Skip to main content
SpringerLink
Log in

Earthworm Eisenia andrei modulates oxidative stress in bean plants Vicia faba irrigated with treated wastewater

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

With respect to reducing the pressure on freshwater resources, treated wastewater (TWW) irrigation represents a sustainable alternative in agriculture. Due to their low quality and variable composition, TWW could entail harmful consequences for living organisms in terrestrial ecosystems. This study aims to evaluate how earthworm (Eisenia andrei) can modulate oxidative stress in bean plants (Vicia faba) that are irrigated over a course of 60 days with two doses of TWW (50 and 100%) in addition to a control condition (0%) irrigated with distilled water. This is achieved by measuring glutathione-S-transferase (GST) activity and malondialdehyde accumulation (MDA) in plants. Furthermore, catalase (CAT), GST, MDA, and acetylcholinesterase (AChE) activities of the earthworms are also assessed. Our results show that growth and physiological parameters are modified when applying TWW irrigation. Moreover, oxidative stress apprehended by GST activity and MDA accumulation is exacerbated in V. faba plants after exposure to increased TWW doses. Similarly, TWW irrigation enhances oxidative stress parameters in earthworms with a crucial decrease in AChE activity. In addition, the presence of earthworms increases growth and physiological parameters; it also results in a significant reduction in GST activity and MDA rate in V. faba plants. Our results provide new insights into the impact of TWW irrigation on soil organisms and the importance of earthworms in the reduction of oxidative stress in plants.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • AbdElgawad H, Zinta G, Hegab MM et al. (2016) High salinity induces different oxidative stress and antioxidant responses in maize seedlings organs. Front Plant Sci 7:1–11. https://doi.org/10.3389/fpls.2016.00276

    Article  Google Scholar 

  • Adriano DC (2001) Biogeochemistry, bioavailability and risks of metals. Trace elements in the terrestrial environment, 2nd edn. Springer-Verlag, New York, NY

    Google Scholar 

  • Ahmad P, Alam P, Balawi TH et al. (2020) Sodium nitroprusside (SNP) improves tolerance to arsenic (As) toxicity in Vicia faba through the modifications of biochemical attributes, antioxidants, ascorbate-glutathione cycle and glyoxalase cycle. Chemosphere 244:125480. https://doi.org/10.1016/j.chemosphere.2019.125480

    Article  CAS  Google Scholar 

  • Aliyat FZ, Messaoud BBen, Nassiri L et al. (2018) Assess biol nitrogen fixation soybean sown differ types moroccan soils 12:704–707

    Google Scholar 

  • APIA (Agence de la Promotion des investissements Agricoles) (2015) Study of investment incentives and development of vegetable production under greenhouses. Final synthesis report

  • Arora A, Sairam RK, Srivastava GC (2002) Oxidative stress and antioxidative system in plants. Current science 1227–1238

  • Azeem F, Bilal A, Rana MA et al. (2019) Drought affects aquaporins gene expression in important pulse legume chickpea (Cicer arietinum L.). Pak J Bot 51:81–88. https://doi.org/10.30848/PJB2019

    Article  CAS  Google Scholar 

  • Bedbabis S, Trigui D, Ben Ahmed C et al. (2015) Long-terms effects of irrigation with treated municipal wastewater on soil, yield and olive oil quality. Agric Water Manag 160:14–21. https://doi.org/10.1016/j.agwat.2015.06.023

    Article  Google Scholar 

  • Ben Youssef N, Nouairi I, Temime SB, Taamalli W, Zarrouk M, Ghorbal MH, Daoud DBM (2005) Effets du cadmium sur le métabolisme des lipides de plantules de colza (Brassica napus L.). Comptes Rendus Biologies 328(8):745–757

  • Blouin M, Barrere J, Meyer N et al. (2019) Vermicompost significantly affects plant growth. A meta-analysis. Agron Sustain Dev 39. https://doi.org/10.1007/s13593-019-0579-x

