure. Taking into account the accumulation capacity and tolerance to heavy metals, L. laevigatum is suitable for phytoremediation in aquatic environments contaminated with moderated concentrations of Cr, Ni, Pb, and Zn in the early stages of exposure.
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Andra SS, Datta R, Sarkar D, Saminathan SKM, Mullens CP, Bach SBH (2009) Analysis of phytochelatin complexes in the lead tolerant vetiver grass [Vetiveria zizanioides (L.)] using liquid chromatography and mass spectrometry. Environ Pollut 157:2173–2183. doi:10.1016/j.envpol.2009.02.014
Apel K, Hirt H (2004) REACTIVE OXYGEN SPECIES: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. doi:10.1146/annurev.arplant.55.031903.141701
Aponte H, Pacherres CO (2013) Growth and propagation of Limnobium laevigatum (Hydrocharitaceae) under different nutrient concentrations. Biologist 11:69–78
Argentina Legislation (1991) Law 24051 (Ley Nacional 24051 de la República Argentina). URL: http://www2.medioambiente.gov.ar/mlegal/residuos/ley24051.htm. Accessed 21 Dec 2016
Assunção AGL, Schat H, Aarts MGM (2003) Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytol 159:351–360. doi:10.1046/j.1469-8137.2003.00820.x
Cheng S (2003) Heavy metals in plants and phytoremediation. Environ Sci Pollut Res 10:335–340. doi:10.1065/espr2002.11.141.3
Choi JH, Park SS, Jaffé PR (2006) The effect of emergent macrophytes on the dynamics of sulfur species and trace metals in wetland sediments. Environ Pollut 140:286–293. doi:10.1016/j.envpol.2005.07.009
Cook CDK, Urmi-König K (1983) A revision of the genus Limnobium including Hydromystria (hydrocharitaceae). Aquat Bot 17:1–27. doi:10.1016/0304-3770(83)90015-3
Dhir B, Sharmila P, Saradhi PP (2004) Hydrophytes lack potential to exhibit cadmium stress induced enhancement in lipid peroxidation and accumulation of proline. Aquat Toxicol 66:141–147. doi:10.1016/j.aquatox.2003.08.005
Doust JL, Schmidt M, Doust LL (1994) Biological assessment of aquatic pollution: a review, with emphasis on plants as biomonitors. Biol Rev 69:147–186. doi:10.1111/j.1469-185X.1994.tb01504.x
Duman F, Leblebici Z, Aksoy A (2009) Growth and bioaccumulation characteristics of watercress (Nasturtium officinale R. BR.) exposed to cadmium, cobalt and chromium. Chem Speciat Bioavailab 21:257–265. doi:10.3184/095422909X12578511366924
Eun S-O, Shik Youn H, Lee Y (2000) Lead disturbs microtubule organization in the root meristem of Zea mays. Physiol Plant 110:357–365. doi:10.1111/j.1399-3054.2000.1100310.x
Förstner U, Wittmann GT (1981) Metal pollution in the aquatic environment. Springer-Verlag, Berlin
Franzaring J, Klumpp A, Fangmeier A (2007) Active biomonitoring of airborne fluoride near an HF producing factory using standardised grass cultures. Atmos Environ 41:4828–4840. doi:10.1016/j.atmosenv.2007.02.010
Fu J, Hu X, Tao X, Yu H, Zhang X (2013) Risk and toxicity assessments of heavy metals in sediments and fishes from the Yangtze River and Taihu Lake. China Chemosphere 93:1887–1895. doi:10.1016/j.chemosphere.2013.06.061
Garbisu C, Alkorta I (2001) Phytoextraction: a cost-effective plant-based technology for the removal of metals from the environment. Bioresour Technol 77:229–236. doi:10.1016/S0960-8524(00)00108-5
García Vargas D (2007) Efectos fisiológicos y compartimentación radicular en plantas de Zea mays L. expuestas a la toxicidad por plomo. Doctoral, Universitat Autònoma de Barcelona
Gupta M, Chandra P (1994) Lead accumulation and toxicity in Vallisneria spiralis.(L.) and Hydrilla verticillata (l.f.) Royle Journal of Environmental Science and Health Part A: Environmental Science and Engineering and Toxicology 29:503–516. doi:10.1080/10934529409376051
