Abstract
Amphibians are now recognized as the most endangered group. One of this decline causes is the degradation of their habitat through direct contamination of water, soil leaching, or runoff from surrounding contaminated soils and environments. In the North of France, the extensive industrial activities resulted in massive soil contamination by metal compounds. Mineral amendments were added to soils to decrease trace metal mobility. Because of the large areas to be treated, the use of inexpensive industrial by-products was favored. Two types of fly ashes were both tested in an experimental site with the plantation of trees in 2000. Aim of the present work was to investigate the effects of extracts from metal-contaminated soils treated or not for 10 years with fly ashes on Xenopus laevis oocyte using cell biology approaches. Indeed, our previous studies have shown that the Xenopus oocyte is a relevant model to study the metal ion toxicity. Survival and maturation of oocyte exposed to the soil extracts were evaluated by phenotypic approaches and electrophysiological recordings. An extract derived from a metal-contaminated soil treated for 10 years with sulfo-calcic ashes induced the largest effects. Membrane integrity appeared affected and ion fluxes in exposed oocytes were changed. Thus, it appeared that extracted elements from certain mineral amendments used to prevent the mobility of metals in the case of highly metal-contaminated soils could have a negative impact on X. laevis oocytes.
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References
Ali M, Parvez S, Pandey S, Atif F, Kaur M, Rehman H, Raisuddin S (2004) Fly ash leachate induces oxidative stress in freshwater fish Channa punctata (Bloch). Environ Int 30:933–938. https://doi.org/10.1016/j.envint.2004.03.004
Baize D, Sterckeman T (2001) Of the necessity of knowledge of the natural pedo-geochemical background content in the evaluation of the contamination of soils by trace elements. Sci Total Environ 264:127–139. https://doi.org/10.1016/S0048-9697(00)00615-X
Békaert C, Rast C, Ferrier V, Bispo A, Jourdain MJ, Vasseur P (1999) Use of in vitro (Ames and Mutatox tests) and in vivo (Amphibian Micronucleus test) assays to assess the genotoxicity of leachates from a contaminated soil. Org Geochem 30:953–962. https://doi.org/10.1016/S0146-6380(99)00079-0
Berzins DW, Bundy KJ (2002) Bioaccumulation of lead in Xenopus laevis tadpoles from water and sediment. Environ Int 28:69–77. https://doi.org/10.1016/S0160-4120(02)00006-5
Bodart J-F, Gutierrez D, Nebreda A et al (2002) Characterization of MPF and MAPK activities during meiotic maturation of Xenopus tropicalis Oocytes. Dev Biol 245:348–361. https://doi.org/10.1006/dbio.2002.0647
Chakraborty R, Mukherjee A (2009) Mutagenicity and genotoxicity of coal fly ash water leachate. Ecotoxicol Environ Saf 72:838–842. https://doi.org/10.1016/j.ecoenv.2008.09.023
Charbonneau M, Moreau M, Picheral B, Vilain JP, Guerrier P (1983) Fertilization of amphibian eggs: a comparison of electrical responses between anurans and urodeles. Dev Biol 98:304–318. https://doi.org/10.1016/0012-1606(83)90361-5
Collins J, Storfer A (2003) Global amphibian declines: sorting the hypotheses. Divers Distrib 9:89–98. https://doi.org/10.1046/j.1472-4642.2003.00012.x
Demuynck S, Succiu IR, Grumiaux F, Douay F, Leprêtre A (2014) Effects of field metal-contaminated soils submitted to phytostabilisation and fly ash-aided phytostabilisation on the avoidance behaviour of the earthworm Eisenia fetida. Ecotoxicol Environ Saf 107:170–177. https://doi.org/10.1016/j.ecoenv.2014.05.011
Dumont J (1972) Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J Morphol 136:153–179. https://doi.org/10.1002/jmor.1051360203
Duprat F (1998) Étude par Électrophysiologie des Relations Structure-fonction, de la Pharmacologie et des Régulations de Canaux Potassiques Clonés. Ph.D. thesis. Université de Nice Sophia Antipolis, France
