Cadmium tolerance in seven Daphnia magna clones is associated with reduced hsp70 baseline levels and induction

Aquatic Toxicology

Volumn 94, Issue 2, 2009, Pages 131-137

  Haap, Timo ^a   Köhler, Heinz R ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Adaptation; Heat shock proteins; Heavy metals; Microevolution; Resistance

Indexed keywords

CADMIUM; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; HEAVY METAL;

ADAPTATION; BIOACCUMULATION; BIOASSAY; CADMIUM; CLONE; CRUSTACEAN; EVOLUTION; GENE EXPRESSION; IMMOBILIZATION; POLLUTION EFFECT; POLLUTION TOLERANCE; PROTEIN; TOXICOLOGY;

ARTICLE; BIOACCUMULATION; BIOGEOGRAPHIC REGION; CHEMOSENSITIVITY; CLONAL VARIATION; CLONE; DAPHNIA; IMMOBILIZATION; INVERTEBRATE; METAL TOLERANCE; NONHUMAN; PARTHENOGENESIS; POLLUTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; TOXICITY TESTING;

ANIMALS; CADMIUM; CLONE CELLS; DAPHNIA; ENVIRONMENTAL POLLUTANTS; HSP70 HEAT-SHOCK PROTEINS; TOXICITY TESTS;

DAPHNIA MAGNA; INVERTEBRATA;

EID: 68049135709     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2009.06.006     Document Type: Article

References (73)

