Using biomarkers in an evolutionary context: Lessons from the analysis of biological responses of oligochaete annelids to metal exposure

Environmental Pollution

Volumn 179, Issue , 2013, Pages 343-350

  Pauwels, Maxime ^a   Frérot, Hélène ^a   Souleman, Dima ^a   Vandenbulcke, Franck ^a  

^a UNIV LILLE   (France)

Author keywords

Biomarker; Earthworms; Gene expression; Local adaptation; Metal pollution

Indexed keywords

GENE EXPRESSION; POLLUTION; SOIL POLLUTION;

ANTHROPOGENIC ACTIVITY; BIOLOGICAL MODIFICATION; BIOLOGICAL ORGANIZATION; EARTHWORMS; ENVIRONMENTAL EXPOSURE; LABORATORY CONDITIONS; LOCAL ADAPTATION; METAL POLLUTION;

BIOMARKERS;

BIOLOGICAL MARKER; TRACE ELEMENT; TRANSCRIPTOME; METAL;

BIOMARKER; EARTHWORM; GENE EXPRESSION; LOCAL ADAPTATION; METAL; PHYSIOLOGICAL RESPONSE; POLLUTION EXPOSURE; SOIL POLLUTION;

ANNELID; BIOLOGICAL ACTIVITY; ECOTOXICOLOGY; EISENIA ANDREI; EISENIA FETIDA; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL IMPACT ASSESSMENT; ENVIRONMENTAL STRESS; GENETIC VARIABILITY; LOCAL ADAPTATION; LUMBRICUS RUBELLUS; NONHUMAN; REVIEW; SOIL POLLUTION; TRANSCRIPTOMICS; ANIMAL; ENVIRONMENTAL MONITORING; EVOLUTION; METABOLISM; METHODOLOGY; OLIGOCHAETA; PHYSIOLOGY; SOIL POLLUTANT;

ANNELIDA; LUMBRICIDAE;

ANIMALS; BIOLOGICAL EVOLUTION; BIOLOGICAL MARKERS; ENVIRONMENTAL MONITORING; METALS; OLIGOCHAETA; SOIL POLLUTANTS;

EID: 84887216812     PISSN: 02697491     EISSN: 18736424     Source Type: Journal    
DOI: 10.1016/j.envpol.2013.05.005     Document Type: Review

References (93)