Grumiaux F, Demuynck S, Schikorski D, Lemière S, Vandenbulcke F, Leprêtre A (2007) Effect of fluidized bed combustion ashes used in metal polluted soil remediation on life history traits of the oligochaeta Eisenia andrei. Eur J Soil Biol 43:S256–S260. https://doi.org/10.1016/j.ejsobi.2007.08.038
Grumiaux F, Demuynck S, Schikorski D, Lemière S, Leprêtre A (2010) Assessing the effects of FBC ash treatments of metal-contaminated soils using life history traits and metal bioaccumulation analysis of the earthworm Eisenia andrei. Chemosphere 79:156–161. https://doi.org/10.1016/j.chemosphere.2010.01.018
Guerrier P, Moreau M, Meijer L, Mazzei G, Vilain JP, Dubé F (1982) The role of calcium in meiosis reinitiation. Prog Clin Biol Res 91:139–155
Heikkila JJ, Kaldis A, Morrow G, Tanguay RM (2007) The use of the Xenopus oocyte as a model system to analyze the expression and function of eukaryotic heat shock proteins. Biotechnol Adv 25:385–395. https://doi.org/10.1016/j.biotechadv.2007.03.003
Hillman S (1980) Physiological correlates of diffenrential dehydration tolerance anuran amphibians. Copeia 1980(1):125–129
IUCN (2018) Threatened species in past and present IUCN Red Lists. In: IUCN.com. http://www.iucnredlist.org/about/summary-statistics
Leclercq-Dransart J, Santorufo L, Pernin C, Louvel B, Demuynck S, Grumiaux F, Douay F, Leprêtre A (2018) Litter breakdown as a tool for assessment of the efficiency of afforestation and ash-aided phytostabilization on metal-contaminated soils functioning in Northern France. Environ Sci Pollut Res Int 25:18579–18595. https://doi.org/10.1007/s11356-018-2038-7
Lienesch L, Dumont J, Bantle J (2000) The effect of cadmium on oogenesis in Xenopus laevis. Chemosphere 41:1651–1658. https://doi.org/10.1016/S0045-6535(00)00046-1
Lopareva-Pohu A, Pourrut B, Waterlot C, Garçon G, Bidar G, Pruvot C, Shirali P, Douay F (2011a) Assessment of fly ash-aided phytostabilisation of highly contaminated soils after an 8-year field trial: Part 1. Influence on soil parameters and metal extractability. Sci Total Environ 409:647–654. https://doi.org/10.1016/j.scitotenv.2010.10.040
Lopareva-Pohu A, Verdin A, Garçon G, Lounès-Hadj Sahraoui A, Pourrut B, Debiane D, Waterlot C, Laruelle F, Bidar G, Douay F, Shirali P (2011b) Influence of fly ash aided phytostabilisation of Pb, Cd and Zn highly contaminated soils on Lolium perenne and Trifolium repens metal transfer and physiological stress. Environ Pollut 159:1721–1729. https://doi.org/10.1016/j.envpol.2011.02.030
Manerikar RS, Apte AA, Ghole VS (2008) In vitro genotoxicity of fly ash leachate in earthworm coelomocytes. Toxicol Environ Chem 90:293–300. https://doi.org/10.1080/02772240701458451
Marin M, Sellier C, Paul-Antoine A et al (2010) Calcium dynamics during physiological acidification in Xenopus oocyte. J Membr Biol 236:233–245
Marin M, Slaby S, Marchand G, Demuynck S, Friscourt N, Gelaude A, Lemière S, Bodart JF (2015) Xenopus laevis oocyte maturation is affected by metal chlorides. Toxicol in Vitro 29:1124–1131. https://doi.org/10.1016/j.tiv.2015.04.016
Mench M, Lepp N, Bert V, Schwitzguébel JP, Gawronski SW, Schröder P, Vangronsveld J (2010) Successes and limitations of phytotechnologies at field scale: outcomes, assessment and outlook from COST Action 859. J Soils Sediments 10:1039–1070
Monastersky R (2014) Life -- a status report. Nature 516:158–161. https://doi.org/10.1038/516158a
Nebreda AR, Ferby I (2000) Regulation of the meiotic cell cycle in oocytes. Curr Opin Cell Biol 12:666–675. https://doi.org/10.1016/S0955-0674(00)00150-2
Papadimitriou CA, Haritou I, Samaras P, Zouboulis AI (2008) Evaluation of leaching and ecotoxicological properties of sewage sludge–fly ash mixtures. Environ Res 106:340–348. https://doi.org/10.1016/j.envres.2007.04.007
Parker I, Miledi R (1988) A calcium-independent chloride current activated by hyperpolarization in Xenopus oocytes. Proc R Soc L B Biol Sci 233:191–199