1. Amiard J.C., Amiard-Triquet C., Barka S., Pellerin J., and Rainbow P.S. Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquat. Toxicol. 76 (2006) 160-202
2. Antunes S.C., Castro B.B., and Goncalves F. Chronic response of different clones of Daphnia longispina (field and ephippia) to different food levels. Acta Oecol. 24 1 (2003) 325-332
3. Arts M.-J.S.J., Schill R.O., Knigge T., Eckwert H., Kammenga J.E., and Köhler H.-R. Stress proteins (hsp70, hsp60) induced in isopods and nematodes by field exposure to metals in a gradient near Avonmouth, UK. Ecotoxicology 13 (2004) 739-755
4. Baird D.J., and Barata C. Genetic variation in the response of Daphnia to toxic substances: implications for risk assessment. In: Forbes V.E. (Ed). Genetics and Ecotoxicology (1998), Taylor and Francis, Ann Arbor 207-221
5. Baird D.J., Barber I., Bradley M., Soares A.M.V.M., and Calow P. A comparative study of genotype sensitivity to acute toxic stress using clones of Daphnia magna Straus. Ecotoxicol. Environ. Saf. 21 (1991) 257-265
6. Baird D.J., Soares A.M.V.M., Girling A., Barber M.C., and Calow P. The long term maintenance of Daphnia magna Straus for use in ecotoxicity tests: problems and prospects. In: Lokke H., Tyle H., and Bro-Rasmussen F. (Eds). Proceedings of the First European Conference on Ecotoxicology (1989), Lyngby, Denmark 144-148
7. Barata C., Baird D.J., Mitchell S.E., and Soares A.M.V.M. Among and within-population variability in tolerance to cadmium stress in natural populations of Daphnia magna: implications for ecological risk assessment. Environ. Toxicol. Chem. 21 (2002) 1058-1064
8. Barata C., Markich S.J., and Baird D.J. Influence of genetic and environmental factors on the tolerance of Daphnia magna Straus to essential and non-essential metals. Aquat. Toxicol. 42 (1998) 115-137
9. Bettencourt B.R., Feder F.E., and Cavicchi S. Experimental evolution of Hsp70 expression and thermotolerance in Drosophila melanogaster. Evolution 53 (1999) 1796-1801
10. Bettencourt B.R., Kim I.Y., Hoffmann A.A., and Feder M.E. Response to natural and laboratory selection at the Drosophila hsp70 genes. Evolution 56 (2002) 1796-1801
11. Bijlsma R., and Loeschcke V. Environmental stress, adaptation and evolution: an overview. J. Evol. Biol. 18 (2005) 744-749
12. Bond J.A., and Bradley B.P. Heat shock reduces the toxicity of malathion in Daphnia magna. Mar. Environ. Res. 39 (1995) 209-212
13. Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of protein, utilising the principle of protein-dye landing. Anal. Biochem. 72 (1976) 248-254
14. Brown D.C., Bradley B.P., and Tedengren M. Genetic and environmental regulation of hsp70 expression. Mar. Environ. Res. 39 (1995) 181-184
15. Declerck S., Cousyn C., and De Meester L. Evidence for local adaptation in neighbouring Daphnia populations: a laboratory transplant experiment. Freshwater Biol. 46 (2001) 187-198
16. Dietz T.J., and Somero G.N. Species- and tissue-specific synthesis patterns for heat-shock proteins HSP70 and HSP90 in several marine teleost fishes. Physiol. Zool. 66 (1994) 863-880
17. Eckwert H., and Köhler H.-R. The indicative value of the hsp70 stress response as a marker for metal effects in Oniscus asellus (Isopoda) field populations: variability between populations from metal-polluted and uncontaminated sites. Appl. Soil Ecol. 6 (1997) 275-282
18. Feder M.E., and Hofmann G.E. Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and ecological physiology. Annu. Rev. Physiol. 61 (1999) 243-282
19. Fraysse B., Geffard O., Berthet B., Quéau H., Biagianti-Risbourg S., and Geffard A. Importance of metallothioneins in the cadmium detoxification process in Daphnia magna. Comp. Biochem. Physiol. 144C (2006) 286-293
20. Guan R., and Wang W.-X. Comparison between two clones of Daphnia magna: Effects of multigenerational cadmium exposure on toxicity, individual fitness, and biokinetics. Aquat. Toxicol. 76 (2006) 217-229
21. Haap T., Triebskorn R., and Köhler H.-R. Acute effects of diclofenac and DMSO to Daphnia magna: immobilisation and hsp70 induction. Chemosphere 73 (2008) 353-359
22. Hairston Jr. N.G., Lampert W., Cáceres C.E., Holtmeier C.L., Weider L.J., Gaedke U., Fischer J.M., Fox J.A., and Prost D.M. Rapid evolution revealed by dormant eggs. Nature 401 (1999) 446
23. Hightower L. Heat shock, stress proteins, chaperones, and proteotoxicity. Cell 66 (1991) 191-197
24. Kammenga J.E., Dallinger R., Donker M.H., Köhler H.-R., Simonsen V., Triebskorn R., and Weeks J.M. Biomarkers in terrestrial invertebrates for ecotoxicological soil risk assessment. Rev. Environ. Contam. Toxicol. 164 (2000) 93-147
25. Ketola T., Laakso J., Kaitala V., and Airaksinen S. Evolution of Hsp90 expression in Tetrahymena thermophila (Protozoa, Ciliata) populations exposed to thermally variable environments. Evolution 58 (2004) 741-748
