Effects of sewage sludge on bio-accumulation of heavy metals in tomato seedlings

  • Nada Elloumi Sfax University, Higher Institute of Biotechnology of Sfax. Laboratory of Water, Energy and Environment. BP 261 Sfax 3000
  • Dalel Belhaj Sfax University. National Engineering School of Sfax. Laboratory of Water, Energy and Environment. BP 1173 Sfax 3038
  • Boutheina Jerbi Sfax University. National Engineering School of Sfax. Laboratory of Water, Energy and Environment. BP 1173 Sfax 3038
  • Mohamed Zouari University of Limoges. Faculty of Pharmacy. Laboratory of Botany and Cryptogamy. GRESE EA 4330, 2 rue du Docteur Marcland, F-87025 Limoges
  • Monem Kallel Sfax University. National Engineering School of Sfax. Laboratory of Water, Energy and Environment. BP 1173 Sfax 3038
Keywords: sewage sludge amendment, soil fertility, biochemical responses, Solanum lycopersicum

Abstract

The proposal to use sewage sludge (SS) on agricultural fields as a sustainable way to dispose of the waste is based on its high organic and nutrients content. However, the presence of heavy metals (HMs) in sludge can contaminate crops and accumulate in the food chain. The aim of this study was to assess changes in soil fertility, biochemical responses of tomato (Solanum lycopersicum L. cv. Rio Grande) seedlings and the availability of HMs with increased rate application of SS (0, 2.5, 5 and 7.5%). Leaf chlorophyll content, nutritional status, proline, membrane peroxidation, stomatal conductance and HM accumulation were investigated. Results showed that the soil pH decreased, whereas soil salinity, organic carbon, total N, available P and exchangeable Na, Ca, K and HM content increased significantly with increasing application rates of SS. Among the three HMs (Zn, Cu and Cr), Zn had the highest capacity for transferring from soil into plants. Low metal translocation was observed from roots to leaves. The 7.5% SS dose decreased biomass production and caused a decline in chlorophyll content and stomatal conductance. However, lipid peroxidation and proline contents increased. Therefore, the use of 2.5 and 5% doses of sewage sludge in agriculture would be an efficient and cost-effective method to restore the fertility of soil and an environment-friendly solution for disposal problems.

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Author Biographies

Dalel Belhaj, Sfax University. National Engineering School of Sfax. Laboratory of Water, Energy and Environment. BP 1173 Sfax 3038


Boutheina Jerbi, Sfax University. National Engineering School of Sfax. Laboratory of Water, Energy and Environment. BP 1173 Sfax 3038

Monem Kallel, Sfax University. National Engineering School of Sfax. Laboratory of Water, Energy and Environment. BP 1173 Sfax 3038

References

Al-Harbi AR, Wahb-Allah MA, Abu-Muriefah SS, 2008. Salinity and nitrogen level affects germination, emergence, and seedling growth of tomato. Int J Veget Sci 14 (4): 380-392. http://dx.doi.org/10.1080/19315260802371369

Angin I, Aslantas R, Kose M, Karakurt H, Ozkan G, 2012. Changes in chemical properties of soil and sour cherry as a result of sewage sludge application. Hort Sci (Prague) 39: 61-66.

Antolín MC, Pascual I, García C, Polo A, Sánchez-Díaz M, 2005. Growth, yield and solute content of barley in soils treated with sewage sludge under semiarid Mediterranean conditions. Field Crop Res 94: 224-237. http://dx.doi.org/10.1016/j.fcr.2005.01.009

Antolín MC, Muro I, Sánchez-Díaz M, 2010. Application of sewage sludge improves growth, photosynthesis and antioxidant activities of nodulated alfalfa plants under drought conditions. Environ Exp Bot 68: 75-82. http://dx.doi.org/10.1016/j.envexpbot.2009.11.001

Araùjo ASF, Monteiro RTR, 2005. Plant bioassays to assess toxicity of textile sludge compost. Sci Agric Piracicaba Brazil 62: 286-290. http://dx.doi.org/10.1590/s0103-90162005000300013

