[en] Very few ecotoxicological studies have been performed on long-term exposure under controlled conditions, hence limiting the assessment of the impact of chronic and diffuse chemical pressures on the health of aquatic organisms. In this study, an ecotoxicoproteomic approach was used to assess the integrated response and possible acclimation mechanisms in Gammarus fossarum following chronic exposures to Cd, Cu or Pb, at environmentally realistic concentrations (i.e. 0.25, 1.5 and 5 µg/L respectively). After 10-week exposure, changes in protein expression were investigated in caeca of control and exposed males. Gel-free proteomic analyses allowed for the identification of 35 proteins involved in various biological functions, for which 23 were significantly deregulated by metal exposures. The protein deregulation profiles were specific to each metal, providing evidence for metal-specific action sites and responses of gammarids. Among the tested metals, Cu was the most toxic in terms of mortality, probably linked with persistent oxidative stress. Moulting and osmoregulation were the major biological functions affected by Cu in the long-term. In Pb-exposed gammarids, significant deregulations of proteins involved in immune response and cytoskeleton were observed. Reproduction appears to be strongly affected in gammarids chronically exposed to Cd or Pb. Besides, modified expressions of several proteins involved in energy transfer and metabolism highlighted important energetic reshuffling to cope with chronic metal exposures. These results support the fact that metallic pressures induce a functional and energetic cost for individuals of G. fossarum with potential repercussions on population dynamics. Furthermore, this ecotoxicoproteomic study offers promising lines of enquiry in the development of new biomarkers that could make evidence of long-term impacts of metals on the health of organisms.
Centre/Unité de recherche :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Disciplines :
Sciences de l’environnement & écologie
Auteur, co-auteur :
Gismondi, Eric ; Université de Liège > Département de Biologie, Ecologie et Evolution > Ecologie animale et écotoxicologie
Thomé, Jean-Pierre ; Université de Liège > Département de Biologie, Ecologie et Evolution > Ecologie animale et écotoxicologie
Abidi, S., Abbaci, K.T., Geffard, O., Boumaiza, M., Dumet, A., Garric, J., Mondy, N., Impact of cadmium on the ecdysteroids production in Gammarus fossarum. Ecotoxicology 25 (2016), 880–887.
Arce Funck, J., Danger, M., Gismondi, E., Cossu-Leguille, C., Guérold, F., Felten, V., Behavioural and physiological responses of Gammarus fossarum (Crustacea Amphipoda) exposed to silver. Aquat. Toxicol. 142–143 (2013), 73–84.
Brooks, S.J., Lloyd Mills, C., The effect of copper on osmoregulation in the freshwater amphipod Gammarus pulex. Comp. Biochem. Physiology - Part A Mol. Integr. Physiology 135 (2003), 527–537.
Cox, J., Hein, M.Y., Luber, C.A., Paron, I., Nagaraj, N., Mann, M., Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol. Cell. Proteomics MCP 13 (2014), 2513–2526.
de Oliveira, E.C., Lopes, R.M., Paumgartten, F.J.R., Comparative study on the susceptibility of freshwater species to copper-based pesticides. Chemosphere 56 (2004), 369–374.
De Schamphelaere, K.A.C., Forrez, I., Dierckens, K., Sorgeloos, P., Janssen, C.R., Chronic toxicity of dietary copper to Daphnia magna. Aquat. Toxicol. 81 (2007), 409–418.
Directive 2008/105/EC, Directive of the European Parliament and the Council of the European Union for environmental quality standards in the field of water policy (WFD). Official Journal of European Communities.
Ellington, W.R., Evolution and physiological roles of phosphagen systems. Annu. Rev. Physiology, 2001, 289–325.
Fechner, L.C., Versace, F., Gourlay-Francé, C., Tusseau-Vuillemin, M.H., Adaptation of copper community tolerance levels after biofilm transplantation in an urban river. Aquat. Toxicol. 106–107 (2012), 32–41.
Feckler, A., Thielsch, A., Schwenk, K., Schulz, R., Bundschuh, M., Differences in the sensitivity among cryptic lineages of the Gammarus fossarum complex. Sci. Total Environ. 439 (2012), 158–164.
Felten, V., Charmantier, G., Mons, R., Geffard, A., Rousselle, P., Coquery, M., Garric, J., Geffard, O., Physiological and behavioural responses of Gammarus pulex (Crustacea: Amphipoda) exposed to cadmium. Aquat. Toxicol. 86 (2008), 413–425.
Forbes, V.E., Palmqvist, A., Bach, L., The use and misuse of biomarkers in ecotoxicology. Environ. Toxicol. Chem. 25 (2006), 272–280.
Gaillardet, J., Viers, J., Dupré, B., Trace elements in river waters. Holland, H.D., Turekian, K.K., (eds.) Treatise on Geochemistry: Surface and Ground Water, Weathering, and Soils, 2004, Elsevier, Amsterdam, 225–272.