  • Blouin M (2018) Chemical communication: An evidence for co-evolution between plants and soil organisms. App Soil Ecol 123:409–415

  • Bouché MB (1977) Strategies lombriciennes. Ecological Bulletins 122–132

  • Boughattas I, Hattab S, Alphonse V et al. (2019) Use of earthworms Eisenia andrei on the bioremediation of contaminated area in north of Tunisia and microbial soil enzymes as bioindicator of change on heavy metals speciation. J Soils Sediment 19:296–309. https://doi.org/10.1007/s11368-018-2038-8

    Article  CAS  Google Scholar 

  • Boughattas I, Hattab S, Boussetta H, Banni M, Navarro E (2017) Impact of heavy metal contamination on oxidative stress of Eisenia andrei and bacterial community structure in Tunisian mine soil. Environ Sci and Pollut Res 24(22):18083–18095. https://doi.org/10.1007/s11356-017-9449-8

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analy Biochem 72(1–2):248–254

  • Canesi L, Procházková P (2014) The invertebrate immune system as a model for investigating the environmental impact of nanoparticles. In Nanoparticles and the immune system (pp. 91–112). Academic Press

  • Cavusoglu K, Yapar K, Kinalioglu K, Turkmen Z, Cavusoglu K, Yalcin E (2010) Protective role of Ginkgo biloba on petroleum wastewater-induced toxicity in Vicia faba L. (Fabaceae) root tip cells. J Environ Bio 31(3):319

  • Chebil A, Souissi A, Frija A, Stambouli T (2019) Estimation of the economic loss due to irrigation water use inefficiency in Tunisia. Environ Sci Poll Res 26(11):11261–11268

  • Claiborne A (1985) Catalase activity. In: Greenwald RA (Ed.), Handbook of Methods for Oxygene Radical Research. CRC Press, BocaRaton, FL, pp. 283–284

  • Collange B, Wheelock CE, Rault M et al. (2010) Inhibition, recovery and oxime-induced reactivation of muscle esterases following chlorpyrifos exposure in the earthworm Lumbricus terrestris. Environ Pollut 158:2266–2272. https://doi.org/10.1016/j.envpol.2010.02.009

    Article  CAS  Google Scholar 

  • Dahmouni M, Hoermann G, Jouzdan O, Hachicha M (2019) Spatio-temporal variability of hydrochemical parameters and heavy metals in shallow groundwater of the area of Cebala–Borj–Touil, irrigated with treated wastewater (Tunisia). Environ Earth Sci 78:0. https://doi.org/10.1007/s12665-019-8056-z

    Article  CAS  Google Scholar 

  • Dai J, Becquer T, Rouiller JH et al. (2004) Heavy metal accumulation by two earthworm species and its relationship to total and DTPA-extractable metals in soils. Soil Biol Biochem 36:91–98. https://doi.org/10.1016/j.soilbio.2003.09.001

    Article  CAS  Google Scholar 

  • Das P, Barua S, Sarkar S et al. (2018) Mechanism of toxicity and transformation of silver nanoparticles: inclusive assessment in earthworm-microbe-soil-plant system. Geoderma 314:73–84. https://doi.org/10.1016/j.geoderma.2017.11.008

    Article  CAS  Google Scholar 

  • Das S, Bora J, Goswami L et al. (2015) Vermiremediation of water treatment plant sludge employing Metaphire posthuma: a soil quality and metal solubility prediction approach. Ecol Eng 81:200–206. https://doi.org/10.1016/j.ecoleng.2015.04.069

    Article  Google Scholar 

  • Dewez D, Didur O, Vincent-Héroux J, Popovic R (2008) Validation of photosynthetic-fluorescence parameters as biomarkers for isoproturon toxic effect on alga Scenedesmus obliquus. Environ Pollut 151:93–100. https://doi.org/10.1016/j.envpol.2007.03.002

    Article  CAS  Google Scholar 

  • Doan TT, Ngo PT, Rumpel C, Van Nguyen B, Jouquet P (2013) Interactions between compost, vermicompost and earthworms influence plant growth and yield: A one-year greenhouse experiment. Sci Hortic 160:148–154