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
Harguinteguy CA, Schreiber R, Pignata ML (2013) Myriophyllum aquaticum As a biomonitor of water heavy metal input related to agricultural activities in the Xanaes River (Córdoba, Argentina). Ecol Indic 27:8–16. doi:10.1016/j.ecolind.2012.11.018
Harguinteguy CA, Cirelli AF, Pignata ML (2014) Heavy metal accumulation in leaves of aquatic plant Stuckenia filiformis and its relationship with sediment and water in the Suquía river (Argentina). Microchem J 114:111–118. doi:10.1016/j.microc.2013.12.010
Harguinteguy CA, Pignata ML, Fernández-Cirelli A (2015) Nickel, lead and zinc accumulation and performance in relation to their use in phytoremediation of macrophytes Myriophyllum aquaticum and Egeria densa. Ecol Eng 82:512–516. doi:10.1016/j.ecoleng.2015.05.039
Harguinteguy CA, Noelia Cofré M, Fernández-Cirelli A, Luisa Pignata M (2016) The macrophytes Potamogeton pusillus L. and Myriophyllum aquaticum (Vell.) Verdc. as potential bioindicators of a river contaminated by heavy metals. Microchem J 124:228–234. doi:10.1016/j.microc.2015.08.014
Jackson L (1998) Paradigms of metal accumulation in rooted aquatic vascular plants. Sci Total Environ 219:223–231. doi:10.1016/S0048-9697(98)00231-9
Kabata-Pendias A, Pendias H (2001) Trace elements in soils and plants. CRC Press, London
Kastratović V, Jaćimović Ž, Đurović D, Bigović M, Krivokapić S (2015) Lemna minor L. as bioindicator of heavy metal pollution in Skadar Lake (Montenegro) Kragujevac. Journal of Science 37:123–134
Khellaf N, Zerdaoui M (2009) Phytoaccumulation of zinc by the aquatic plant, Lemna gibba L. Bioresour Technol 100:6137–6140. doi:10.1016/j.biortech.2009.06.043
Kunze R, Frommer WB, Flügge U-I (2002) Metabolic engineering of plants: the role of membrane transport. Metab Eng 4:57–66. doi:10.1006/mben.2001.0207
Lafont M (2002) A conceptual approach to the biomonitoring of freshwater: the ecological ambience system. J Limnol 60:17–24. doi:10.4081/jlimnol.2001.s1.17
Levin AG, Pignata ML (1995) Ramalina ecklonii as a bioindicator of atmospheric pollution in Argentina. Can J Bot 73:1196–1202. doi:10.1139/b95-129
Li Y, Zhang S, Jiang W, Liu D (2013) Cadmium accumulation, activities of antioxidant enzymes, and malondialdehyde (MDA) content in Pistia stratiotes L. Environ Sci Pollut Res 20:1117–1123. doi:10.1007/s11356-012-1054-2
Liao S, Chang W-L (2004) Heavy metal phytoremediation by water hyacinth at constructed wetlands in Taiwan. Photogramm Eng Remote Sensing 54:177–185
Maine MA, Suñé NL, Lagger SC (2004) Chromium bioaccumulation: comparison of the capacity of two floating aquatic macrophytes. Water Res 38:1494–1501. doi:10.1016/j.watres.2003.12.025
Maleva MG, Nekrasova GF, Malec P, Prasad MNV, Strzałka K (2009) Ecophysiological tolerance of Elodea canadensis to nickel exposure. Chemosphere 77:392–398. doi:10.1016/j.chemosphere.2009.07.024
Megateli S, Semsari S, Couderchet M (2009) Toxicity and removal of heavy metals (cadmium, copper, and zinc) by Lemna gibba. Ecotoxicol Environ Saf 72:1774–1780. doi:10.1016/j.ecoenv.2009.05.004
Merlo C et al (2011) Integral assessment of pollution in the Suquía River (Córdoba, Argentina) as a contribution to lotic ecosystem restoration programs. Sci Total Environ 409:5034–5045. doi:10.1016/j.scitotenv.2011.08.037
Metwally A, Safronova VI, Belimov AA, Dietz K-J (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot 56:167–178. doi:10.1093/jxb/eri017
Miretzky P, Saralegui A, Fernandez Cirelli A (2006) Simultaneous heavy metal removal mechanism by dead macrophytes. Chemosphere 62:247–254. doi:10.1016/j.chemosphere.2005.05.010
Mishra VK, Tripathi B (2008) Concurrent removal and accumulation of heavy metals by the three aquatic macrophytes. Bioresour Technol 99:7091–7097. doi:10.1016/j.biortech.2008.01.002