Arnon DI, 1949. Copper enzymes in isolated chloroplast, polyphenol oxidase in Beta vulgaris. Plant Physiol 24: 1-15. http://dx.doi.org/10.1104/pp.24.1.1

Babel S, Dacera DM, 2005. Heavy metal removal from contaminated sludge for land application: A review. Waste Manage 26 (9): 988-1004. http://dx.doi.org/10.1016/j.wasman.2005.09.017

Bates LS, Waldran RP, Teare ID, 1973. Rapid determination of proline for water stress studies. Plant Soil 39: 205-208. http://dx.doi.org/10.1007/BF00018060

Čásová K, Černý J, Száková J, Balík J, Tlustoš P, 2009. Cadmium balance in soils under different fertilization managements including sewage sludge application. Plant Soil Environ 55 (8): 353-361.

Chandra R, Yadav S,Mohan D, 2008. Effect of distillery sludge on seed germination and growth parameters of green gram (Phaseolus mungo L.). J Hazard Mater 152: 431-439. http://dx.doi.org/10.1016/j.jhazmat.2007.06.124

Chen Y, Li X, Shen Z, 2004. Leaching and uptake of heavy metals by ten different species of plants during an EDTA-assisted phytoextraction process. Chemosphere 57: 187-196. http://dx.doi.org/10.1016/j.chemosphere.2004.05.044

Cui S, Zhou Q, Chao L, 2007. Potential hyper-accumulation of Pb, Zn, Cu and Cd in endurant plants distributed in an old smeltery, northeast China. Environ Geol 51: 1043-1048. http://dx.doi.org/10.1007/s00254-006-0373-3

Daud MK, Quiling H, Lei M, Ali B, Zhu SJ, 2015. Ultrastructural, metabolic and proteomic changes in leaves of upland cotton in response to cadmium stress. Chemosphere 120: 309-320. http://dx.doi.org/10.1016/j.chemosphere.2014.07.060

Di Salvatore M, Carafa A, Carratù G, 2008. Assessment of heavy metals phytotoxicity using seed germination and root elongation tests: A comparison of two growth substrates. Chemosphere 73: 1461-1464. http://dx.doi.org/10.1016/j.chemosphere.2008.07.061

EC, 1986. Council Directive of 12 June 1986 (86/278/EEC) concerning the protection of the environment, and in particular of the soil, when sewage sludge is used in agriculture. Off J Eur Communities L 181/6-12 of 04.07.1986. http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:31986L0278&from=EN.

Elloumi N, Zouari M, Chaari L, Jomni C, Ben Rouina B, Ben Abdallah F, 2014. Ecophysiological responses of almond (Prunusdulcis) seedlings to cadmium stress. Biologia 69: 604-609. http://dx.doi.org/10.2478/s11756-014-0348-x

Elloumi N, Zouari M, Chaari L, Ben AbdallahF, Woodward S, Kallel M, 2015. Effect of phosphogypsum on growth, physiology, and the antioxidative defense system in sunflower seedlings. Environ Sci Pollut Res 22: 14829-14840. http://dx.doi.org/10.1007/s11356-015-4716-z

Gajewska E, Niewiadomska E, Tokarz K, Slaba M, Sklodowska M, 2013. Nickel-induced changes in carbon metabolism in wheat shoots. J Plant Physiol 170: 369-377. http://dx.doi.org/10.1016/j.jplph.2012.10.012

Gao YZ, He JZ, Ling WT, Hu HQ, Liu F, 2003. Effects of organic acids on copper and cadmium desorption from contaminated soils. Environ Int 29: 613-618. http://dx.doi.org/10.1016/S0160-4120(03)00048-5

Gao X,Chen S, Long A, 2008.Composition and sources of organic matter and its solvent extractable components in surface sediments of a bay under serious anthropogenic influences: Daya Bay, China. Mar Pollut Bull 56:1066-1075. http://dx.doi.org/10.1016/j.marpolbul.2008.03.036