  • Ečimović S, Grgić M, Bošnjaković R, Velki M (2019) Biomarker responses in earthworm coelomocyte extract—noninvasively collected sample for pesticide effect assessment. Chemosphere 234:837–844. https://doi.org/10.1016/j.chemosphere.2019.06.141

    Article  CAS  Google Scholar 

  • Ellman GL, Courtney KD, Andres Jr V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7(2):88–95

  • FAO, IFAD, UNICEF, WFP and WHO (2018) The state of food security and nutrition in the world, 2018. Building climate resilience for food security and nutritionFAO, Rome

    Google Scholar 

  • Farhadkhani M, Nikaeen M, Yadegarfar G et al. (2018) Effects of irrigation with secondary treated wastewater on physicochemical and microbial properties of soil and produce safety in a semi-arid area. Water Res 144:356–364. https://doi.org/10.1016/j.watres.2018.07.047

    Article  CAS  Google Scholar 

  • Flecha GBS, Repetto M, Evelson P, Boveris A (1991) Inhibition of microsomal lipid peroxidation by α-tocopherol and α-tocopherol acetate. Xenobiotica 21(8):1013–1022

  • Fonte SJ, Botero C, Quintero DC et al. (2019) Earthworms regulate plant productivity and the efficacy of soil fertility amendments in acid soils of the Colombian Llanos. Soil Biol Biochem 129:136–143. https://doi.org/10.1016/j.soilbio.2018.11.016

    Article  CAS  Google Scholar 

  • Frazão J, de Goede RGM, Capowiez Y, Pulleman MM (2019) Soil structure formation and organic matter distribution as affected by earthworm species interactions and crop residue placement. Geoderma 338:453–463. https://doi.org/10.1016/j.geoderma.2018.07.033

    Article  Google Scholar 

  • Frouz J (2018) Earthworms increase plant biomass more in soil with no earthworm legacy than in earthworm mediated soil, and four late successional species in competition. Funct Ecol

  • Gao C, Xu J, Li J, Liu Z (2016) Determination of metallothionein, malondialdehyde, and antioxidant enzymes in earthworms (Eisenia fetida) following exposure to chromium. Anal Lett 49:1748–1757. https://doi.org/10.1080/00032719.2015.1120738

    Article  CAS  Google Scholar 

  • Ghori NH, Ghori T, Hayat MQ et al. (2019) Heavy metal stress and responses in plants. Int J Environ Sci Technol 16:1807–1828. https://doi.org/10.1007/s13762-019-02215-8

    Article  CAS  Google Scholar 

  • Goswami L, Pratihar S, Dasgupta S et al. (2016) Exploring metal detoxification and accumulation potential during vermicomposting of tea factory coal ash: sequential extraction and fluorescence probe analysis. Sci Rep 6:1–13. https://doi.org/10.1038/srep30402

    Article  CAS  Google Scholar 

  • Goswami L, Sarkar S, Mukherjee S et al. (2014) Vermicomposting of tea factory coal ash: metal accumulation and metallothionein response in Eisenia fetida (Savigny) and Lampito mauritii (Kinberg). Bioresour Technol 166:96–102. https://doi.org/10.1016/j.biortech.2014.05.032

    Article  CAS  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases the first enzymatic step in mercapturic acid formation. J Biol Chem 249(22):7130–7139

  • Halušková LU, Valentovičová K, Huttová J, Mistrík I, Tamás L (2009) Effect of abiotic stresses on glutathione peroxidase and glutathione S-transferase activity in barley root tips. Plant Physiol and Biochem 47(11–12):1069–1074

  • Hobbelen PHF, Koolhaas JE, van Gestel CAM (2006) Bioaccumulation of heavy metals in the earthworms Lumbricus rubellus and Aporrectodea caliginosa in relation to total and available metal concentrations in field soils. Environ Pollut 144:639–646. https://doi.org/10.1016/j.envpol.2006.01.019

