Metallic trace element body burdens and gene expression analysis of biomarker candidates in Eisenia fetida, using an "exposure/depuration" experimental scheme with field soils

Ecotoxicology and Environmental Safety

Volumn 73, Issue 5, 2010, Pages 1034-1045

  Bernard, Fabien ^a,b   Brulle, Franck ^a,b   Douay, Francis ^c   Lemière, Sébastien ^a,b   Demuynck, Sylvain ^a,b   Vandenbulcke, Franck ^a,b  

^a UNIV LILLE   (France)

^b Mines Douai   (France)

^c Groupe ISA   (France)

Author keywords

Detoxification; Earthworms; Gene expression; Microcosm study; Soil metallic contaminants

Indexed keywords

BIOLOGICAL MARKER; CADMIUM; CALCIUM; COATOSIN LIKE PROTEIN; COPPER; IRON; LEAD; LYSENIN; METALLOTHIONEIN; PHOSPHORUS; PHYTOCHELATIN SYNTHASE; TRACE METAL; UNCLASSIFIED DRUG; ZINC;

AGRICULTURAL SOIL; BIOACCUMULATION; CONCENTRATION (COMPOSITION); DETOXIFICATION; EARTHWORM; ECOTOXICOLOGY; GENE EXPRESSION; SMELTING; TOPSOIL; TRACE ELEMENT;

AGRICULTURAL LAND; ANIMAL EXPERIMENT; ANNELID WORM; ARTICLE; ATMOSPHERIC DISPERSION; BIOACCUMULATION; CONTROLLED STUDY; EARTHWORM; ECOTOXICOLOGY; EISENIA FOETIDA; GENE EXPRESSION PROFILING; LONG TERM EXPOSURE; LUMBRICUS RUBELLUS; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; SMELTER; SOIL POLLUTION; URBAN AREA;

AMINOACYLTRANSFERASES; ANIMALS; BIOLOGICAL MARKERS; BODY BURDEN; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL MONITORING; GENE EXPRESSION; METALLOTHIONEIN; METALS; OLIGOCHAETA; SOIL POLLUTANTS; TOXINS, BIOLOGICAL;

FRANCE;

ANNELIDA; EISENIA FETIDA; LUMBRICUS RUBELLUS;

EID: 77953537338     PISSN: 01476513     EISSN: 10902414     Source Type: Journal    
DOI: 10.1016/j.ecoenv.2010.01.010     Document Type: Article

References (72)