Gasco G, Lobo MC, 2007. Composition of a Spanish sewage sludge and effects on treated soil and olive trees. Waste Manage 27: 1494-1500. http://dx.doi.org/10.1016/j.wasman.2006.08.007

Gill SS, Tuteja N, 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909-930. http://dx.doi.org/10.1016/j.plaphy.2010.08.016

Gill SS, Khan NA, Tuteja N, 2012. Cadmium at high dose perturbs growth, photosynthesis and nitrogen metabolism while at low dose it up regulates sulfur assimilation and antioxidant machinery in garden cress (Lepidium sativum L.). Plant Sci 182: 112-120. http://dx.doi.org/10.1016/j.plantsci.2011.04.018

Gomes MP, LeManac'h SG, Maccario S, Labrecque M, Lucotte M, Juneau P, 2015. Differential effects of glyphosate and amino methyl phosphonic acid (AMPA) on photosynthesis and chlorophyll metabolism in willow plant. Pestic Biochem Phys 130: 65-70. http://dx.doi.org/10.1016/j.pestbp.2015.11.010

Gonçalves ICR, Araújo ASF, Nunes LAPL, Bezerra AAC,José de Melo W, 2014. Heavy metals and yield of cowpea cultivated under composted tannery sludge amendment. Acta Scienti Agron 63: 443-448. http://dx.doi.org/10.4025/actasciagron.v36i4.18094

Gratao PL, Monteiro CC, Rossi ML, Martinelli AP, Peres LEP, Medici LO, Lea PJ, Azevedo RA, 2009. Differential ultrastructural changes in tomato hormonal mutants exposed to cadmium. Environ Exp Bot 67: 387-394. http://dx.doi.org/10.1016/j.envexpbot.2009.06.017

Gunes A, Inal A, Bagci EG, Coban S, Sahin O, 2007. Silicon increases boron tolerance and reduces oxidative damage of wheat grown in soil with excess boron. Biol Plant 51: 571-574. http://dx.doi.org/10.1007/s10535-007-0125-6

Gupta AK, Sinha S, 2007. Phytoextraction capacity of the plants growing on tannery sludge dumping sites. Biores Technol 98: 1788-1794. http://dx.doi.org/10.1016/j.biortech.2006.06.028

Heath RL, Packer L, 1968. Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125: 189-198. http://dx.doi.org/10.1016/0003-9861(68)90654-1

Hoekstra NJ, Bosker T, Lantinga EA, 2002. Effects of cattle dung from farms with different feeding strategies on germination and initial root growth of cress (Lepidium sativum L.). Agric Ecosyst Environ 93: 189-196. http://dx.doi.org/10.1016/S0167-8809(01)00348-6

Hue NV, Ranjith SA, 1994. Sewage sludges in Hawaii: Chemical composition and reactions with soils and plants. Water Air Soil Poll 72: 265-283. http://dx.doi.org/10.1007/BF01257129

Imran MA, Sajid ZA, Chaudhry MN, 2015. Arsenic (As) toxicity to germination and vegetative growth of sunflower (Helianthus annuus L.). Pol J Environ Stud 24 (5): 1993-2002. http://dx.doi.org/10.15244/pjoes/39553

Kalra YP, Maynard DG, 1991. Methods for forest soil and plant analysis. Information Report NOR-X-319. Forestry Canada, Northwest Region, Northern Forestry Center.

Kashem MA, Singh BR, Kondo T, Imamul Huq SM, Kawai S, 2007. Comparison of extractability of Cd, Cu, Pb and Zn with sequential extraction in contaminated and non-contaminated soils. Int J Environ Sci Tech 4: 169-176. http://dx.doi.org/10.1007/BF03326270

Khoudi H, Maatar Y, Brini F, Fourati A, Ammar N, Masmoudi K, 2013. Phytoremediation potential of Arabidopsis thaliana, expressing ectopically a vacuolar proton pump, for the industrial waste phosphogypsum. Environ Sci Pollut Res 20: 270-280. http://dx.doi.org/10.1007/s11356-012-1143-2

