Biochemical and transcriptomic response of earthworms Eisenia andrei exposed to soils irrigated with treated wastewater

Abstract

In order to ensure better use of treated wastewater (TWW), we investigated the effect of three increasing doses of TWW, 10%, 50%, and 100%, on biochemical and transcriptomic statuses of earthworms Eisenia andrei exposed during 7 and 14 days. The effect of TWW on the oxidative status of E. andrei was observed, but this effect was widely dependent on the dilution degree of TWW. Results showed a significant decrease in the catalase (CAT) activity and an increase in the glutathione-S-transferase (GST) activity, and considerable acetylcholinesterase (AChE) inhibition was recorded after 14 days of exposure. Moreover, malondialdehyde (MDA) accumulation was found to be higher in exposed animals compared to control worms. The gene expression level revealed a significant upregulation of target genes (CAT and GST) during experimentation. These data provided new information about the reuse of TWW and its potential toxicity on soil organisms.

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References

  1. Abdoulkader BA, Mohamed B, Nabil M, Alaoui-Sossé B, Eric C, Aleya L (2015) Wastewater use in agriculture in Djibouti: Effectiveness of sand filtration treatments and impact of wastewater irrigation on growth and yield of Panicum maximum. Ecol Eng 84:607–614. https://doi.org/10.1016/j.ecoleng.2015.09.065

    Article  Google Scholar 

  2. Abegunrin TP, Awe GO, Idowu DO, Adejumobi MA (2016) Impact of wastewater irrigation on soil physico-chemical properties, growth and water use pattern of two indigenous vegetables in southwest Nigeria. Catena 139:167–178. https://doi.org/10.1016/j.catena.2015.12.014

    CAS  Article  Google Scholar 

  3. AFNOR NF EN 1988-1. Water quality-determination of biochemical oxygen demand after n days (BODn)

  4. AFNOR NF T 90-101 (1988) Qualité de l’eau. Détérm. Oxyg (DCO), Demande Chim.

    Google Scholar 

  5. Al-Lahham O, El Assi NM, Fayyad M (2003) Impact of treated wastewater irrigation on quality attributes and contamination of tomato fruit. Agric Water Manag 61:51–62. https://doi.org/10.1016/S0378-3774(02)00173-7

    Article  Google Scholar 

  6. Angelakis AN, Durham B (2008) Water recycling and reuse in EUREAU countries: Trends and challenges. Desalination 218(1-3):3–12. https://doi.org/10.1016/j.desal.2006.07.015

    CAS  Article  Google Scholar 

  7. Antunes SC, Castro BB, Nunes B, Pereira R, Gonçalves F (2008) In situ bioassay with Eisenia andrei to assess soil toxicity in an abandoned uranium mine. Ecotoxicol Environ Saf 71:620–631. https://doi.org/10.1016/j.ecoenv.2008.02.007

    CAS  Article  Google Scholar 

  8. Arora M, Kiran B, Rani S, Rani A, Kaur B, Mittal N (2008) Heavy metal accumulation in vegetables irrigated with water from different sources. Food Chem 111:811–815. https://doi.org/10.1016/j.foodchem.2008.04.049

    CAS  Article  Google Scholar 

  9. Assouline S, Narkis K, Gherabli R, Sposito G (2015) Combined effect of sodicity and organic matter on soil properties under long-term irrigation with treated wastewater. https://doi.org/10.2136/vzj2015.12.0158

  10. Banni M, Dondero F, Jebali J, Guerbej H, Boussetta H, Viarengo A (2007) Assessment of heavy metal contamination using real-time PCR analysis of mussel metallothionein mt10 and mt20 expression: a validation along the Tunisian coast. Biomarkers 12:369–383. https://doi.org/10.1080/13547500701217061

  11. Banni M, Negri A, Mignone F, Boussetta H, Viarengo A, Dondero F (2011) Gene expression rhythms in the mussel mytilus galloprovincialis (Lam.) across an annual cycle. PLoS One 6. https://doi.org/10.1371/journal.pone.0018904