26. Klaassen C.D., Liu J., and Choudhuri S. Metallothionein: an intracellular protein to protect against cadmium toxicity. Annu. Rev. Pharmacol. Toxicol. 39 (1999) 267-294
27. Klerks P.L., and Weis J.S. Genetic adaptation to heavy metals in aquatic organisms: a review. Environ. Pollut. 45 (1987) 173-205
28. Knigge T., and Köhler H.-R. Lead impact on nutrition, energy reserves, respiration and stress protein (hsp70) level in Porcellio scaber (Isopoda) populations differently preconditioned in their habitats. Environ. Pollut. 108 (2000) 209-217
29. Köhler H.-R., Belitz B., Eckwert H., Adam R., Rahman B., and Trontelj P. Validation of hsp70 stress gene expression as a marker of metal effects in Deroceras reticulatum (Pulmonata): correlation with demographic parameters. Environ. Toxicol. Chem. 17 11 (1998) 2246-2253
30. Köhler H.-R., and Eckwert H. The induction of stress proteins (hsp) in Oniscus asellus (Isopoda) as a molecular marker of multiple heavy metal exposure. 2. Joint toxicity and transfer to field situations. Ecotoxicology 6 (1997) 263-274
31. Köhler H.-R., Eckwert H., Triebskorn R., and Bengtsson G. Interaction between tolerance and 70 kD stress protein (hsp70) induction in collembolan populations exposed to long-term metal pollution. Appl. Soil Ecol. 11 (1999) 43-52
32. Köhler H.-R., Triebskorn R., Stöcker W., Kloetzel P.-M., and Alberti G. The 70 kD heat shock protein (hsp70) in soil invertebrates: a possible tool for monitoring environmental toxicants. Arch. Environ. Contam. Toxicol. 22 (1992) 334-338
33. Köhler H.-R., Zanger M., Eckwert H., and Einfeldt I. Selection favours low Hsp70 levels in chronically metal-stressed soil arthropods. J. Evol. Biol. 13 (2000) 569-582
34. Krebs R.A., and Loeschcke V. Costs and benefits of activation of the heat-shock response in Drosophila melanogaster. Funct. Ecol. 8 (1994) 730-737
35. Kristensen T.N., Hoffmann A.A., Overgaard J., Sørensen J.G., Hallas R., and Loeschcke V. Costs and benefits of cold acclimation in field released Drosophila. Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 216-221
36. Lam P.K.S. Methods for distinguishing genetic and environmental variance in stress tolerance. Ecol. Appl. 9 (1999) 445-449
37. Lansing E., Justesen J., and Loeschcke V. Variation in the expression of Hsp70, the major heat-shock protein, and thermotolerance in larval and adult selection lines of Drosophila melanogaster. J. Therm. Biol. 25 (2000) 443-450
38. Lewis S., Donkin M.E., and Depledge M.H. Hsp70 expression in Enteromorpha intestinalis (Chlorophyta) exposed to environmental stressors. Aquat. Toxicol. 51 (2001) 277-291
39. Lindquist S. The heat shock response. Ann. Rev. Biochem. 55 (1986) 1151-1191
40. Lopes I., Baird D.J., and Ribeiro R. Genetic adaptation to metal stress by natural populations of Daphnia longispina. Ecotoxicol. Environ. Saf. 63 2 (2006) 275-285
41. Lopes I., Baird D.J., and Ribeiro R. Genetic determination of tolerance to lethal and sublethal copper concentrations in field populations of Daphnia longispina. Arch. Environ. Contam. Toxicol. 46 1 (2004) 43-51
42. Lynch M., and Gabriel W. Phenotypic evolution and parthenogenesis. Am. Nat. 122 (1983) 745-764
43. Morgan A.J., Kille P., and Stürzenbaum S. Microevolution and ecotoxicology of metals in invertebrates. Environ. Sci. Technol. 41 (2007) 1085-1096
44. OECD (Organisation for Economic Co-operation and Development), 2004. Guideline for Testing of Chemicals, 202, Daphnia sp., Acute Immobilisation Test. Environment Directorate OECD, Paris.
45. Parsell D.A., and Lindquist S. The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu. Rev. Genet. 27 (1993) 437-496
46. Pauwels K., Stoks R., and De Meester L. Coping with predator stress: interclonal differences in induction of heat-shock proteins in the water flea Daphnia magna. J. Evol. Biol. 18 (2005) 867-872
47. Pauwels K., Stoks R., Decaestecker E., and De Meester L. Evolution of heat shock protein expression in a natural population of Daphnia magna. Am. Nat. 170 (2007) 800-805
48. Pedersen S.N., Lundebye A.-K., and Depledge M.H. Field application of metallothionein and stress protein biomarkers in the shore crab (Carcinus maenas) exposed to trace metals. Aquat. Toxicol. 37 (1997) 183-200
49. Picado A., Chankova S., Fernandes A., Simões F., Leverett D., Johnson I., Hernan R., Pires A.M., and Matos J. Genetic variability in Daphnia magna and ecotoxicological evaluation. Ecotoxicol. Environ. Saf. 67 3 (2007) 406-410
50. Posthuma L., Hogervorst R.F., Joosse E.N.G., and Van Straalen N.M. Genetic variation and covariation for characteristics associated with cadmium tolerance in natural populations of the springtail Orchesella cincta. Evolution 47 (1993) 619-631