    Article  CAS  Google Scholar 

  • Hossain MA, Hasanuzzaman M, Fujita M (2010) Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer tolerance to cadmium stress. Physiol Mol Biol Plants 16:259–272. https://doi.org/10.1007/s12298-010-0028-4

    Article  CAS  Google Scholar 

  • Ibekwe AM, Gonzalez-Rubio A, Suarez DL (2018) Impact of treated wastewater for irrigation on soil microbial communities. Sci Tot Environ 622:1603–1610

  • Iqbal M (2016) Vicia faba bioassay for environmental toxicity monitoring: a review. Chemosphere 144:785–802. https://doi.org/10.1016/j.chemosphere.2015.09.048

    Article  CAS  Google Scholar 

  • Kallel S, Abid M, Jarraya A et al. (2012) Cinétique et intérêt diagnostique et pronostique de la procalcitonine aprés chirurgie cardiaque. Ann Biol Clin 70:567–580. https://doi.org/10.1684/abc.2012.0745

    Article  CAS  Google Scholar 

  • Kaur H, Sharma S, Vijaya P (2019a) Toxicological effect of Parthenium hysterophorus and milk processing industry sludge on earthworms, Eisenia fetida. Environ Sci Pollut Res https://doi.org/10.1007/s11356-019-05222-x

  • Kaur P, Bali S, Sharma A et al. (2019b) Cd induced generation of free radical species in Brassica juncea is regulated by supplementation of earthworms in the drilosphere. Sci Total Environ 655:663–675. https://doi.org/10.1016/j.scitotenv.2018.11.096

  • Khan S, Cao Q, Zheng YM, Huang YZ, Zhu YG (2008) Health risks of heavy metals in contaminated soils and food crops irrigated with wastewater in Beijing, China. Environ Poll 152(3):686–692

  • Klay S, Charef A, Ayed L et al. (2010) Effect of irrigation with treated wastewater on geochemical properties (saltiness, C, N and heavy metals) of isohumic soils (Zaouit Sousse perimeter, Oriental Tunisia). Desalination 253:180–187. https://doi.org/10.1016/j.desal.2009.10.019

    Article  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680–685

  • Lafaurie M (1998) Biomarqueurs: les pollutions sous surveillance. Biofutur 179:79–81

    Article  Google Scholar 

  • Lemtiri A, Liénard A, Alabi T et al. (2016) Earthworms Eisenia fetida affect the uptake of heavy metals by plants Vicia faba and Zea mays in metal-contaminated soils. Appl Soil Ecol 104:67–78. https://doi.org/10.1016/j.apsoil.2015.11.021

    Article  Google Scholar 

  • Li Y, Wang S, Lu M et al. (2019) Rhizosphere interactions between earthworms and arbuscular mycorrhizal fungi increase nutrient availability and plant growth in the desertification soils. Soil Tillage Res 186:146–151. https://doi.org/10.1016/j.still.2018.10.016

    Article  Google Scholar 

  • Lin Z, Zhen Z, Wu Z, Yang J et al. (2016) The impact on the soil microbial community and enzyme activity of two earthworm species during the bioremediation of pentachlorophenol-contaminated soils. J Hazard Mater 301:35–45. https://doi.org/10.1016/j.jhazmat.2015.08.034

    Article  CAS  Google Scholar 

  • Liu S, Zhou Q, Wang Y (2011) Ecotoxicological responses of the earthworm Eisenia fetida exposed to soil contaminated with HHCB. Chemosphere 83(8):1080–1086

  • Livingstone DR, Martinez PG, Michel X, Narbonne JF, O’hara S, Ribera D, Winston GW (1990) Oxyradical production as a pollution-mediated mechanism of toxicity in the common mussel, Mytilus edulis L., and other molluscs. Func Ecol 415–424

  • Lu G, Tan W, Li G, et al. (2019) Effects of carbendazim on catalase activity and related mechanism. Environ Sci Pollut Res 1–6. https://doi.org/10.1007/s11356-019-06125-7