Leita L, De Nobili M, Mondini C, Muhlbachoa G, Marchiol L, Bragato G, Contin M, 1999. Influence of inorganic and organic fertilization on soil microbial biomass, metabolic quotient and heavy metal bioavailability. Biol Fertil Soil 28: 371-376. http://dx.doi.org/10.1007/s003740050506

Li W, Khan MA, Yamaguchi S, Kamiya Y, 2005. Effects of heavy metals on seed germination and early seedling growth of Arabidopsis thaliana. Plant Growth Reg 46: 45-50. http://dx.doi.org/10.1007/s10725-005-6324-2

Li MS, Luo YP, Su ZY, 2007.Heavy metal concentrations in soils and plant accumulation in a restored manganese mineland in Guangxi, South China. Environ Pollut 147: 168-175. http://dx.doi.org/10.1016/j.envpol.2006.08.006

Li F, Zeng XY, Wu CH, Duan ZP, Wen YM, Huang GR, Long XL, Li MJ, Li MJ, Xu JY, 2013. Ecological risks assessment and pollution source identification of trace elements in contaminated sediments from the Pearl River Delta, China. Biol Trace Elem Res 155: 301-313. http://dx.doi.org/10.1007/s12011-013-9789-2

Lin RZ, Wang XR, Luo Y, Du WC, Guo HY, Yin DQ, 2007.Effects of soil cadmium on growth, oxidative stress and antioxidant system in wheat seedlings (Triticum aestivum L.). Chemosphere 69 (1): 89-98. http://dx.doi.org/10.1016/j.chemosphere.2007.04.041

Logan TJ, Lindsay BJ, Goins LE, Ryan JA, 1997. Field assessment of sludge metal bioavailability to crops: sludge rate response. J Environ Qual 26: 534-550. http://dx.doi.org/10.2134/jeq1997.00472425002600020027x

Luković J, MerkulovLj, Pajević S, Zorić L, Nikolić N, Borišev M, Karanović D, 2012. Quantitative assessment of effects of cadmium on the histological structure of poplar and willow leaves. Water Air Soil Pollut 223: 2979-2993. http://dx.doi.org/10.1007/s11270-012-1081-0

Lux A, Vaculík M, Martinka M, Lišková D, Kulkarni MG, Wendy AS, Van Staden J, 2011. Cadmium induces hypodermal periderm formation in the roots of the monocotyledonous medical plant Merwilla plumbea. Ann Bot 107: 285-292. http://dx.doi.org/10.1093/aob/mcq240

Mata-Gonzalez R, Sosebee RE, Wan C, 2002. Physiological impacts of biosolids application in desert grasses. Environ Exp Bot 48: 139-148. http://dx.doi.org/10.1016/S0098-8472(02)00019-9

McGrath SP, 1987. Long-term studies of metal transfers following application of sewage sludge. In: Pollutant transport and fate in ecosystems; Coughtrey PJ, Martin JH, Unsworth MH (eds). pp: 301-317. Blackwell Scientific, Oxford.

McGrath SP, Cunliffe CH, 1985. A simplified method for the extraction of the metals Fe, Zn, Cu, Ni, Pb, Cr, Co and Mn from soils and sewage sludges. J Sci Food Agr 36: 794-798. http://dx.doi.org/10.1002/jsfa.2740360906

Mishra RN, Behera PK, 1991.The effect of paper industry effluent on growth pigment, carbohydrate, and protein of rice seedlings. Environ Pollut 72: 159-168. http://dx.doi.org/10.1016/0269-7491(91)90065-5

Morera MT, Echeverria J, Garrido J, 2002. Bioavailability of heavy metals in soils amended with sewage sludge. Can J Soil Sci 82: 433-438. http://dx.doi.org/10.4141/S01-072

Nayak AK, Raja R, Rao KS, Shukla AK, Mohanty S, Shahid M, Tripathi R, Panda BB, Bhattacharyya P, Kumar A, et al., 2015. Effect of fly ash application on soil microbial response and heavy metal accumulation in soil and rice plant. Ecotoxicol Environ Saf 114: 257-262. http://dx.doi.org/10.1016/j.ecoenv.2014.03.033

NT, 2002. NT 106.20, Matières fertilisantes - Boues des ouvrages de traitement des eaux usées urbaines. Normes Tunisiens Enregistrée, 12 pp.