51. Poynton H.C., Varshavsky J.R., Chang B., Cavigiolio G., Chan S., Holman P.S., Loguinov A.V., Bauer D.J., Komachi K., Theil E.C., Perkins E.J., Hughes O., and Vulpe C.D. Daphnia magna ecotoxicogenomics provides mechanistic insights into metal toxicity. Environ. Sci. Technol. 41 (2007) 1044-1050
52. Radlowska M., and Pempkowiak J. Stress-70 as indicator of heavy metals accumulation in blue mussel Mytilus edulis. Environ. Int. 27 (2002) 605-608
53. Sanders B.M. Stress proteins in aquatic organisms: An environmental perspective. Crit. Rev. Toxicol. 23 (1993) 49-75
54. Sanders B.M., Hope C., Pascoe V.M., and Martin L.S. Characterization of the stress protein response in two species of Collisella limpets with different temperature tolerances. Physiol. Zool. 64 (1991) 1471-1489
55. Sanders B.M., and Martin L.S. Stress proteins as biomarkers of contaminant exposure in archived environmental samples. Sci. Total Environ. 139 (1993) 459-470
56. Soares A.M.V.M., Baird D.J., and Calow P. Interclonal variation in the performance of Daphnia-magna Straus in chronic bioassays. Environ. Toxicol. Chem. 11 10 (1992) 1477-1483
57. Sørensen J.G., Dahlgaard J., and Loeschcke V. Genetic variation in thermal tolerance among natural populations of Drosophila buzzatii: down regulation of Hsp70 expression and variation in heat stress resistance traits. Funct. Ecol. 15 (2001) 289-296
58. Sørensen J.G., Kristensen T.N., and Loeschcke V. The evolutionary and ecological role of heat shock proteins. Ecol. Lett. 6 (2003) 1025-1037
59. Sørensen J.G., and Loeschcke V. Natural adaptation to environmental stress via physiological clock-regulation of stress resistance in Drosophila. Ecol. Lett. 5 (2002) 16-19
60. Sørensen J.G., Michalak P., Justesen J., and Loeschcke V. Expression of the heat shock protein HSP70 in Drosophila buzzattii lines selected for thermal resistance. Hereditas 131 (1999) 155-164
61. Sørensen J.G., Norry F.M., Scannapieco A.C., and Loeschcke V. Altitudinal variation for stress resistant traits and thermal adaptation in adult Drosophila buzzatii from the New World. J. Evol. Biol. 18 (2005) 829-837
62. Spitze K. Chaoborus predation and life-history evolution in Daphnia pulex: temporal pattern of population diversity, fitness, and mean life history. Evolution 45 (1991) 82-92
63. Stuhlbacher A., Bradley M.C., Naylor C., and Calow P. Induction of cadmium tolerance in two clones of Daphnia magna Straus. Comp. Biochem. Physiol. 101C (1992) 571-577
64. Stuhlbacher A., Bradley M.C., Naylor C., and Calow P. Variation in the development of cadmium resistance in Daphnia magna Straus: effect of temperature, nutrition, age and genotype. Environ. Pollut. 80 (1993) 153-158
65. Tedengren M., Olsson B., Bradley B.P., and Zhou L. Heavy metal uptake, physiological response and survival of the blue mussel (Mytilus edulis) from marine and brackish waters in relation to the induction of heat-shock protein 70. Hydrobiologia 393 (1999) 261-269
66. Tedengren M., Olsson B., Reimer O., Brown D.C., and Bradley B.P. Heat pretreatment increases cadmium resistance and hsp70 levels in Baltic Sea mussels. Aquat. Toxicol. 48 (1999) 1-12
67. Triebskorn R., Köhler H.-R., Honnen W., Schramm M., Adams S.M., and Müller E.F. Induction of heat shock proteins, changes in liver ultrastructure, and alterations of fish behaviour: are these biomarkers related and are they useful to reflect the state of pollution in the field? J. Aquat. Ecosyst. Stress. Recov. 6 (1997) 57-73
68. Tsui M.T.K., and Wang W.X. Biokinetics and tolerance development of toxic metals in Daphnia magna. Environ. Toxicol. Chem. 26 5 (2007) 1023-1032
69. Veldhuizen-Tsoerkan M.B., Holwerda D.A., van der Maast C.A., and Zandee D.I. Effects of cadmium exposure and heat shock on protein synthesis in gill tissue of the sea mussel Mytilus edulis L. Comp. Biochem. Physiol. 96C (1990) 419-426
70. Warchalowska-Sliwa E., Niklinska M., Gorlich A., Michailova P., and Pyza E. Heavy metal accumulation, heat shock protein expression and cytogenetic changes in Tetrix tenuicornis (L.) (Tetrigidae, Orthoptera) from polluted areas. Environ. Pollut. 133 (2005) 373-381
71. Ward T.J., and Robinson E.R. Evolution of cadmium resistance in Daphnia magna. Environ. Toxicol. Chem. 24 9 (2005) 2341-2349
72. Weber A., and Declerck S. Phenotypic plasticity of Daphnia life history traits in response to predator kairomones: genetic variability and evolutionary potential. Hydrobiologia 360 (1997) 89-99
73. Zatsepina O.G., Velikodvorskaia V.V., Molodtsov V., Bettencourt B.R., Lerman D.N., Feder M.E., and Evgenev M.B. A Drosophila melanogaster strain from sub-equatorial Africa has exceptional thermotolerance but decreased Hsp70 expression. J. Exp. Biol. 204 (2001) 1869-1881