  • Martínez Morcillo S, Yela JL, Capowiez Y et al. (2013) Avoidance behaviour response and esterase inhibition in the earthworm, Lumbricus terrestris, after exposure to chlorpyrifos. Ecotoxicology 22:597–607. https://doi.org/10.1007/s10646-013-1051-3

    Article  CAS  Google Scholar 

  • Mkhinini M, Boughattas I, Alphonse V, Livet A, Bousserrhine N, Banni M (2019a) Effect of treated wastewater irrigation in East Central region of Tunisia (Monastir governorate) on the biochemical and transcriptomic response of earthworms Eisenia andrei. Sci Tot Environ 647:1245–1255

  • Mkhinini M, Boughattas I, Bousserhine N, Banni M (2019b) Biochemical and transcriptomic response of earthworms Eisenia andrei exposed to soils irrigated with treated wastewater. Environ Sci Poll Res 26(3):2851–2863

  • Molaei S, Shirani H, Hamidpour M et al. (2016) Effect of vermicompost, pistachio kernel and shrimp shell on some growth parameters and availability of Cd, Pb and Zn in Corn in a Polluted Soil. J Water Soil Sci 19:113–124. https://doi.org/10.18869/acadpub.jstnar.19.74.10

    Article  Google Scholar 

  • Mroczek-Zdyrska M, Wójcik M (2012) The influence of selenium on root growth and oxidative stress induced by lead in Vicia faba L. minor plants. Biol Trace Elem Res 147:320–328. https://doi.org/10.1007/s12011-011-9292-6

    Article  CAS  Google Scholar 

  • Nam TH, Jeon HJ, Mo Hho et al. (2015) Determination of biomarkers for polycyclic aromatic hydrocarbons (PAHs) toxicity to earthworm (Eisenia fetida). Environ Geochem Health 37:943–951. https://doi.org/10.1007/s10653-015-9706-z

    Article  CAS  Google Scholar 

  • Nannoni F, Protano G, Riccobono F (2011) Uptake and bioaccumulation of heavy elements by two earthworm species from a smelter contaminated area in northern Kosovo. Soil Biol Biochem 43:2359–2367. https://doi.org/10.1016/j.soilbio.2011.08.002

    Article  CAS  Google Scholar 

  • OECD (2004) Organization for Economic Cooperation and Development: Earthworm reproduction test. Guideline for Testing Chemicals no. 222. Paris, France

  • OECD Organization for Economic Co-operation and Development (2004a) Guideline for testing chemicals no. 222. OECD, Paris

  • Ortega-Villasante C, Rellán-Alvarez R, Del Campo FF, Carpena-Ruiz RO, Hernández LE (2005) Cellular damage induced by cadmium and mercury in Medicago sativa. J Exp Bot 56(418):2239–2251

  • Pandolfini T, Gabbrielli R, Comparini C (1992) Nickel toxicity and peroxidase activity in seedlings of Triticum aestivum L. Plant, Cell Environ 15(6):719–725

  • Panzarino O, Hyršl P, Dobeš P et al. (2016) Rank-based biomarker index to assess cadmium ecotoxicity on the earthworm Eisenia andrei. Chemosphere 145:480–486. https://doi.org/10.1016/j.chemosphere.2015.11.077

    Article  CAS  Google Scholar 

  • Pelosi C, Barot S, Capowiez Y et al. (2014) Pesticides and earthworms. A review. Agron Sustain Dev 34:199–228. https://doi.org/10.1007/s13593-013-0151-z

    Article  CAS  Google Scholar 

  • Peterson TJ, Western AW (2018) Statistical interpolation of groundwater hydrographs. Water Resour Res 54:4663–4680. https://doi.org/10.1029/2017WR021838

    Article  Google Scholar 

  • Puga-Freitas R, Abbad S, Gigon A et al. (2012b) Control of cultivable IAA-producing bacteria by the plant Arabidopsis thaliana and the earthworm Aporrectodea caliginosa. Appl Environ Soil Sci 2012:1–5. https://doi.org/10.1155/2012/307415