1. Anderson, C.J., Kille, P., Lawlor, A.J., Spurgeon, D.J., 2013. Life-history effects of arsenic toxicity in clades of the earthworm Lumbricus rubellus. Environmental Pollution 172, 200-207.
2. Arnold, R.E., Hodson, M.E., Langdon, C.J., 2008. A Cu tolerant population of the earthworm Dendrodrilus rubidus (Savigny, 1862) at Coniston Copper Mines, Cumbria, UK. Environmental Pollution 152, 713-722. (Pubitemid 351442816)
3. Baird, S.K., Kurz, T., Brunk, U.T., 2006. Metallothionein protects against oxidative stress-induced lysosomal destabilization. Biochemical Journal 394, 275-283. (Pubitemid 43259678)
4. Barrett, R.D.H., Hoekstra, H.E., 2011. Molecular spandrels: tests of adaptation at the genetic level. Nature Reviews Genetics 12 (11), 767-780.
5. Beattie, J.H., Owen, H.L.H., Wallace, S.M., Arthur, J.R., Kwun, I.S., Hawksworth, G.M., Wallace, H.M., 2005. Metallothionein overexpression and resistance to toxic stress. Toxicology Letters 157, 69-78. (Pubitemid 40410614)
6. Beeby, A., 2001. What do sentinels stand for? Environmental Pollution 112, 285-298. (Pubitemid 33592964)
7. Bickham, J.W., 2011. The four cornerstones of evolutionary toxicology. Ecotoxicology 20, 497-502.
8. Bouché, M.B., 1992. Earthworm species and ecotoxicological studies. In: Greig-Smith, P.W., Becker, H., Edwards, P.J., Heimbach, F. (Eds.), Ecotoxicology of Earthworms. Intercept Press, Andover.
9. Bradl, H., 2005. In: Hubbard, A. (Ed.), Heavy Metals in the Environment: Origin, Interaction and Remediation. Interface Science and Technology. Elsevier, Academic Press, Neubrucke, Germany.
10. Brulle, F., Cocquerelle, C., Mitta, G., Castric, V., Douay, F., Leprêtre, A., Vandenbulcke, F., 2008. Identification and expression profile of gene transcripts differentially expressed during metallic exposure in Eisenia fetida coelomocytes. Developmental and Comparative Immunology 32, 1441-1453.
11. Brulle, F., Mitta, G., Cocquerelle, C., Vieau, D., Lemière, S., Leprêtre, A., Vandenbulcke, F., 2006. Cloning and real-time PCR testing of 14 potential biomarkers in Eisenia fetida following cadmium exposure. Environmental Science & Technology 40, 2844-2850.
12. Brulle, F., Morgan, A.J., Cocquerelle, C., Vandenbulcke, F., 2010. Transcriptomic underpinning of toxicant-mediated physiological function alterations in three terrestrial invertebrate taxa: a review. Environmental Pollution 158, 2793-2808.
13. Calisi, A., Lionetto, M.G., Schettino, T., 2009. Pollutant-induced alterations of granulocyte morphology in the earthworm Eisenia foetida. Ecotoxicology and Environmental Safety 72, 1369-1377.
14. Calisi, A., Lionetto, M.G., Schettino, T., 2011. Biomarker response in the earthworm Lumbricus terrestris exposed to chemical pollutants. Science of The Total Environment 409, 4456-4464.
15. Capowiez, Y., Bérard, A., 2006. Assessment of the effects of imidacloprid on the behavior of two earthworm species (Aporrectodea nocturna and Allolobophora chlorotica) using 2D terraria. Ecotoxicology and Environmental Safety 64, 198-206. (Pubitemid 43786270)
16. Capowiez, Y., Rault, M., Mazzia, C., Belzunces, L., 2003. Earthworm behaviour as a source of biomarkers - a study case with imidacloprid. Pedobiologia 47, 542-547. (Pubitemid 38097840)
17. Christensen, O., 1988. Lumbricid earthworms as bio-indicators relative to soil factors in different agro-ecosystems. Advances in Management and Conservation of Soil Fauna, 839-849.
18. Clements, W.H., Rohr, J.R., 2009. Community responses to contaminants: using basic ecological principles to predict ecotoxicological effects. Environmental Toxicology and Chemistry 28, 1789-1800.