Geffard, A., Sartelet, H., Garric, J., Biagianti-Risbourg, S., Delahaut, L., Geffard, O., Subcellular compartmentalization of cadmium, nickel, and lead in Gammarus fossarum: comparison of methods. Chemosphere 78 (2010), 822–829.
Gismondi, E., Mazzucchelli, G., De Pauw, E., Joaquim-Justo, C., Thomé, J.P., Gender differences in responses in Gammarus pulex exposed to BDE-47: a gel-free proteomic approach. Ecotox. Environ. Safe 122 (2015), 205–213.
Gismondi, E., Rigaud, T., Beisel, J.-N., Cossu-Leguille, C., Effect of multiple parasitic infections on the tolerance to pollutant contamination. PLoS One, 7, 2012 e41950.
Gismondi, E., Thomé, J.P., Effects of two PBDE congeners on the moulting enzymes of the freshwater amphipod Gammarus pulex. Environ. Pollut. 191 (2014), 119–125.
Gismondi, E., Thomé, J.P., Transcriptome of the freshwater amphipod Gammarus pulex hepatopancreas. Genomics Data 8 (2016), 91–92.
Giusti, A., Leprince, P., Mazzucchelli, G., Thomé, J.-P., Lagadic, L., Ducrot, V., Joaquim-Justo, C., Proteomic analysis of the reproductive organs of the hermaphroditic gastropod Lymnaea stagnalis exposed to different endocrine disrupting chemicals. PLoS One, 8, 2013 e81086.
Grabner, D.S., Weigand, A.M., Leese, F., Winking, C., Hering, D., Tollrian, R., Sures, B., Invaders, natives and their enemies: distribution patterns of amphipods and their microsporidian parasites in the Ruhr Metropolis, Germany. Parasites vectors, 8, 2015, 419.
Hadji, R., Urien, N., Uher, E., Fechner, L.C., Lebrun, J.D., Contribution of aqueous and dietary uptakes to lead (Pb) bioaccumulation in Gammarus pulex: from multipathway modeling to in situ validation. Ecotox. Environ. Safe 129 (2016), 257–263.
Heckmann, L.-H., Sibly, R.M., Connon, R., Hooper, H.L., Hutchinson, T.H., Maund, S.J., Hill, C.J., Bouetard, A., Callaghan, A., Systems biology meets stress ecology: linking molecular and organismal stress responses in Daphnia magna. Genome Biol. 9 (2008), 1–14.
Jager, T., Barsi, A., Hamda, N.T., Martin, B.T., Zimmer, E.I., Ducrot, V., Dynamic energy budgets in population ecotoxicology: applications and outlook. Ecol. Model. 280 (2014), 140–147.
Jager, T., Hansen, B.H., Linking survival and biomarker responses over time. Environ. Toxicol. Chem. 32 (2013), 1842–1845.
Khan, F.R., Bury, N.R., Hogstrand, C., Copper and zinc detoxification in Gammarus pulex (L.). J. Exp. Biol. 215 (2012), 822–832.
Khan, F.R., Irving, J.R., Bury, N.R., Hogstrand, C., Differential tolerance of two Gammarus pulex populations transplanted from different metallogenic regions to a polymetal gradient. Aquat. Toxicol. 102 (2011), 95–103.
Lebrun, J.D., Perret, M., Geffard, A., Gourlay-Francé, C., Modelling copper bioaccumulation in Gammarus pulex and alterations of digestive metabolism. Ecotoxicology 21 (2012), 2022–2030.
Lebrun, J.D., Perret, M., Uher, E., Tusseau-Vuillemin, M.H., Gourlay-France, C., Waterborne nickel bioaccumulation in Gammarus pulex: comparison of mechanistic models and influence of water cationic composition. Aquat. Toxicol. 104 (2011), 161–167.
Lebrun, J.D., Uher, E., Tusseau-Vuillemin, M.-H., Gourlay-Francé, C., Essential metal contents in indigenous gammarids related to exposure levels at the river basin scale: metal-dependent models of bioaccumulation and geochemical correlations. Sci. Total Environ. 466–467 (2014), 100–108.
Leroy, D., Haubruge, E., De Pauw, E., Thome, J.P., Francis, F., Development of ecotoxicoproteomics on the freshwater amphipod Gammarus pulex: identification of PCB biomarkers in glycolysis and glutamate pathways. Ecotox. Environ. Safe 73 (2010), 343–352.
Maund, S.J., Taylor, E.J., Pascoe, D., Population responses of the freshwater amphipod crustacean Gammarus pulex (L.) to copper. Freshw. Biol. 28 (1992), 29–36.
Miyake, K., Tanaka, T., McNeil, P.L., Lectin-based food poisoning: a new mechanism of protein toxicity. PLoS One, 2, 2007 e687.
Muyssen, B.T.A., De Schamphelaere, K.A.C., Janssen, C.R., Mechanisms of chronic waterborne Zn toxicity in Daphnia magna. Aquat. Toxicol. 77 (2006), 393–401.