    Article  Google Scholar 

  • Puga-Freitas R, Barot S, Taconnat L et al. (2012a) Signal molecules mediate the impact of the earthworm Aporrectodea caliginosa on growth, development and defence of the plant Arabidopsis thaliana. PLoS ONE 7. https://doi.org/10.1371/journal.pone.0049504

  • Ren F, Sun N, Xu M et al. (2019) Changes in soil microbial biomass with manure application in cropping systems: a meta-analysis. Soil Tillage Res 194:104291. https://doi.org/10.1016/j.still.2019.06.008

    Article  Google Scholar 

  • Rieder SR, Brunner I, Horvat M et al. (2011) Accumulation of mercury and methylmercury by mushrooms and earthworms from forest soils. Environ Pollut 159:2861–2869. https://doi.org/10.1016/j.envpol.2011.04.040

    Article  CAS  Google Scholar 

  • Rodriguez-Campos J, Perales-Garcia A, Hernandez-Carballo J, Martinez-Rabelo F, Hernández-Castellanos B, Barois I, Contreras-Ramos SM (2019) Bioremediation of soil contaminated by hydrocarbons with the combination of three technologies: bioaugmentation, phytoremediation, and vermiremediation. J Soils and Sediments 19(4):1981–1994

  • Rousseau L, Fonte SJ, Téllez O et al. (2013) Soil macrofauna as indicators of soil quality and land use impacts in smallholder agroecosystems of western Nicaragua. Ecol Indic 27:71–82. https://doi.org/10.1016/j.ecolind.2012.11.020

    Article  CAS  Google Scholar 

  • Ruiz E, Rodríguez L, Alonso-Azcárate J (2009) Effects of earthworms on metal uptake of heavy metals from polluted mine soils by different crop plants. Chemosphere 75:1035–1041. https://doi.org/10.1016/j.chemosphere.2009.01.042

    Article  CAS  Google Scholar 

  • Saint-Denis M, Labrot F, Narbonne JF, Ribera D (1998) Glutathione, glutathione-related enzymes, and catalase activities in the earthworm Eisenia fetida andrei. Arch Environ Contam Toxicol 35:602–614. https://doi.org/10.1007/s002449900422

    Article  CAS  Google Scholar 

  • Sakalli S, Giang PT, Burkina V, Zamaratskaia G, Rasmussen MK, Bakal T, Turek J (2018) The effects of sewage treatment plant effluents on hepatic and intestinal biomarkers in common carp (Cyprinus carpio). Sci Tot Environ 635:1160–1169

  • Sanchez-Hernandez JC, Ríos JM, Attademo AM (2018) Response of digestive enzymes and esterases of ecotoxicological concern in earthworms exposed to chlorpyrifos-treated soils. Ecotoxicology 27:890–899. https://doi.org/10.1007/s10646-018-1914-8

    Article  CAS  Google Scholar 

  • Schacht K, Chen Y, Tarchitzky J, Marschner, B (2016) The use of treated wastewater for irrigation as a component of integrated water resources management: reducing environmental implications on soil and groundwater by evaluating site-specific soil sensitivities. In Integrated water resources management: concept, research and implementation (pp. 459–470). Springer, Cham

  • Scott-Fordsmand JJ, Weeks JM (2000) Biomarkers in earthworms. Rev Environ Contam Toxicol 165:117–159

    CAS  Google Scholar 

  • Sdiri W, Mansour HBen, Albergamo A, Di Bella G (2020) Effectiveness of dairy treated wastewater and different irrigation systems on the growth, biomass and fruiting of a Tunisian olive orchard (Olea europaea L., cv Chemlali). Nat Prod Res 34:183–186. https://doi.org/10.1080/14786419.2019.1607859

    Article  CAS  Google Scholar 

  • Shakir E, Zahraw Z, Al-Obaidy AHMJ (2017) Environmental and health risks associated with reuse of wastewater for irrigation. Egypt J Pet 26:95–102. https://doi.org/10.1016/j.ejpe.2016.01.003