Murillo Castillo PA, Novoa Acuna LG, Rodríguez Miranda JP (2012) Evaluación de un humedal artificial de flujo superficial con Limnobium laevigatum para el tratamiento de aguas residuales combinadas (domésticas y pecuarias) en Bogotá D.C. Colombia Tecno ambiente: Revista profesional de tecnología y equipamiento de ingeniería ambiental 22:9–16
Nekrasova G, Ushakova O, Ermakov A, Uimin M, Byzov I (2011) Effects of copper(II) ions and copper oxide nanoparticles on Elodea densa Planch Russian. J Ecol 42:458–463. doi:10.1134/s1067413611060117
Nichols PB, Couch JD, Al-Hamdani SH (2000) Selected physiological responses of Salvinia minima to different chromium concentrations. Aquat Bot 68:313–319. doi:10.1016/S0304-3770(00)00128-5
Olguín EJ, Sánchez-Galván G (2012) Heavy metal removal in phytofiltration and phycoremediation: the need to differentiate between bioadsorption and bioaccumulation. New Biotechnol 30:3–8. doi:10.1016/j.nbt.2012.05.020
Ozturk F, Duman F, Leblebici Z, Temizgul R (2010) Arsenic accumulation and biological responses of watercress (Nasturtium officinale R. Br.) exposed to arsenite. Environ Exp Bot 69:167–174. doi:10.1016/j.envexpbot.2010.03.006
Paiva LB, de Oliveira JG, Azevedo RA, Ribeiro DR, da Silva MG, Vitória AP (2009) Ecophysiological responses of water hyacinth exposed to Cr3+ and Cr6+. Environ Exp Bot 65:403–409. doi:10.1016/j.envexpbot.2008.11.012
Pignata ML, Gudiño GL, Wannaz ED, Plá RR, González CM, Carreras HA, Orellana L (2002) Atmospheric quality and distribution of heavy metals in Argentina employing Tillandsia capillaris as a biomonitor. Environ Pollut 120:59–68. doi:10.1016/S0269-7491(02)00128-8
Polechońska L, Samecka-Cymerman A (2016) Bioaccumulation of macro- and trace elements by European frogbit (Hydrocharis morsus-ranae L.) in relation to environmental pollution. Environ Sci Pollut Res 23:3469–3480. doi:10.1007/s11356-015-5550-z
Prasad MNV, Strzałka K (1999) Impact of heavy metals on photosynthesis. In: Prasad MNV, Hagemeyer J (eds) Heavy metal stress in plants—from molecules to ecosystems. Springer, Berlin, pp 117–138
Samecka-Cymerman A, Kempers A (2004) Toxic metals in aquatic plants surviving in surface water polluted by copper mining industry. Ecotoxicol Environ Saf 59:64–69. doi:10.1016/j.ecoenv.2003.12.002
Sharma S, Singh B, Manchanda V (2015) Phytoremediation: role of terrestrial plants and aquatic macrophytes in the remediation of radionuclides and heavy metal contaminated soil and water. Environ Sci Pollut Res 22:946–962. doi:10.1007/s11356-014-3635-8
Singh R, Tripathi RD, Dwivedi S, Kumar A, Trivedi PK, Chakrabarty D (2010) Lead bioaccumulation potential of an aquatic macrophyte Najas indica are related to antioxidant system. Bioresour Technol 101:3025–3032. doi:10.1016/j.biortech.2009.12.031
Sinha S, Pandey K (2003) Nickel induced toxic effects and bioaccumulation in the submerged plant, Hydrilla verticillata (L.F.) Royle under repeated metal exposure. Bull Environ Contam Toxicol 71:1175–1183. doi:10.1007/s00128-003-8896-8
Smith VH (2003) Eutrophication of freshwater and coastal marine ecosystems a global problem. Environ Sci Pollut Res 10:126–139. doi:10.1065/espr2002.12.142
Soda S et al (2012) Constructed wetlands for advanced treatment of wastewater with a complex matrix from a metal-processing plant: Bioconcentration and translocation factors of various metals in Acorus gramineus and Cyperus alternifolius. Ecol Eng 39:63–70. doi:10.1016/j.ecoleng.2011.11.014
Somashekaraiah BV, Padmaja K, Prasad ARK (1992) Phytotoxicity of cadmium ions on germinating seedlings of mung bean (Phaseolus vulgaris): involvement of lipid peroxides in chlorphyll degradation. Physiol Plant 85:85–89. doi:10.1111/j.1399-3054.1992.tb05267.x