1. AFNOR, NF X31-107, 1983. Analyse granulométrique par sédimentation. Méthode à la pipette. In Qualité du sol. AFNOR, Paris, 15p.
2. AFNOR, NF ISO 10390, 1994. Détermination du pH. In Qualité du sol. AFNOR, Paris, 5p.
3. AFNOR, NF ISO 10693, 1995. Détermination de la teneur en carbonate. In Qualité du sol. AFNOR, Paris, 1995, 7p.
4. AFNOR, NF ISO 10694, 1995. Dosage du carbone organique et du carbone total après combustion sèche. In Qualité du sol. AFNOR, Paris, 7p.
5. AFNOR, NF X 31-147, 1996. Sols, sédiments. Mise en solution totale par attaque acide. In Qualité du sol. AFNOR, Paris, 12p.
6. Albani J.R., Demuynck S., Grumiaux F., Leprĉtre A. Fluorescence fingerprintings of Eisenia fetida and Eisenia andrei. Photochem. Photobiol. 2003, 9:165-173.
7. Arukwe A. Toxciological housekeeping genes: do they really keep the house?. Environ. Sci. Technol. 2006, 40:7944-7949.
8. Brousseau P., Fugère N., Bernier J., Coderre D., Nadeau D., Poirier G., Fournier M. Evaluation of earthworm exposure to contaminated soil by cytometric assay of coelomocytes phagocytosis in Lumbricus trerrestris (Oligochaeta). Soil Biol. Biochem. 1997, 29:681-684.
9. Brulle F., Mitta G., Cocquerelle C., Vieau D., Lemière S., Leprĉtre A., Vandenbulcke F. Cloning and Real-Time PCR testing of 14 potential biomarkers in Eisenia fetida following cadmium exposure. Environ. Sci. Technol. 2006, 40:2844-2850.
10. Brulle F., Mitta G., Leroux R., Lemière S., Leprĉtre A., Vandenbulcke F. The strong induction of metallothionein gene following cadmium exposure transiently affects the expression of many genes in Eisenia fetida: a trade-off mechanism?. Comp. Biochem. Phys. C. 2007, 144:334-341.
11. Brulle F., Cocquerelle C., Wamalah A.N., Morgan A.J., Kille P., Leprĉtre A., Vandenbulcke F. cDNA cloning and expression analysis of Eisenia fetida (Annelida; Oligochaeta) phytochelatin synthase under cadmium exposure. Ecotox. Environ. Safe. 2008, 71:47-55.
12. Brulle F., Cocquerelle C., Mitta G., Castric V., Douay F., Leprĉtre A., Vandenbulcke F. Identification and expression profile of gene transcripts differentially expressed during metallic exposure in Eisenia fetida cœlomocytes. Dev. Comp. Immunol. 2008, 32:1441-1453.
13. Chabicovsky M., Niederstätter H., Thaler R., Hödl E., Parson W., Rossmanith W., Dallinger R. Localization and quantification of Cd- and Cu-specific metallothionein isoform mRNA in cells and organs of the terrestrial gastropod Helix pomatia. Toxicol. Appl. Pharm. 2003, 190:25-36.
14. Cholewa J., Feeney G.P., O'Reilly M., Stürzenbaum S.R., Morgan A.J., Plytycz B. Autofluorescence in eleocytes of some earthworm species. Folia Histochem. Cytobiol. 2006, 44:65-71.
15. Chung S., Kim M., Choi W.-J., Chung J.-K., Lee K. Expression of translationally controlled tumor protein mRNA in human colon cancer. Cancer Lett. 2000, 156:185-190.
16. Clemens S., Kim E.J., Neumann D., Schroeder J.I. Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J. 1999, 18:3325-3333.
17. Clemens S., Schroeder J.I., Degenkolb T. Caenorhabditis elegans expresses a functional phytochelatin synthase. Eur. J. Biochem. 2001, 268:3640-3643.
18. Clemens S. Evolution and function of phytochelatin synthases. J. Plant. Physiol. 2006, 163:319-332.
19. Demuynck S., Grumiaux F., Descamps M., Leprĉtre A. Differential expression of stress proteins in response to heat and cadmium in two oligochaete species Eisenia fetida and E. Andrei. Trends Comp. Biochem. Physiol. 2005, 10:105-110.
20. Demuynck S., Grumiaux F., Mottier V., Schikorski D., Leprĉtre A. Metallothionein response following cadmium exposure in the oligochaete species Eisenia fetida. Comp. Biochem. Phys. C. 2006, 144:34-46.