  12. Banni M, Hajer A, Sforzini S, Oliveri C, Boussetta H, Viarengo A (2014) Transcriptional expression levels and biochemical markers of oxidative stress in Mytilus galloprovincialis exposed to nickel and heat stress. Comp Biochem Physiol - C Toxicol Pharmacol 160:23–29. https://doi.org/10.1016/j.cbpc.2013.11.005

    CAS  Article  Google Scholar 

  13. Banni M, Sforzini S, Balbi T, Corsi I, Viarengo A, Canesi L (2016a) Combined effects of n-TiO2and 2,3,7,8-TCDD in Mytilus galloprovincialis digestive gland: a transcriptomic and immunohistochemical study. Environ Res 145:135–144 . https://doi.org/10.1016/j.envres.2015.12.003

  14. Banni M, Sforzini S, Balbi T, et al. (2016b) Digestive gland : a transcriptomic and immunohistochemical study. 145:135–144 . https://doi.org/10.1016/j.envres.2015.12.003

  15. Bedbabis S, Ben Rouina B, Boukhris M, Ferrara G (2014) Effect of irrigation with treated wastewater on soil chemical properties and infiltration rate. J Environ Manage 133:45–50. https://doi.org/10.1016/j.jenvman.2013.11.007

    CAS  Article  Google Scholar 

  16. Bedbabis S, Trigui D, Ben 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

  17. Behera SK, Kim HW, Oh JE, Park HS (2011) Occurrence and removal of antibiotics, hormones and several other pharmaceuticals in wastewater treatment plants of the largest industrial city of Korea. Sci Total Environ 409:4351–4360. https://doi.org/10.1016/j.scitotenv.2011.07.015

    CAS  Article  Google Scholar 

  18. Belhaj D, Baccar R, Jaabiri I, Bouzid J, Kallel M, Ayadi H, Zhou JL (2015) Fate of selected estrogenic hormones in an urban sewage treatment plant in Tunisia (North Africa). Sci Total Environ 505:154–160. https://doi.org/10.1016/j.scitotenv.2014.10.018

    CAS  Article  Google Scholar 

  19. Booth LH, Heppelthwaite V, Eason CT (1998) Cholinesterase and glutathione S-transferase in the earthworm Apporectodea Caliginosa as biomarkers of organophosphate exposure. Society 138–142

  20. Booth LH, Hodge S, O’Halloran K (2001) Use of biomarkers in earthworms to detect use and abuse of field applications of a model organophosphate pesticide. Bull Environ Contam Toxicol 67:633–640. https://doi.org/10.1007/s001280171

    CAS  Article  Google Scholar 

  21. Bouché MB (1972) Lombriciens de France. Ecologie et systématique, I.N.R.A.

    Google Scholar 

  22. Boughattas I, Hattab S, Boussetta H, Sappin-Didier V, Viarengo A, Banni M, Sforzini S (2016) Biomarker responses of Eisenia andrei to a polymetallic gradient near a lead mining site in North Tunisia. Environ Pollut 218:530–541. https://doi.org/10.1016/j.envpol.2016.07.033

    CAS  Article  Google Scholar 

  23. 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 Pollut Res 24:18083–18,095. https://doi.org/10.1007/s11356-017-9449-8

    CAS  Article  Google Scholar 

  24. 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. https://doi.org/10.1016/0003-2697(76)90527-3

    CAS  Article  Google Scholar 

  25. Brown GG, Barois I, Lavelle P (2000) Regulation of soil organic matter dynamics and microbial activityin the drilosphere and the role of interactionswith other edaphic functional domains. Eur J Soil Biol 36:177–198. https://doi.org/10.1016/S1164-5563(00)01062-1

    Article  Google Scholar 

  26. Campani T, Caliani I, Pozzuoli C, Romi M, Fossi MC, Casini S (2017) Assessment of toxicological effects of raw and bioremediated olive mill waste in the earthworm Eisenia fetida: A biomarker approach for sustainable agriculture. Appl Soil Eco 119:18–25. https://doi.org/10.1016/j.apsoil.2017.05.016