19. Costa, D., Mariën, J., Janssens, T., van Gestel, C., Driessen, G., Sousa, J., van Straalen, N., Roelofs, D., 2012. Influence of adaptive evolution of cadmium tolerance on neutral and functional genetic variation in Orchesella cincta. Ecotoxicology 21, 2078-2087.
20. Cotrufo, M.F., De Santo, A.V., Alfani, A., Bartoli, G., De Cristofaro, A., 1995. Effects of urban heavy metal pollution on organic matter decomposition in Quercus ilex L. Woods. Environmental Pollution 89, 81-87.
21. Coutellec, M.A., Barata, C., 2011. An introduction to evolutionary processes in ecotoxicology. Ecotoxicology 20 (3), 493-496.
22. Demuynck, S., Grumiaux, F., Descamps, M., Leprêtre, A., 2005. Differential expression of stress protein in response to heat and cadmium in two oligochaete species Eisenia fetida and Eisenia andrei. Trends in Comparative Biochemistry & Physiology 10, 105-110.
23. Demuynck, S., Grumiaux, F., Mottier, V., Schikorski, D., Lemière, S., Leprêtre, A., 2006. Metallothionein response following cadmium exposure in the oligochaete Eisenia fetida. Comparative Biochemistry and Physiology - C Toxicology and Pharmacology 144, 34-46.
24. Demuynck, S., Grumiaux, F., Mottier, V., Schikorski, D., Lemière, S., Leprêtre, A., 2007. Cd/Zn exposure interactions on metallothionein response in Eisenia fetida (Annelida, Oligochaeta). Comparative Biochemistry and Physiology - C Toxicology and Pharmacology 145, 658-668.
25. Dickinson, N.M., Turner, A.P., Watmough, S.A., Lepp, N.W., 1992. Acclimation of trees to pollution stress: cellular metal tolerance traits. Annals of Botany 70, 569-572.
26. Dupont, L., 2009. Perspectives on the application of molecular genetics to earthworm ecology. Pedobiologia 52, 191-205.
27. Edwards, C.A., 1998. Earthworm Ecology. Soil and Water Conservation Society, St. Lucie Press, Iowa.
28. Edwards, C.A., Bohlen, P.J., 1996. Biology and Ecology of Earthworms, third ed. Chapman & Hall, London.
29. Ernst, G., Zimmermann, S., Christie, P., Frey, B., 2008. Mercury, cadmium and lead concentrations in different ecophysiological groups of earthworms in forest soils. Environmental Pollution 156, 1304-1313.
30. Fisker, K., Sørensen, J., Damgaard, C., Pedersen, K., Holmstrup, M., 2011. Genetic adaptation of earthworms to copper pollution: is adaptation associated with fitness costs in Dendrobaena octaedra? Ecotoxicology 20, 563-573.
31. Fourie, F., Reinecke, S.A., Reinecke, A.J., 2007. The determination of earthworm species sensitivity differences to cadmium genotoxicity using the comet assay. Ecotoxicology and Environmental Safety 67, 361-368. (Pubitemid 46836733)
32. Fründ, H.C., Butt, K., Capowiez, Y., Eisenhauer, N., Emmerling, C., Ernst, G., Potthoff, M., Schadler, M., Schrader, S., 2010. Using earthworms as model organisms in the laboratory: recommendations for experimental implementations. Pedobiologia 53, 119-125.
33. Ghalambor, C.K., McKay, J.K., Carroll, S.P., Reznick, D.N., 2007. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology 21, 394-407. (Pubitemid 46802146)
34. Ghoshal, K., Wang, Y., Sheridan, J.F., Jacob, S.T., 1998. Metallothionein induction in response to restraint stress. Transcriptional control, adaptation to stress, and role of glucocorticoid. Journal of Biological Chemistry 273, 27904-27910. (Pubitemid 28496079)
35. Gruber, C., Stürzenbaum, S., Gehrig, P., Sack, R., Hunziker, P., Berger, B., Dallinger, R., 2000. Isolation and characterization of a self-sufficient one-domain protein. (Cd)-Metallothionein from Eisenia foetida. European Journal of Biochemistry 267, 573-582. (Pubitemid 30072917)
36. Hendry, A.P., Kinnison, M.T., Heino, M., Day, T., Smith, T.B., Fitt, G., Bergstrom, C.T., Oakeshott, J., Jorgensen, P.S., Zalucki, M.P., Gilchrist, G., Southerton, S., Sih, A., Strauss, S., Denison, R.F., Carroll, S.P., 2011. Evolutionary principles and their practical application. Evolutionary Applications 4 (2), 159-183.