21. Demuynck S., Grumiaux F., Mottier V., Schikorski D., Lemiere S., Leprĉtre A. Cd/Zn exposure interactions on metallothionein response in Eisenia fetida (Annelida, Oligochaeta). Comp. Biochem. Phys. C. 2007, 145:658-668.
22. Dickinson N.M., Turner A.P., Watmough S.A., Lepp N.W. Acclimation of trees to pollution stress: cellular metal tolerance traits. Ann. Bot. 1992, 70:569-572.
23. Doran J.W., Safley M. Defining and assessing soil health and sustainable productivity. Biological Indicators of Soil Health 1997, 1-28. CAB International. C.E. Pankhurst (Ed.).
24. Douay F., Pruvost C., Waterlot C., Fritsch C., Fourrier H., Loriette A., Bidar G., Grand C., de Vaufleury A., Scheifler R. Contamination of woody habitat soils around a former lead smelter in the North of France. Sci. Total Environ. 2009, 407:5564-5577.
25. Doucet J., Provost P., Samuelsson B., Radmark O. Molecular cloning and functional characterization of mouse coactosin-like protein. Biochem. Biophys. Res. C. 2002, 290:783-789.
26. Galay-Burgos M., Winters C., Stürzenbaum S.R., Randerson P.F., Kille P., Morgan A.J. Cu and Cd effects on the earthworm Lumbricus rubellus in the laboratory: multivariate statistical analysis of relationships between exposure, biomarkers, and ecologically relevant parameters. Environ. Sci. Technol. 2005, 39:1757-1763.
27. Grill E., Winnacker E.L., Zenk M.H. Phytochelatins: the principal heavy-metal complexing peptides of higher plants. Science 1985, 230:674-676.
28. Gruber C., Stürzenbaum S.R., Gehrig P., Sack R., Hunziker P., Berger B., Dallinger R. Isolation and characterization of a self-sufficient one-domain protein (Cd)-metallothionein from Eisenia foetida. Eur. J. Biochem. 2000, 267:573-582.
29. Ha S.-B., Smith A.P., Howden R., Dietrich W.M., Bugg S., O'Connell M.J. Phytochelatin synthase genes from arabidopsis and the yeast schizosaccharomyces pombe. Plant Cell 1999, 11:1153-1163.
30. Hall J.L. Cellular mechanisms for heavy metal detoxification and tolerance. J. Exp. Bot. 2002, 53:1-11.
31. Hendawi M., Sauvé S., Ashour M., Brousseau P., Fournier M. A new ultrasond protocol for extrusion of coelomocyte cells from the earthworm Eisenia fetida. Ecotox. Environ. Safe. 2004, 59:17-22.
32. Hughes S.L., Bundy J.G., Want E.J., Kille P., Stürzenbaum S.R. The metabolomic responses of Caenorhabditis elegans to cadmium are largely independent of metallothionein status, but dominated by changes in cystathionine and phytochelatins. J. Proteome Res. 2009, 8:3512-3519.
33. Janssens T.K.S., Del Rio Lopez R., Mariën J., Timmermans M.J.T.N., Montagne-Wajer K., Van Straalen N.M., Roelofs D. Comparative population analysis of metallothionein promoter alleles suggests stress-induced microevolution in the field. Environ. Sci. Technol. 2008, 42:3873-3878.
34. Klaassen C.D., Liu J., Choudhuri S. Metallothionein: an intracellular protein to protect against cadmium toxicity. Annu. Rev. Pharmacol. 1999, 39:267-294.
35. Kobayashi H., Sekiwaza Y., Aizu M., Umeda M. Lethal and non-lethal responses of spermatozoa from a wide variety of vertebrates and invertebrates to lysenin, a protein from the coelomic fluid of the earthworm Eisenia fetida. J. Biol. Chem. 2000, 286:538-549.
36. Langdon C.J., Morgan A.J., Charnock J.M., Semple K.T., Lowe C.N. As-resistance in laboratory-reared F1, F2 and F3 generation offspring of the earthworm Lumbricus rubellus inhabiting an As-contaminated mine soil. Environ. Pollut. 2009, 157:3114-3119.
37. Laszczyca P., Augustyniak M., Babczynska A., Bednarska K., Kafel A., Migula P., Wilczek G., Witas I. Profiles of enzymatic activity in earthworms from zinc, lead and cadmium polluted areas near Olkusz (Poland). Environ. Int. 2004, 30:901-910.