    Article  Google Scholar 

  27. Candan N, Tarhan L (2003) The correlation between antioxidant enzyme activities and lipid peroxidation levels in Mentha pulegium organs grown in Ca2+, Mg2+, Cu2+, Zn2+and Mn2+stress conditions. Plant Sci 165:769–776. https://doi.org/10.1016/S0168-9452(03)00269-3

    CAS  Article  Google Scholar 

  28. Chen X, Wang X, Gu X, Jiang Y, Ji R (2017) Oxidative stress responses and insights into the sensitivity of the earthworms Metaphire guillelmi and Eisenia fetida to soil cadmium. Sci Tot Environ 574:300–306. https://doi.org/10.1016/j.scitotenv.2016.09.059

    CAS  Article  Google Scholar 

  29. Chomczynski P (1987) Single-step method of RNA isolation by acid guanidinium extraction. 159:156–159. https://doi.org/10.1016/0003-2697(87)90021-2

  30. Chouchene L, Banni M, Kerkeni A, Saïd K, Messaoudi I (2011) Cadmium-induced ovarian pathophysiology is mediated by change in gene expression pattern of zinc transporters in zebrafish (Danio rerio). Chem Biol Inter 193(2):172–179. https://doi.org/10.1007/s10534-011-9456-z

    CAS  Article  Google Scholar 

  31. Chung BY, Song CH, Park BJ, Cho JY (2011) Heavy metals in brown rice (Oryza sativa L.) and soil after long-term irrigation of wastewater discharged from domestic sewage treatment plants. Pedosphere 21:621–627. https://doi.org/10.1016/S1002-0160(11)60164-1

    CAS  Article  Google Scholar 

  32. Claiborne A (1985) Catalase activity. In: Greenwald RA (ed) Handbook of methods for oxygen radical research. CRC Press, Boca Raton, pp 283–284

    Google Scholar 

  33. Coleman DC, Crossley DA Jr, Hendrix PF (2004) Fundamentals of Soil Ecology, 2nd edn. Elsevier Academic Press, San Diego

    Google Scholar 

  34. Du L, Li G, Liu M, Li Y, Yin S, Zhao J, Zhang X (2015) Evaluation of DNA damage and antioxidant system induced by di-n-butyl phthalates exposure in earthworms (Eisenia fetida). Ecotoxicol Environ Saf 115:75–82. https://doi.org/10.1016/j.ecoenv.2015.01.031

    CAS  Article  Google Scholar 

  35. Ayni F El, Cherif S, Jrad A, Trabelsi-Ayadi M (2011) Impact of treated wastewater reuse on agriculture and aquifer recharge in a coastal area: Korba Case Study. Water Resour Manag 25:2251–2265 . https://doi.org/10.1007/s11269-011-9805-2

  36. Edwards CA, Bohlen PJ (1992) The effects of toxic chemicals on earthworms. Environ Contam Toxicol 125:23–100

    CAS  Google Scholar 

  37. Ellman GL, Courtney KD, Andres V Jr, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Bioch Pharm 7(2):88–95. https://doi.org/10.1016/0006-2952(61)90145-9

    CAS  Article  Google Scholar 

  38. Emongor VE, Ramolemana GM (2004) Treated sewage effluent (water) potential to be used for horticultural production in Botswana. Phys Chem Earth 29:1101–1108. https://doi.org/10.1016/j.pce.2004.08.003

    Article  Google Scholar 

  39. Frasco MF, Fournier D, Carvalho F, Guilhermino L (2005) Do metals inhibit acetylcholinesterase (AchE)? Implementation of assay conditions for the use of AchE activity as a biomarker of metal toxicity. Biomarkers 10:360–375. https://doi.org/10.1080/13547500500264660

    CAS  Article  Google Scholar 

  40. Gambi N, Pasteris A, Fabbri E (2007) Acetylcholinesterase activity in the earthworm Eisenia andrei at different conditions of carbaryl exposure. Comp Biochem Physiol - C Toxicol Pharmacol 145:678–685. https://doi.org/10.1016/j.cbpc.2007.03.002

    CAS  Article  Google Scholar 

  41. Geret F, Serafim A, Barreira L, João Bebianno M (2002) Response of antioxidant systems to copper in the gills of the clam Ruditapes decussatus. Mar Environ Res 54:413–417. https://doi.org/10.1016/S0141-1136(02)00164-2