Pourrut B, Lopareva-Pohu A, Pruvot C, Garçon G, Verdin A, Waterlot C, Bidar G, Shirali P, Douay F (2011) Assessment of fly ash-aided phytostabilisation of highly contaminated soils after an 8-year field trial: part 2. Influence on plants Sci Total Environ 409:4504–4510. https://doi.org/10.1016/j.scitotenv.2011.07.047
Robidoux PY, Gong P, Sarrazin M, Bardai G, Paquet L, Hawari J, Dubois C, Sunahara GI (2004) Toxicity assessment of contaminated soils from an antitank firing range. Ecotoxicol Environ Saf 58:300–313. https://doi.org/10.1016/j.ecoenv.2003.11.004
Selvi M, Gül A, Yılmaz M (2003) Investigation of acute toxicity of cadmium chloride (CdCl2·H2O) metal salt and behavioral changes it causes on water frog (Rana ridibunda Pallas, 1771). Chemosphere 52:259–263. https://doi.org/10.1016/S0045-6535(03)00262-5
Sharma B, Patiño R (2009) Effects of cadmium on growth, metamorphosis and gonadal sex differentiation in tadpoles of the African clawed frog, Xenopus laevis. Chemosphere 76:1048–1055. https://doi.org/10.1016/j.chemosphere.2009.04.043
Sobotka J, Rahwan R (1995) Teratogenesis induced by short- and long-term exposure of Xenopus laevis progeny to lead. J Toxicol Environ Health 44:469–484
Sterckeman T, Douay F, Fourrier H, Proix N (2002) Référentiel pédo-géochimique du Nord-Pas de Calais. Rapport Technique. Conseil Régional Nord-Pas de Calais - Ministère de l’Aménagement du Territoire et de l’Environnement, France
Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786. https://doi.org/10.1126/science.1103538
Sun L, Hodeify R, Haun S, Charlesworth A, MacNicol AM, Ponnappan S, Ponnappan U, Prigent C, Machaca K (2008) Ca2+ homeostasis regulates Xenopus oocyte maturation. Biol Reprod 78:726–735
Thompson J, Bannigan J (2008) Cadmium: Toxic effects on the reproductive system and the embryo. Reprod Toxicol 25:304–315. https://doi.org/10.1016/j.reprotox.2008.02.001
Ullah G, Jung P, Machaca K (2007) Modeling Ca2+ signaling differentiation during oocyte maturation. Cell Calcium 42:556–564. https://doi.org/10.1016/j.ceca.2007.01.010
Van Gestel C, Van der Waarde J, Derksen J et al (2001) The use of acute and chronic bioassays to determine the ecological risk and bioremediation efficiency of oil-polluted soils. Environ Toxicol Chem 20:1438–1449
Van Maanen J, Borm P, Knaapen A et al (1999) In vitro effects of coal fly ashes: hydroxyl radical generation, iron release, and DNA damage and toxicity in rat lung epithelial cells. Inhal Toxicol 11:1123–1141. https://doi.org/10.1080/089583799196628
Vilain J, Moumene M, Moreau M (1989) Chloride current modulation during meiosis in Xenopus oocytes. J Exp Zool 250:100–108. https://doi.org/10.1002/jez.1402500114
Voelkel K, Krug H, Diabate S (2003) Formation of reactive oxygen species in rat epithelial cells upon stimulation with fly ash. J Biosci 28:51–55
Weber W (1999) Ion currents of Xenopus laevis oocytes: state of the art. Biochim Biophys Acta 1421:213–233
Yao Y, Tsien R (1997) Calcium current activated by depletion of calcium stores in Xenopus oocytes. J Gen Physiol 109:703–715
Acknowledgments
We are indebted to the Research Federation FRABio (Univ. Lille, CNRS, FR 3688, FRABio, Biochimie Structurale et Fonctionnelle des Assemblages Biomoléculaires) for providing the scientific and technical environment conducive to the achievement of this work. Sylvain Slaby is a recipient for a doctoral fellowship from French Minister of Higher Education, Research and Innovation.
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Marchand, G., Demuynck, S., Slaby, S. et al. Adverse effects of fly ashes used as immobilizing agents for highly metal-contaminated soils on Xenopus laevis oocytes survival and maturation—a study performed in the north of France with field soil extracts. Environ Sci Pollut Res 27, 3706–3714 (2020). https://doi.org/10.1007/s11356-019-04560-0
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DOI: https://doi.org/10.1007/s11356-019-04560-0