    Article  Google Scholar 

  • Singh S, Tiwari RK, Pandey RS (2019) Acute toxicity evaluation of triazophos, deltamethrin and their combination on earthworm, Eudrilus eugeniae and its impact on AChE activity. Chem Ecol 35:563–575. https://doi.org/10.1080/02757540.2019.1600679

    Article  CAS  Google Scholar 

  • Smith JH, Benitez A (1955) Chlorophylls: analysis in plant materials. In Modern Methods of Plant Analysis/Moderne Methoden der Pflanzenanalyse (pp. 142–196). Springer, erlin, Heidelberg

  • Sobrino-Plata J, Herrero J, Carrasco-Gil S, Pérez-Sanz A, Lobo C, Escobar C, Hernández LE (2013) Specific stress responses to cadmium, arsenic and mercury appear in the metallophyte Silene vulgaris when grown hydroponically. RSC advances 3(14):4736–4744

  • Song P, Gao J, Li X et al. (2019) Phthalate induced oxidative stress and DNA damage in earthworms (Eisenia fetida). Environ Int 129:10–17. https://doi.org/10.1016/j.envint.2019.04.074

    Article  CAS  Google Scholar 

  • Souguir D, Ferjani E, Ledoigt G, Goupil P (2011) Sequential effects of cadmium on genotoxicity and lipoperoxidation in Vicia faba roots. Ecotoxicology 20:329–336. https://doi.org/10.1007/s10646-010-0582-0

    Article  CAS  Google Scholar 

  • Souguir D, Hörmann G, Hachicha M (2019) Effets génotoxiques de l’irrigation à long-terme par des eaux usées traitées: cas du périmètre Cebala-Borj Touil. J Appl Biosci 139:14191. https://doi.org/10.4314/jab.v139i1.6

    Article  Google Scholar 

  • Sruthi SN, Ramasamy EV (2018) Enrichment of soil organic carbon by native earthworms in a patch of tropical soil, Kerala, India: first report. Sci Rep 8:1–7. https://doi.org/10.1038/s41598-018-24086-8

    Article  CAS  Google Scholar 

  • Taïbi K, Taïbi F, Ait Abderrahim L et al. (2016) Effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidant defence systems in Phaseolus vulgaris L. South Afr J Bot 105:306–312. https://doi.org/10.1016/j.sajb.2016.03.011

    Article  CAS  Google Scholar 

  • Thioulouse J, Dray S, Dufour AB, Siberchicot A, Jombart T, Pavoine S (2018) Multivariate analysis of ecological data with ade4. New York, Dordrecht, London, Heidelberg: Springer

  • Urbano VR, Mendonça TG, Bastos RG, Souza CF (2017) Effects of treated wastewater irrigation on soil properties and lettuce yield. Agric Water Manag 181:108–115. https://doi.org/10.1016/j.agwat.2016.12.001

    Article  Google Scholar 

  • Van Groenigen JW, Lubbers IM, Vos HMJ et al. (2014) Earthworms increase plant production: a meta-analysis. Sci Rep 4:1–7. https://doi.org/10.1038/srep06365

    Article  CAS  Google Scholar 

  • Varghese SM, Prabha ML (2014) Biochemical characterization of vermiwash and its effect on growth of Capsicum frutescens. Malaya J Biosci 1:86–91

    CAS  Google Scholar 

  • Velki M, Hackenberger BK (2013) Biomarker responses in earthworm Eisenia andrei exposed to pirimiphos-methyl and deltamethrin using different toxicity tests. Chemosphere 90:1216–1226. https://doi.org/10.1016/j.chemosphere.2012.09.051

    Article  CAS  Google Scholar 

  • Ventorino V, Pascale A, Fagnano M et al. (2019) Soil tillage and compost amendment promote bioremediation and biofertility of polluted area. J Clean Prod 239:118087. https://doi.org/10.1016/j.jclepro.2019.118087