    CAS  Article  Google Scholar 

  42. Gondhowiardjo TD (1993) Corneal aldehyde dehydrogenase, glutathione reductase, and glutathione S-transferase in pathologic corneas. Cornea 12(4):310–314

    CAS  Article  Google Scholar 

  43. Grisaru D, Deutsch V, Shapira M, Pick M, Sternfeld M, Melamed-Book N, Kaufer D, Galyam N, Gait MJ, Owen D, Lessing JB, Eldor A, Soreq H (2001) ARP, a peptide derived from the stress-associated acetylcholinesterase variant, has hematopoietic growth promoting activities. Mol Med 7:93–105

    CAS  Article  Google Scholar 

  44. Gros M, Petrović M, Ginebreda A, Barceló D (2010) Removal of pharmaceuticals during wastewater treatment and environmental risk assessment using hazard indexes. Environ Int 36:15–26. https://doi.org/10.1016/j.envint.2009.09.002

    CAS  Article  Google Scholar 

  45. Habig WJ, Pabst MJ, Jacoby WB (1974) Glutathione S-transferase, the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    CAS  Google Scholar 

  46. Hamilton AJ, Stagnitti F, Xiong X, Kreidl SL, Benke KK, Maher P (2007) Wastewater irrigation: the state of play. Vadose Zo J 6:823. https://doi.org/10.2136/vzj2007.0026

    Article  Google Scholar 

  47. Hattab S, Boughattas I, Boussetta H, Viarengo A, Banni M, Sforzini S (2015) Transcriptional expression levels and biochemical markers of oxidative stress in the earthworm Eisenia andrei after exposure to 2,4-dichlorophenoxyacetic acid (2,4-D). Ecotoxicol Environ Saf 122:76–82. https://doi.org/10.1016/j.ecoenv.2015.07.014

    CAS  Article  Google Scholar 

  48. Heidarpour M, Mostafazadeh-Fard B, Abedi Koupai J, Malekian R (2007) The effects of treated wastewater on soil chemical properties using subsurface and surface irrigation methods. Agric Water Manag 90:87–94. https://doi.org/10.1016/j.agwat.2007.02.009

    Article  Google Scholar 

  49. Houda Z, Bejaoui Z, Albouchi A (2016) Comparative study of plant growth of two poplar tree species irrigated with treated wastewater , with particular reference to accumulation of heavy metals ( Cd , Pb , As , and Ni ). https://doi.org/10.1007/s10661-016-5102-0

  50. Hyne RV, Maher WA (2003) Invertebrate biomarkers: links to toxicosis that predict population decline. Ecotoxicol Environ Saf 54:366–374. https://doi.org/10.1016/S0147-6513(02)00119-7

    CAS  Article  Google Scholar 

  51. Jaramillo MF, Restrepo I (2017) Wastewater reuse in agriculture: a review about its limitations and benefits. Sustain 9. https://doi.org/10.3390/su9101734

  52. Jones CG, Lawton JH, Shachak M (2014) Positive and negative effects of organisms as physical ecosystem engineers positive and negative effects of organisms as. 78:1946–1957

  53. Jouni F, Sanchez-hernandez JC, Mazzia C, Jobin M (2018) Interspecific differences in biochemical and behavioral biomarkers in endogeic earthworms exposed to ethyl-parathion. ECSN. https://doi.org/10.1016/j.chemosphere.2018.03.060

  54. Khadhar S, Abdelkarim C, Yassin H, Teruo H (2013) The effect of long-term soil irrigation by wastewater on organic matter, polycyclic aromatic hydrocarbons, and heavy metals evolution: case study of Zaouit Sousse (Tunisia). Arab J Geosci 6(11):4337–4346. https://doi.org/10.1007/s12517-012-0666-7

    CAS  Article  Google Scholar 

  55. Kim S, Aga DS (2007) Potential ecological and human health impacts of antibiotics and antibiotic-resistant bacteria from wastewater treatment plants. J Toxicol Environ Heal - Part B Crit Rev 10:559–573. https://doi.org/10.1080/15287390600975137