Oleszczuk P, 2006. Persistence of polycyclic aromatic hydrocarbons (PAHs) in sewage sludge-amended soil. Chemosphere 65: 1616-1626. http://dx.doi.org/10.1016/j.chemosphere.2006.03.007

Ostos JC, Lopez-Garrido R, Murillo JM, Lopez R, 2008. Substitution of peat for municipal solid waste and sewage sludge-based composts in nursery growing media: Effects on growth and nutrition of the native shrub Pistacia lentiscus L. Bioresour Technol 99: 1793-1800. http://dx.doi.org/10.1016/j.biortech.2007.03.033

Parkpain P, Sreesai S, Delaune RD, 2000. Bioavailability of heavy metals in sewage sludge-amended Thai soils. Water Air Soil Pollut 122: 163-182. http://dx.doi.org/10.1023/A:1005247427037

Paschke MW, Perry LG, Redente EF, 2006. Zinc toxicity thresholds for reclamation forb species. Water Air Soil Pollut 170: 317-330. http://dx.doi.org/10.1007/s11270-006-3139-3

Richards BK, Steenhuis TS, Peverly JH, McBride MB, 2000. Effect of sludge-processing mode, soil texture and soil pH on metal mobility in undisturbed soil columns under accelerated loading. Environ Pollut 109: 327-346. http://dx.doi.org/10.1016/S0269-7491(99)00249-3

Romero-Puertas MC, Palma JM, Gómez M, del Río LA, Sandalio LM, 2002. Cadmium causes the oxidative modification of proteins in pea plants. Plant Cell Environ 25: 677-686. http://dx.doi.org/10.1046/j.1365-3040.2002.00850.x

Rowell DM, Prescott CE, Preston CM, 2001. Decomposition and nitrogen mineralization from biosolids and other organic materials: relationship with initial chemistry. J Environ Qual 30: 1401-1410. http://dx.doi.org/10.2134/jeq2001.3041401x

Rrong W, Aiping T, Ashraf MA, 2015. The effects of applying sewage sludge into Jiangxi red soil on the growth of vegetables and the migration and enrichment of Cu and Zn. Saudi J Biol Sci 23 (5): 660-666. http://dx.doi.org/10.1016/j.sjbs.2015.10.028

Sandalio L, Dalurzo H, Gomes M, Romero-Puertas M, Del Rio L, 2001. Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52: 2115-2126.

Santos JA, Nunes LAPL, Melo WJ, Araujo ASF, 2011. Tannery sludge compost amendment rateson soil microbial biomass in two different soils. Eur J Soil Biol 47: 146-151. http://dx.doi.org/10.1016/j.ejsobi.2011.01.002

Scandalios JG, 2005. Oxidative stress: Molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res 38: 995-1014. http://dx.doi.org/10.1590/S0100-879X2005000700003

Singh RP, Agrawal M, 2007. Effects of sewage sludge amendment on heavy metal accumulation and consequent responses of Beta vulgaris plants. Chemosphere 67: 2229-2240. http://dx.doi.org/10.1016/j.chemosphere.2006.12.019

Singh RP, Agrawal M, 2008. Potential benefits and risks of land application of sewage sludge. Waste Manage 28: 347-358. http://dx.doi.org/10.1016/j.wasman.2006.12.010

Singh RP, Agrawal M, 2010. Biochemical and physiological responses of rice (Oryza sativa L.) grown on different sewage sludge amendments rates. Bull Environ Contam Toxicol 84: 606-612. http://dx.doi.org/10.1007/s00128-010-0007-z

Singh RP, Singh P, Hakimi Ibrahim M, Hashim R, 2011. Land application of sewage sludge: physicochemical and microbial response. Rev Environ Contam Toxicol 214: 41-61. http://dx.doi.org/10.1007/978-1-4614-0668-6_3