37. Hopkin, S.P., 1989. Ecophysiology of Metals in Terrestrial Invertebrates. Elsevier Applied Science, London.
38. ISO (International Organisation for Standardization) 17512-1, 2008. Soil Quality - Avoidance Test for Determining the Quality of Soils and Effects of Chemicals on Behaviour - Part 1: Test with Earthworms (Eisenia fetida and Eisenia andrei).
39. James, S.W., Porco, D., Decaens, T., Richard, B., Rougerie, R., Erseus, C., 2010. DNA barcoding reveals cryptic diversity in Lumbricus terrestris L., 1758 (Clitellata): resurrection of L. herculeus (Savigny, 1826). PLoS ONE 5, e15629.
40. Janssens, T.K.S., Lopez, R.D.R., Marien, J., Timmermans, M., Montagne-Wajer, K., Van Straalen, N.M., Roelofs, D., 2008. Comparative population analysis of metallothionein promoter alleles suggests stress-induced microevolution in the field. Environmental Science & Technology 42, 3873-3878. (Pubitemid 351694107)
41. Kaegi, J.H.R., 1993. Evolution, structure and chemical activity of class I metallothioneins: an overview. Metallothionein III, 29-55.
42. Kautenburger, R., 2006. Impact of different agricultural practices on the genetic structure of Lumbricus terrestris, Arion lusitanicus and Microtus arvalis. Animal Biodiversity and Conservation 29, 19-32. (Pubitemid 44144911)
43. Kawecki, T.J., Ebert, D., 2004. Conceptual issues in local adaptation. Ecology Letters 7 (12), 1225-1241. (Pubitemid 39588356)
44. Klaassen, C.D., Liu, J., Choudhuri, S., 1999. Metallothionein: an intracellular protein to protect against cadmium toxicity. Annual Review of Pharmacology and Toxicology 39, 267-294. (Pubitemid 29222560)
45. Kozlov, M.V., Zvereva, E.L., 2011. A second life for old data: global patterns in pollution ecology revealed from published observational studies. Environmental Pollution 159, 1067-1075.
46. Langdon, C.J., Morgan, A.J., Charnock, J.M., Semple, K.T., Lowe, C.N., 2009. As-resistance in laboratory-reared F1, F2 and F3 generation offspring of the earthworm Lumbricus rubellus inhabiting an As-contaminated mine soil. Environmental Pollution 157, 3114-3119.
47. Lavelle, P., Spain, A.V., 2001. Soil Ecology. Kluwer Academic Publishers, Dordrecht, Spain.
48. Liao, V.H.C., Freedman, J.H., 1999. Cadmium-regulated genes from the nematode Caenorhabditis elegans: identification and cloning of new cadmium-responsive genes by differential display. Journal of Biological Chemistry 273, 31962-31970.
49. Lowe, C.N., Butt, K.R., 2007a. Life-cycle traits of the dimorphic earthworm species Allolobophora chlorotica (Savigny, 1826) under controlled laboratory conditions. Biology and Fertility of Soils 43, 495-499.
50. Lowe, C.N., Butt, K.R., 2007b. Culture of commercially obtained Lumbricus terrestris L.: implications for sub-lethal ecotoxicological testing. Soil Biology and Biochemistry 39 (7), 1674-1679. (Pubitemid 46617660)
51. Lowe, C.N., Butt, K.R., 2007c. Earthworm culture, maintenance and species selection in chronic ecotoxicological studies: a critical review. European Journal of Soil Biology 43, S281-S288. (Pubitemid 350137845)
52. Lukkari, T., Taavitsainen, M., Väisänen, A., Haimi, J., 2004. Effects of heavy metals on earthworms along contamination gradients in organic rich soils. Ecotoxicology and Environmental Safety 59, 340-348. (Pubitemid 39243976)
53. Manios, T., Stentiford, E.I., Millner, P.A., 2003. 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. Ecological Engineering 20, 65-74. (Pubitemid 36614699)
54. Marhan, S., Scheu, S., 2005. The influence of mineral and organic fertilisers on the growth of the endogeic earthworm Octolasion tyrtaeum (Savigny). Pedobiologia 49, 239-249. (Pubitemid 40697292)