    CAS  Article  Google Scholar 

  56. 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

    CAS  Article  Google Scholar 

  57. Kono Y, Fridovich I (1982) Superoxide radical inhibits catalase. J Biol Chem 257:5751–5754

    CAS  Google Scholar 

  58. Li L, Yang D, Song Y, Shi Y, Huang B, Bitsch A, Yan J (2017) The potential acute and chronic toxicity of cyfluthrin on the soil model organism, Eisenia fetida. Ecotoxicol Environ Saf 144:456–463. https://doi.org/10.1016/j.ecoenv.2017.06.064

    CAS  Article  Google Scholar 

  59. Liang J, Xia X, Yuan L, Zhang W, Lin K, Zhou B, Hu S (2017) The reproductive responses of earthworms (Eisenia fetida) exposed to nanoscale zero-valent iron (nZVI) in the presence of decabromodiphenyl ether (BDE209). Environ Pollut:1–8. https://doi.org/10.1016/j.envpol.2017.10.130

  60. Liu T, Wang X, You X, Chen D, Li Y, Wang F (2017) Oxidative stress and gene expression of earthworm (Eisenia fetida) to clothianidin. Ecotoxicolo Environ Saf 142:489–496. https://doi.org/10.1016/j.ecoenv.2017.04.012

    CAS  Article  Google Scholar 

  61. Livingstone D, 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 Eco 3(4):415–424. https://doi.org/10.2307/2389604

    Article  Google Scholar 

  62. Luo J, Shi R (2005) Acrolein induces oxidative stress in brain mitochondria. Neurochem Int 46:243–252. https://doi.org/10.1016/j.neuint.2004.09.001

    CAS  Article  Google Scholar 

  63. Maity S, Banerjee R, Goswami P et al (2018) Chemosphere oxidative stress responses of two different ecophysiological species of earthworms ( Eutyphoeus waltoni and Eisenia fetida ) exposed to Cd-contaminated soil. Chemosphere 203:307–317. https://doi.org/10.1016/j.chemosphere.2018.03.189

    CAS  Article  Google Scholar 

  64. Mkhinini M, Boughattas I, Alphonse V, Livet A, Bousserrhine N, Banni M (2019) 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. https://doi.org/10.1016/j.scitotenv.2018.07.449

    CAS  Article  Google Scholar 

  65. Moore MN, Icarus Allen J, McVeigh A (2006) Environmental prognostics: an integrated model supporting lysosomal stress responses as predictive biomarkers of animal health status. Mar Environ Res 61:278–304. https://doi.org/10.1016/j.marenvres.2005.10.005

    CAS  Article  Google Scholar 

  66. Muir MA, Yunusa IAM, Burchett MD, Lawrie R, Chan KY, Manoharan V (2007) Short-term responses of two contrasting species of earthworms in an agricultural soil amended with coal fly-ash. Soil Bio Biochem 39(5):987–992. https://doi.org/10.1016/j.soilbio.2006.10.006

    CAS  Article  Google Scholar 

  67. Negreanu Y, Pasternak Z, Jurkevitch E, Cytryn E (2012) Impact of treated wastewater irrigation on antibiotic resistance in agricultural soils. Environ Sci Technol 46:4800–4808. https://doi.org/10.1021/es204665b

    CAS  Article  Google Scholar 

  68. Negri A, Potocki W, Iwanicki A, Obuchowski M, Hinc K (2013) Expression and display of Clostridium difficile protein FliD on the surface of Bacillus subtilis spores. J Med Microbiol 62:1379–1385. https://doi.org/10.1099/jmm.0.057372-0

    CAS  Article  Google Scholar 

  69. Novo M, Verdú I, Trigo D, Martínez-Guitarte JL (2018) Endocrine disruptors in soil: effects of bisphenol A on gene expression of the earthworm Eisenia fetida. Ecotoxicol Environ Saf 150:159–167. https://doi.org/10.1016/j.ecoenv.2017.12.030

    CAS  Article  Google Scholar 

  70. OECD, 2004a. Test no. 222. Earthworm reproduction test (Eisenia fetida/andrei). OECD Guidelines for the Testing of Chemicals, Organisation for Economic Co-operation and Development.