Paul, N., Chakraborty, S., Sengupta, M., Lead toxicity on non-specific immune mechanisms of freshwater fish Channa punctatus. Aquat. Toxicol. 152 (2014), 105–112.
Rainbow, P.S., Trace metal bioaccumulation: models, metabolic availability and toxicity. Environ. Intern. 33 (2007), 576–582.
Roussel, H., Chauvet, E., Bonzom, J.M., Alteration of leaf decomposition in copper-contaminated freshwater mesocosms. Environ. Toxicol. Chem. 27 (2008), 637–644.
Roussel, H., Ten-Hage, L., Joachim, S., Le Cohu, R., Gauthier, L., Bonzom, J.M., A long-term copper exposure on freshwater ecosystem using lotic mesocosms: primary producer community responses. Aquat. Toxicol. 81 (2007), 168–182.
Santos, E.M., Ball, J.S., Williams, T.D., Wu, H., Ortega, F., Van Aerle, R., Katsiadaki, I., Falciani, F., Viant, M.R., Chipman, J.K., Tyler, C.R., Identifying health impacts of exposure to copper using transcriptomics and metabolomics in a fish model. Environ. Sci. Technol. 44 (2010), 820–826.
Silvestre, F., Dierick, J.-F., Dumont, V., Dieu, M., Raes, M., Devos, P., Differential protein expression profiles in anterior gills of Eriocheir sinensis during acclimation to cadmium. Aquat. Toxicol. 76 (2006), 46–58.
Sricharoen, S., Kim, J.J., Tunkijjanukij, S., Söderhäll, I., Exocytosis and proteomic analysis of the vesicle content of granular hemocytes from a crayfish. Dev. Comp. Immunol. 29 (2005), 1017–1031.
Sroda, S., Cossu-Leguille, C., Effects of sublethal copper exposure on two gammarid species: which is the best competitor?. Ecotoxicology 20 (2011), 264–273.
Thevenot, D.R., Moilleron, R., Lestel, L., Gromaire, M.C., Rocher, V., Cambier, P., Bonte, P., Colin, J.L., de Ponteves, C., Meybeck, M., Critical budget of metal sources and pathways in the Seine River basin (1994-2003) for Cd, Cr, Cu, Hg, Ni, Pb and Zn. Sci. Total Environ. 375 (2007), 180–203.
Urien, N., Uher, E., Billoir, E., Geffard, O., Fechner, L.C., Lebrun, J.D., A biodynamic model predicting waterborne lead bioaccumulation in Gammarus pulex: influence of water chemistry and in situ validation. Environ. Pollut. 203 (2015), 22–30.
Vellinger, C., Gismondi, E., Felten, V., Rousselle, P., Mehennaoui, K., Parant, M., Usseglio-Polatera, P., Single and combined effects of cadmium and arsenate in Gammarus pulex (Crustacea, Amphipoda): understanding the links between physiological and behavioural responses. Aquat. Toxicol. 140–141 (2013), 106–116.
Vinot, I., Pihan, J.C., Circulation of copper in the biotic compartments of a freshwater dammed reservoir. Environ. Pollut. 133 (2005), 169–182.
Wang, Y., Li, E., Yu, N., Wang, X., Cai, C., Tang, B., Chen, L., Van Wormhoudt, A., Characterization and expression of glutamate dehydrogenase in response to acute salinity stress in the Chinese mitten crab, Eriocheir sinensis. PLoS One, 7, 2012 e37316.
Williams, T.D., Diab, A.M., George, S.G., Godfrey, R.E., Sabine, V., Conesa, A., Minchin, S.D., Watts, P.C., Chipman, J.K., Development of the GENIPOL European flounder (Platichthys flesus) microarray and determination of temporal transcriptional responses to cadmium at low dose. Environ. Sci. Technol. 40 (2006), 6479–6488.
Xuereb, B., Bezin, L., Chaumot, A., Budzinski, H., Augagneur, S., Tutundjian, R., Garric, J., Geffard, O., Vitellogenin-like gene expression in freshwater amphipod Gammarus fossarum (Koch, 1835): functional characterization in females and potential for use as an endocrine disruption biomarker in males. Ecotoxicology 20 (2011), 1286–1299.
Yang, J., Liu, D., Jing, W., Dahms, H.-U., Wang, L., Effects of cadmium on lipid storage and metabolism in the freshwater crab Sinopotamon henanense. PLoS One, 8, 2013 e77569.
Zubrod, J.P., Baudy, P., Schulz, R., Bundschuh, M., Effects of current-use fungicides and their mixtures on the feeding and survival of the key shredder Gammarus fossarum. Aquat. Toxicol. 150 (2014), 133–143.
Zubrod, J.P., Englert, D., Rosenfeldt, R.R., Wolfram, J., Lüderwald, S., Wallace, D., Schnetzer, N., Schulz, R., Bundschuh, M., The relative importance of diet-related and waterborne effects of copper for a leaf-shredding invertebrate. Environ. Pollut. 205 (2015), 16–22.