Sinha S, Saxena R, Singh S, 2005. Chromium induced lipid peroxidation in the plants of Pistia stratiotes L.: role of antioxidants and antioxidant enzymes. Chemosphere 58 (5): 595-604. http://dx.doi.org/10.1016/j.chemosphere.2004.08.071

Sipos G, Solti A, Czech V, Vashegyi I, Tóth B, Cseh E, Fodor F, 2013. Heavy metal accumulation and tolerance of energy grass (Elymus elongatus subsp. ponticus cv. Szarvasi-1) grown in hydroponic culture. Plant Physiol Bioch: 96-103.

Sun Z, Wang L, Chen M, Wang L, Liang C, Zhou Q, Huang X, 2012. Interactive effects of cadmium and acid rain on photosynthetic light reaction in soybean seedlings. Ecotoxicol Environ Saf 79: 62-68. http://dx.doi.org/10.1016/j.ecoenv.2011.12.004

Tauqeer HM, Ali S, Rizwan M, Ali Q, Saeed R, Iftikhar U, Ahmad R, Farid M, Abbasi GH, 2016. Phytoremediation of heavy metals by Alternanthera bettzickiana: Growth and physiological response. Ecotoxicol Environ Saf 126: 138-146. http://dx.doi.org/10.1016/j.ecoenv.2015.12.031

Taws N, 2003. Woodland remnants and dry land salinity. Final Report for NSW National Parks and Wild life Service. Greening Australia ACT & SE NSW, Canberra.

Tripathi BN, Gaur JP, 2004. Relationship between copper- and zinc induced oxidative stress and proline accumulation in Scenedesmus sp. Planta 219: 397-404. http://dx.doi.org/10.1007/s00425-004-1237-2

Türkan I, Demiral T, 2009. Recent developments in understanding salinity tolerance. Environ Exp Bot 67: 2-9. http://dx.doi.org/10.1016/j.envexpbot.2009.05.008

Xu D, Chen Z, Sun K, Yan D, Kang M, Zhao Y, 2013. Effect of cadmium on the physiological parameters and the subcellular cadmium localization in the potato (Solanum tuberosum L.). Ecotoxicol Environ Saf 97: 147-153. http://dx.doi.org/10.1016/j.ecoenv.2013.07.021

Yadav S, Irfan M, Ahmad A, Hayat S, 2011. Causes of salinity and plant manifestations to salt stress: A review. J Environ Biol 32: 667-685.

Yilmaz DD, Temizgül A, 2012. Assessment of arsenic and selenium concentration with chlorophyll contents of sugar beet (Beta vulgaris var.Saccharifera) and wheat (Triticum aestivum) exposed to municipal sewage sludge doses. Water Air Soil Pollut 223 (6): 3057-3066. http://dx.doi.org/10.1007/s11270-012-1088-6

Yoon J, Cao X, Zhou Q, Ma LQ, 2006. Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Environ 368: 456-464. http://dx.doi.org/10.1016/j.scitotenv.2006.01.016

Zhang JX, Kirham MB, 1994. Drought stress-induced changes in activities of superoxide dismutase, catalase, and peroxidase in wheat species. Plant Cell Physiol 35: 785-791.

Zouari M, BenAhmed CH, Elloumi N, Bellassoued K, Delmail D, Labrousse P, Ben Abdallah F, Ben Rouina B, 2016. Impact of proline application on cadmium accumulation, mineral nutrition and enzymatic antioxidant defense system of Olea europaea L. cv Chemlali exposed to cadmium stress. Ecotox Environ Safe 128: 195-205. http://dx.doi.org/10.1016/j.ecoenv.2016.02.024

Published
2017-01-20
How to Cite
Elloumi, N., Belhaj, D., Jerbi, B., Zouari, M., & Kallel, M. (2017). Effects of sewage sludge on bio-accumulation of heavy metals in tomato seedlings. Spanish Journal of Agricultural Research, 14(4), e0807. https://doi.org/10.5424/sjar/2016144-9210
Section
Plant physiology