  71. OECD, 2004b. Test no. 220. Enchytraeid Reproduction Test. OECD Guidelines for the Testing of Chemicals, Organisation for Economic Co-operation and Development.

  72. Panzarino O, Hyršl P, Dobeš P, Vojtek L, Vernile P, Bari G, Terzano R, Spagnuolo M, de Lillo E (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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  74. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36. https://doi.org/10.1093/nar/30.9.e36

    Article  Google Scholar 

  75. Rodriguez-Campos J, Dendooven L, Alvarez-Bernal D, Contreras-Ramos SM (2014) Potential of earthworms to accelerate removal of organic contaminants from soil: a review. Appl Soil Ecol 79:10–25. https://doi.org/10.1016/j.apsoil.2014.02.010

    Article  Google Scholar 

  76. Rodríguez-Castellanos L, Sanchez-Hernandez JC (2007) Earthworm biomarkers of pesticide contamination: current status and perspectives. J Pestic Sci 32:360–371 . https://doi.org/10.1584/jpestics. R07-14

  77. Romani R, Antognelli C, Baldracchini F, De Santis A, Isani G, Giovannini E, Rosi G (2003) Increased acetylcholinesterase activities in specimens of Sparus auratus exposed to sublethal copper concentrations. Chem Biol Interact 145:321–329. https://doi.org/10.1016/S0009-2797(03)00058-9

    CAS  Article  Google Scholar 

  78. Ronis MJJ, Hakkak R, Korourian S, Albano E, Yoon S, Ingelman-Sundberg M, Lindros KO, Badger TM (2004) Alcoholic liver disease in rats fed ethanol as part of oral or intragastric low-carbohydrate liquid diets. Exp Biol Med (Maywood) 229:351–360

    CAS  Article  Google Scholar 

  79. Saint-Denis M, Narbonne JF, Arnaud C, Ribera D (2001) Biochemical responses of the earthworm Eisenia fetida andrei exposed to contaminated artificial soil: effects of lead acetate. Soil Biol Biochem 33:395–404. https://doi.org/10.1016/S0038-0717(00)00177-2

    CAS  Article  Google Scholar 

  80. Sanchez-Hernandez JC (2006) Earthworm biomarkers in ecological risk assessment. In: Reviews of environmental contamination and toxicology. Springer, New York, pp 85–126

    Google Scholar 

  81. Sanchez-Hernandez JC, Manuel J, Andrés R (2018a) Response of digestive enzymes and esterases of ecotoxicological concern in earthworms exposed to chlorpyrifos-treated soils. Ecotoxicology:890–899. https://doi.org/10.1007/s10646-018-1914-8

  82. Sanchez-Hernandez JC, Notario del Pino J, Capowiez Y et al (2018b) Soil enzyme dynamics in chlorpyrifos-treated soils under the influence of earthworms. Sci Total Environ 612:1407–1416. https://doi.org/10.1016/j.scitotenv.2017.09.043

    CAS  Article  Google Scholar 

  83. Sanchez-Hernandez JC, Notario del Pino J, Capowiez Y, Mazzia C, Rault M (2018c) Soil enzyme dynamics in chlorpyrifos-treated soils under the influence of earthworms. Sci Total Environ 612:1407–1416. https://doi.org/10.1016/j.scitotenv.2017.09.043

    CAS  Article  Google Scholar 

  84. Schreck E, Geret F, Gontier L, Treilhou M (2008) Neurotoxic effect and metabolic responses induced by a mixture of six pesticides on the earthworm Aporrectodea caliginosa nocturna. Chemosphere 71:1832–1839. https://doi.org/10.1016/j.chemosphere.2008.02.003

    CAS  Article  Google Scholar 

  85. Sforzini S, Moore MN, Boeri M, Bencivenga M, Viarengo A (2014) Effects of PAHs and dioxins on the earthworm Eisenia andrei: a multivariate approach for biomarker interpretation. Environ Pollut 196:60–71. https://doi.org/10.1016/j.envpol.2014.09.015