    Article  CAS  Google Scholar 

  • Weeks JM (1995) The value of biomarkers for ecological risk assessment: academic toys or legislative tools? Appl Soil Ecol 2:215–216

    Article  Google Scholar 

  • Wei QB, Lei ZR, Nauen R et al. (2015) Abamectin resistance in strains of vegetable leafminer, Liriomyza sativae (Diptera: Agromyzidae) is linked to elevated glutathione S-transferase activity. Insect Sci 22:243–250. https://doi.org/10.1111/1744-7917.12080

    Article  CAS  Google Scholar 

  • Wu CH, Bernard SM, Andersen GL, Chen W (2009) Developing microbe–plant interactions for applications in plant‐growth promotion and disease control, production of useful compounds, remediation and carbon sequestration. Microb Biotechnol 2(4):428–440

  • Yadav KK, Gupta N, Kumar V, Singh JK (2017) Bioremediation of heavy metals from contaminated sites using potential species: a review. Indian J Environ Prot 37:65–84

    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 Cracoviensia Ser Bot 47:157–164

    Google Scholar 

  • Zhang Q, Zhang B, Wang C (2014) Ecotoxicological effects on the earthworm Eisenia fetida following exposure to soil contaminated with imidacloprid. Environ Sci Pollut Res 21:12345–12353. https://doi.org/10.1007/s11356-014-3178-z

    Article  CAS  Google Scholar 

  • Zhang S, Hu F, Li H, Li X (2009) Influence of earthworm mucus and amino acids on tomato seedling growth and cadmium accumulation. Environ Pollut 157:2737–2742. https://doi.org/10.1016/j.envpol.2009.04.027

  • Zhang W, Cao J, Zhang S, Wang C (2016) Effect of earthworms and arbuscular mycorrhizal fungi on the microbial community and maize growth under salt stress. Appl Soil Ecol 107:214–223. https://doi.org/10.1016/j.apsoil.2016.06.005

    Article  Google Scholar 

  • Zhang Y, Shen G, Yu Y, Zhu H (2009) The hormetic effect of cadmium on the activity of antioxidant enzymes in the earthworm Eisenia fetida. Environ Pollut 157:3064–3068. https://doi.org/10.1016/j.envpol.2009.05.039

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by funds from the ‘Ministry of High Education and Scientific Research’. Also, this study was undertaken using facilities in the research unit UR04A6R05 ‘Laboratory of Biochemistry and Environmental Toxicology’ at ISA-CM, Tunisia.

Funding

This research was financially supported by the Ministry of higher education and scientific research of Tunisia and the University of Sousse. Also, this study was undertaken using facilities in the research unit UR04A6R05 ‘Laboratory of Biochemistry and Environmental Toxicology’ at ISA-CM, Tunisia.

Author information

Authors and Affiliations

  1. Laboratory of Biochemistry and Environmental Toxicology, Higher Institute of Agronomy Chott-Meriem, University of Sousse, Sousse, Tunisia

    Marouane Mkhinini, Sondes Helaoui, Iteb Boughattas, Cyrine Amemou & Mohammed Banni

Authors
  1. Marouane Mkhinini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sondes Helaoui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Iteb Boughattas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cyrine Amemou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mohammed Banni
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Iteb Boughattas.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This paper does not contain any studies with human participants or animals performed by any of the authors. All authors have read and approved this version of the article, and due care has been taken to ensure the integrity of the work. Neither the entire paper nor any part of its content has been published or has been accepted elsewhere. And it is not being submitted to any other journal.

Informed consent

This paper does not contain any studies with human participants or animals performed by any of the authors.

Additional information

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

Mkhinini, M., Helaoui, S., Boughattas, I. et al. Earthworm Eisenia andrei modulates oxidative stress in bean plants Vicia faba irrigated with treated wastewater. Ecotoxicology 29, 1003–1016 (2020). https://doi.org/10.1007/s10646-020-02243-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-020-02243-y

Keywords

Search

Navigation