Umebese CE, Motajo AF (2008) Accumulation, tolerance and impact of aluminium, copper and zinc on growth and nitrate reductase activity of Ceratophyllum demersum (hornwort). J Environ Biol 29:197–200
Vangronsveld J, Clijsters H (1994) Toxic effects of metals. In: Farago ME (ed) Plants and the chemical elements: biochemistry, uptake, tolerance and toxicity. Wiley-VCH Verlag GmbH, pp 149–177. doi:10.1002/9783527615919.ch6
Veselý T, Tlustoš P, Száková J (2011) The use of water lettuce (Pistia stratiotes L.) for Rhizofiltration of a highly polluted solution by cadmium and lead. Int J Phytorem 13:859–872. doi:10.1080/15226514.2011.560214
Wang Q, Cui Y, Dong Y (2002) Phytoremediation of polluted waters potentials and prospects of wetland plants. Acta Biotechnol 22:199–208. doi:10.1002/1521-3846(200205)22:1/2<199::AID-ABIO199>3.0.CO;2-T
Wang C, Zhang SH, Wang PF, Qian J, Hou J, Zhang WJ, Lu J (2009) Excess Zn alters the nutrient uptake and induces the antioxidative responses in submerged plant Hydrilla verticillata (L.f.) Royle Chemosphere 76:938–945. doi:10.1016/j.chemosphere.2009.04.038
Wang Q, Li Z, Cheng S, Wu Z (2010) Effects of humic acids on phytoextraction of Cu and Cd from sediment by Elodea nuttallii. Chemosphere 78:604–608. doi:10.1016/j.chemosphere.2009.11.011
Winner RW, Gauss JD (1986) Relationship between chronic toxicity and bioaccumulation of copper, cadmium and zinc as affected by water hardness and humic acid. Aquat Toxicol 8:149–161. doi:10.1016/0166-445X(86)90061-5
Wintermans JFGM, De Mots A (1965) Spectrophotometric characteristics of chlorophylls a and b and their phenophytins in ethanol. Biochim Biophys Acta Biophys Incl Photosynth 109:448–453. doi:10.1016/0926-6585(65)90170-6
Yapoga S, Ossey YB, Kouame V (2013) Phytoremediation of zinc, cadmium, copper and chrome from industrial wastewater by Eichhornia crassipes. Int J Conserv Sci 4:81–86
Zayed A, Gowthaman S, Terry N (1998) Phytoaccumulation of trace elements by wetland plants: I duckweed. J Environ Qual 27:715–721. doi:10.2134/jeq1998.00472425002700030032x
Zurayk R, Sukkariyah B, Baalbaki R (2001) Common hydrophytes as bioindicators of nickel, chromium and cadmium pollution. Water Air Soil Pollut 127:373–388. doi:10.1023/A:1005209823111
Acknowledgements
This work was partially supported by the Agencia Nacional de Promoción Científica y Tecnológica (FONCyT PICT-2014-3474) and the Secretaría de Ciencia y Técnica de la Universidad Nacional de Córdoba (SECYT-UNC-2014). The authors wish to acknowledge the assistance of the Consejo Nacional de Investigación Científica y Técnicas (CONICET) and the Universidad Nacional de Córdoba, both of which supported the facilities used in this investigation. The authors thank Dr. Paul Hobson, native speaker, for revision of the manuscript.
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Highlights
• Accumulation of Pb, Cr, Ni, and Zn in roots was higher than in leaves of L. laevigatum.
• This species can be considered as a hyperaccumulator of Ni and Zn.
• The toxicity of metals does not represent any danger to the survival of macrophytes.
• L. laevigatum is a species of interest for use in phytoremediation of wastewater.
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Arán, D.S., Harguinteguy, C.A., Fernandez-Cirelli, A. et al. Phytoextraction of Pb, Cr, Ni, and Zn using the aquatic plant Limnobium laevigatum and its potential use in the treatment of wastewater. Environ Sci Pollut Res 24, 18295–18308 (2017). https://doi.org/10.1007/s11356-017-9464-9
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DOI: https://doi.org/10.1007/s11356-017-9464-9