    CAS  Article  Google Scholar 

  86. Sforzini S, Oliveri C, Orrù A, Chessa G, Pacchioni B, Millino C, Jha AN, Viarengo A, Banni M (2018) Application of a new targeted low density microarray and conventional biomarkers to evaluate the health status of marine mussels: a field study in Sardinian coast, Italy. Sci Total Environ 628–629:319–320. https://doi.org/10.1016/j.scitotenv.2018.01.293

    CAS  Article  Google Scholar 

  87. Shalata A, Tal M (1998) The effect of salt stress on lipid peroxidation and antioxidants in the leaf of the cultivated tomato and its wild salt‐tolerant relative Lycopersicon pennellii. Physio Plant 104(2):169–174. https://doi.org/10.1034/j.1399-3054.1998.1040204.x

    CAS  Article  Google Scholar 

  88. Sharma KP, Sharma S, Sharma S, Singh PK, Kumar S, Grover R, Sharma PK (2007) A comparative study on characterization of textile wastewaters (untreated and treated) toxicity by chemical and biological tests. Chemo 69(1):48–54. https://doi.org/10.1016/j.chemosphere.2007.04.086

    CAS  Article  Google Scholar 

  89. Sperling LE, Klaczinski J, Schütz C, Rudolph L, Layer PG (2012) Mouse acetylcholinesterase enhances neurite outgrowth of rat R28 cells through interaction with laminin-1. PLoS One 7:1–11. https://doi.org/10.1371/journal.pone.0036683

    CAS  Article  Google Scholar 

  90. Sui Q, Huang J, Deng S, Chen W, Yu G (2011) Seasonal variation in the occurrence and removal of pharmaceuticals and personal care products in different biological wastewater treatment processes. Environ Sci Tech 45(8):3341–3348. https://doi.org/10.1021/es200248d

    CAS  Article  Google Scholar 

  91. Sun KH, De Pablo Y, Vincent F, Shah K (2008) Deregulated Cdk5 promotes oxidative stress and mitochondrial dysfunction. J Neurochem 107:265–278. https://doi.org/10.1111/j.1471-4159.2008.05616.x

    CAS  Article  Google Scholar 

  92. Tanoue R, Sato Y, Motoyama M, Nakagawa S, Shinohara R, Nomiyama K (2012) Plant uptake of pharmaceutical chemicals detected in recycled organic manure and reclaimed wastewater. https://doi.org/10.1021/jf303142t

  93. Thioulouse J, Dray S (2007) Interactive multivariate data analysis in R with the ade4 and ade4TkGUI Packages. J Stat Softw 22:1–14 . citeulike-article-id:3973175

  94. Travis MJ, Wiel-Shafran A, Weisbrod N, Adar E, Gross A (2010) Greywater reuse for irrigation: Effect on soil properties. Sci Tot Environ 408(12):2501–2508. https://doi.org/10.1016/j.scitotenv.2010.03.005

    CAS  Article  Google Scholar 

  95. Tsyusko OV, Hardas SS, Shoults-Wilson WA, Starnes CP, Joice G, Butterfield DA, Unrine JM (2012) Short-term molecular-level effects of silver nanoparticle exposure on the earthworm, Eisenia fetida. Environ Pollut 171:249–255. https://doi.org/10.1016/j.envpol.2012.08.003

    CAS  Article  Google Scholar 

  96. Vasseur P, Bonnard M (2014) Ecogenotoxicology in earthworms: a review. Curr Zool 60:255–272. https://doi.org/10.1093/czoolo/60.2.255

    CAS  Article  Google Scholar 

  97. Velki M, Hackenberger BK (2013) Inhibition and recovery of molecular biomarkers of earthworm Eisenia andrei after exposure to organophosphate dimethoate. Soil Biol Biochem 57:100–108. https://doi.org/10.1016/j.soilbio.2012.09.018

    CAS  Article  Google Scholar 

  98. Wang Y, Zhang Q, Lv J, Li A, Liu H, Li G, Jiang G (2007) Polybrominated diphenyl ethers and organochlorine pesticides in sewage sludge of wastewater treatment plants in China. Chemosphere 68(9):1683–1691. https://doi.org/10.1016/j.chemosphere.2007.03.060