38. Manios T., Stentiford E.I., Millner P.A. The effect of heavy metals accumulation on the chlorophyll concentration of Typha latifolia plants, growing in a substrate containing sewage sludge compost and watered with metaliferus water. Ecol. Eng. 2003, 20:65-74.
39. Morgan A.J., Stürzenbaum S.R., Winters C., Kille P. Cellular and molecular aspects of metal sequestration and toxicity in earthworms. Invertebr. Repr. Dev. 1999, 36:17-24.
40. Morgan A.J., Turner M.P., Morgan J.E. Morphological plasticity in metal-sequestering earthworm chloragocytes: Morphometric electron microscopy provides a biomarker of exposure in field populations. Environ. Toxicol. Chem. 2002, 21:610-618.
41. Morgan A.J., Kille P., Stürzenbaum S.R. Microevolution and ecotoxicology of metals in invertebrates. Environ. Sci. Technol. 2007, 41:1085-1096.
42. Novozamsky J., Lexmond T.M., Houba V.J.G. A single extraction procedure of soil for evaluation of uptake of some heavy metals by plants. Int. J. Environ. Anal. Chem. 1993, 51:47-58.
43. Ohta N., Shioda S., Sekizawa Y., Nakai Y., Kobayashi H. Sites of expression of mRNA for lysenin, a protein isolated from the coelomic fluid of the earthworm Eisenia fetida. Cell Tissue Res. 2000, 302:263-270.
44. Owen J., Hedley B.A., Svendsen C., Wren J., Jonker M.J., Hankard P., Lister J.L., Stürzenbaum S.R., Morgan A.J., Spurgeon D.J., Blaxter M.L., Kille P. Transcriptome profiling of developmental and xenobiotic responses in a keystone soil animal, the oligochaete annelid Lumbricus rubellus. BMC Genomics. 2008, 9. art. no. 266.
45. Palmiter R.D. The elusive function of metallothioneins. P. Natl. Acad. Sci. USA. 1998, 95:8428-8430.
46. Peijnenburg W.J.G.M., Posthuma L., Eijsackers H.J.P., Allen H.E. A conceptual framework for implementation of bioavailability of metals for environmental management purposes. Ecotox. Environ. Safe. 1997, 37:163-172.
47. Plytycz B., Lis-Molenda U., Cygal M., Kielbasa E., Grebosz A., Duchnowski M., Andre J., Morgan A.J. Riboflavin content of coelomocytes in earthworm (Dendrodrilus rubidus) field populations as a molecular biomarker of soil metal pollution. Environ. Pollut. 2009, 157:3042-3050.
48. Prochazkova P., Silerova M., Felsberg J., Joskova R., Beschin A., De Baetselier P., Bilej M. Relationship between hemolytic molecules in Eisenia fetida earthworms. Dev. Comp. Immunol. 2006, 30:381-392.
49. Raab A., Feldmann J., Meharg A.A. The nature of arsenic-phytochelatin complexes in Holcus lanatus and Pteris cretica. Plant Physiol. 2004, 134:1113-1122.
50. Rakonjac M., Fischer L., Provost P., Werz O., Steinhilber D., Samuelsson B., Radmark O. Coactosin-like protein supports 5-lipoxygenase enzyme activity and up-regulates leukotriene A4 production. P. Natl. Acad. Sci. USA 2006, 103:13150-13155.
51. Rea P.A., Vatamaniuk O.K., Rigden D.J. Weeds, worms, and more. Papain's long-lost cousin, phytochelatin synthase. Plant Physiol. 2004, 136:2463-2474.
52. Ricketts H.J., Morgan A.J., Spurgeon D.J., Kille P. Measurement of annetocin gene expression: a new reproductive biomarker in eartworm ecotoxicology. Ecotox. Environ. Safe. 2004, 57:4-10.
53. Roch P., Canicatti C., Valembois P. Interactions between earthworm hemolysis and sheep red blood cell membranes. Biochim. Biophys. Acta-Biomembranes 1989, 983:193-198.
54. Roelofs D., Overhein L., de Boer M.E., Janssens T.K.S., Van Straalen N.M. Additive genetic variation of transcriptional regulation: metallothionein expression in the soil insect Orchesella cincta. Heredity 2006, 96:85-92.