    CAS  Article  Google Scholar 

  99. Wang C, Zhang Q, Wang F, Liang W (2017) Toxicological effects of dimethomorph on soil enzymatic activity and soil earthworm (Eisenia fetida). Chemosphere 169:316–323. https://doi.org/10.1016/j.chemosphere.2016.11.090

    CAS  Article  Google Scholar 

  100. Weeks JM, Spurgeon DJ, Svendsen C, Hankard PK, Kammenga JE, Dallinger R, Köhler HR, Simonsen V, Scott-Fordsmand J (2004) Critical analysis of soil invertebrate biomarkers: a field case study in Avonmouth, UK. Ecotoxicology 13:817–822. https://doi.org/10.1007/s10646-003-4479-z

    CAS  Article  Google Scholar 

  101. Wu S, Kuschk P, Brix H, Vymazal J, Dong R (2014a) Development of constructed wetlands inperformance intensifications for wastewater treatment: a nitrogen and organic matter targeted review. Water Res 57:40–45. https://doi.org/10.1016/j.watres.2014.03.020

    CAS  Article  Google Scholar 

  102. Wu X, Conkle JL, Ernst F, Gan J (2014b) Treated wastewater irrigation: uptake of pharmaceutical and personal care products by common vegetables under field conditions. Environ Sci Technol 48:11286–11,293. https://doi.org/10.1021/es502868k

    CAS  Article  Google Scholar 

  103. Xu FJ, Li G, Jin CW, Liu WJ, Zhang SS, Zhang YS, Lin XY (2012) Aluminum-induced changes in reactive oxygen species accumulation, lipid peroxidation and antioxidant capacity in wheat root tips. Biol Plant 56:89–96. https://doi.org/10.1007/s10535-012-0021-6

    CAS  Article  Google Scholar 

  104. Xue Y, Gu X, Wang X, Sun C, Xu X, Sun J, Zhang B (2009) The hydroxyl radical generation and oxidative stress for the earthworm Eisenia fetida exposed to tetrabromobisphenol A. Ecotoxicology 18:693–699. https://doi.org/10.1007/s10646-009-0333-2

    CAS  Article  Google Scholar 

  105. Yang G, Chen C, Yu Y et al (2018) Ecotoxicology and environmental safety combined effects of four pesticides and heavy metal chromium ( VI ) on the earthworm using avoidance behavior as an endpoint. Ecotoxicol Environ Saf 157:191–200. https://doi.org/10.1016/j.ecoenv.2018.03.067

    CAS  Article  Google Scholar 

  106. Zayneb C, Lamia K, Olfa E, Naïma J, Grubb CD, Bassem K et al (2015) Morphological, physiological and biochemical impact of ink industry effluent on germination of maize (Zea mays), Barley (Hordeum vulgare) and Sorghum (Sorghum bicolor). Bul Environ Contam Tox 95(5):687–693. https://doi.org/10.1007/s00128-015-1600-y

    CAS  Article  Google Scholar 

  107. Zhang Y, Sallach JB, Hodges L, Snow DD, Bartelt-Hunt SL, Eskridge KM, Li X (2016) Effects of soil texture and drought stress on the uptake of antibiotics and the internalization of Salmonella in lettuce following wastewater irrigation. Environ Pollut 208:523–531. https://doi.org/10.1016/j.envpol.2015.10.025

    CAS  Article  Google Scholar 

  108. Zoghlami RI, Hamdi H, Boudabbous K, Hechmi S (2018) Seasonal toxicity variation in light-textured soil amended with urban sewage sludge : interaction effect on cadmium , nickel , and phytotoxicity. 3608–3615

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Correspondence to Iteb Boughattas.

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Mkhinini, M., Boughattas, I., Bousserhine, N. et al. Biochemical and transcriptomic response of earthworms Eisenia andrei exposed to soils irrigated with treated wastewater. Environ Sci Pollut Res 26, 2851–2863 (2019). https://doi.org/10.1007/s11356-018-3794-0

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Keywords

  • Eisenia andrei
  • Oxidative stress
  • TWW
  • Gene expression level
  • Lipid peroxidation