55. Rozen A. Effect of Cd on life history parameters in Dendrobaena octaedra (Lumbricidae:Oligocheta) populations originating from forests differently polluted with heavy metals. Soil Biol. Biochem. 2006, 38:489-503.
56. Sauvé S., Fournier M. Age-specific immunocompetence of the earthworm Eisenia andrei: exposure to methylmercury chloride. Ecotox. Environ. Safe. 2005, 60:67-72.
57. Spurgeon D.J., Hopkin S.P. Effects of metal- contaminated soils on the growth, sexual development, and early cocoon production of the earthworm Eisenia fetida, with particular reference to zinc. Ecotox. Environ. Safe. 1996, 35:86-95.
58. Spurgeon D.J., Hopkin S.P. Tolerance to zinc in populations of the earthworms Lumbricus rubellus from uncontaminated and metal-contaminated ecosystems. Environ. Contam. Toxicol. 1999, 37:332-337.
59. Spurgeon D.J., Hopkin S.P. Comparisons of metal accumulation and excretion kinetics in earthworms (Eisenia fetida) exposed to contaminated field and laboratory soils. Appl. Soil Ecol. 1999, 11:227-243.
60. Sterckeman T., Douay F., Proix F., Fourrier H., Perdrix E. Assessment of the contamination of cultivated soils by eighteen trace elements around smelters in the North of France. Water Air Soil Pollut. 2002, 135:173-194.
61. Stone D., Jepson P., Kramarz P., Laskowski R. Time to death response in carabid beetles exposed to multiple stressors along a gradient of heavy metal pollution. Environ. Pollut. 2001, 113:239-244.
62. Stürzenbaum S.R., Kille P., Morgan A.J. Identification of heavy metal induced changes in the expression patterns of the translationally controlled tumour protein (TCTP) in the earthworm Lumbricus rubellus. Biochim. Biophys. Acta. 1998, 1398:294-304.
63. Stürzenbaum S.R., Winters C., Galay M., Morgan A.J., Kille P. Metal ion trafficking in earthworms. Identification of a cadmium-specific metallothionein. J. Biol. Chem. 2001, 276:34013-34018.
64. Stürzenbaum S.R., Kille P. Control genes in quantitative molecular biological techniques: the variability of invariance. Comp. Biochem. Phys. B. 2001, 130:281-289.
65. Stürzenbaum S.R., Parkinson J., Blaxter M., Morgan A.J., Kille P. The earthworm expressed sequence tag project. Pedobiologia 2003, 47:447-451.
66. Timmermans M.J.T.N., Ellers J., Roelofs D., van Straalen N.M. Metallothionein mRNA expression and cadmium tolerance in metal-stressed and reference populations of the springtail Orchesella cincta. Ecotoxicology 2005, 14:727-739.
67. Timmermans M.J.T.N., Ellers J., van Straalen N.M. Allelic diversity of metallothionein in Orchesella cincta (L.): traces of natural selection by environmental pollution. Heredity 2007, 98:311-319.
68. Vatamaniuk O.K., Bucher E.A., Ward J.T., Rea P.A. A new pathway for heavy metal detoxification in animals. phytochelatin synthase is required for cadmium tolerance in Caenorhabditis elegans. J. Biol. Chem. 2001, 276:20817-20820.
69. Veltman K., Huijbregts M.A.J., Vijver M.G., Peijnenburg W.J.G.M., Hobbelen P.H.F., Koolhaas J.E., van Gestel C.A.M., van Vliet P.C.J., Hendriks A.J. Metal accumulation in the earthworm Lumbricus rubellus. Model predictions compared to field data. Environ. Pollut. 2007, 146:428-436.
70. Yamaji-Hasegawa A., Makino A., Baba T., Senoh Y., Kimura-Suda H., Sato S.B., Terada N., Kiyokawa E., Umeda M., Kobayashi T. Oligomerization and pore formation of a sphingomyelin-specific toxin, lysenin. J. Biol. Chem. 2003, 278:22762-22770.
71. Yamaji A., Sekizawa Y., Emoto K., Sakuraba H., Inoue K., Kobayashi H., Umeda M. Lysenin, a novel sphingomyelin-specific binding protein. J. Biol. Chem. 1998, 273:5300-5306.
72. Zhang H., Xu W., Guo J., He Z., Ma M. Coordinated responses of phytochelatins and metallothioneins to heavy metals in garlic seedlings. Plant Sci. 2005, 169:1059-1065.