55. Medina, M.H., Correa, J.A., Barata, C., 2007. Micro-evolution due to pollution: possible consequences for ecosystem responses to toxic stress. Chemosphere 67, 2105-2114. (Pubitemid 46463929)
56. Moffett, B.F., Nicholson, F.A., Uwakwe, N.C., Chambers, B.J., Harris, J.A., Hill, T.C.J., 2003. Zinc contamination decreases the bacterial diversity of agricultural soil. FEMS Microbiology Ecology 43, 13-19. (Pubitemid 36173509)
57. Morgan, A.J., Kille, P., Sturzenbaum, S.R., 2007. Microevolution and ecotoxicology of metals in invertebrates. Environmental Science & Technology 41, 1085-1096.
58. Müller, A.K., Westergaard, K., Christensen, S., Sørensen, S.J., 2001. The effect of long-term mercury pollution on the soil microbial community. FEMS Microbiology Ecology 36, 11-19. (Pubitemid 32476855)
59. Nahmani, J., Hodson, M.E., Black, S., 2007a. Effects of metals on life cycle parameters of the earthworm Eisenia fetida exposed to field-contaminated, metal-polluted soils. Environmental Pollution 149, 44-58. (Pubitemid 47069662)
60. Nahmani, J., Hodson, M.E., Black, S., 2007b. A review of studies performed to assess metal uptake by earthworms. Environmental Pollution 145, 402-424. (Pubitemid 44821484)
61. Nahmani, J., Lavelle, P., Lapied, E., van Oort, F., 2003. Effects of heavy metal soil pollution on earthworm communities in the north of France: the 7th international symposium on earthworm ecology. Cardiff. Wales. 2002. Pedobiologia 47, 663-669. (Pubitemid 38097854)
62. Nawrot, T., Plusquin, M., Hogervorst, J., Roels, H.A., Celis, H., Thijs, L., Vangronsveld, J., Van Hecke, E., Staessen, J.A., 2006. Environmental exposure to cadmium and risk of cancer: a prospective population-based study. Lancet Oncology 7, 119-126. (Pubitemid 43159497)
63. Obrien, D.J., Kaneene, J.B., Poppenga, R.H., 1993. The use of mammals as sentinels for human exposure to toxic contaminants in the environment. Environmental Health Perspectives 99, 351-368. (Pubitemid 23174501)
64. Orr, H.A., 2009. Fitness and its role in evolutionary genetics. Nature Reviews Genetics 10 (8), 531-539.
65. Palmiter, R.D., 1998. The elusive function of metallothioneins. Proceedings of the National Academy of Sciences of the United States of America 95, 8428-8430. (Pubitemid 28350503)
66. Peralta-Videa, J.R., Lopez, M.L., Narayan, M., Saupe, G., Gardea-Torresdey, J., 2009. The biochemistry of environmental heavy metal uptake by plants: implications for the food chain. International Journal of Biochemistry and Cell Biology 41, 1665-1677.
67. Pérés, G., Vandenbulcke, F., Guernion, M., Hedde, M.l., Beguiristain, T., Douay, F., Houot, S., Piron, D., Richard, A., Bispo, A., Grand, C.c., Galsomies, L., Cluzeau, D., 2011. Earthworm indicators as tools for soil monitoring, characterization and risk assessment. An example from the national bioindicator programme (France). Pedobiologia 54 (Suppl.), S77-S87.
68. Piearce, T.G., Langdon, C.J., Meharg, A.A., Semple, K.T., 2002. Yellow earthworms: distinctive pigmentation associated with arsenic- and copper-tolerance in Lumbricus rubellus. Soil Biology and Biochemistry 34, 1833-1838. (Pubitemid 36137422)
69. Pigliucci, M., 2005. Evolution of phenotypic plasticity: where are we going now? Trends in Ecology and Evolution 20, 481-486. (Pubitemid 41207083)
70. Pizl, V., Josens, G., 1995. Earthworm communities along a gradient of urbanization. Environmental Pollution 90, 7-14.
71. Ricketts, H.J., Morgan, A.J., Spurgeon, D.J., Kille, P., 2004. Measurement of annetocin gene expression: a new reproductive biomarker in earthworm ecotoxicology. Ecotoxicology and Environmental Safety 57, 4-10. (Pubitemid 37491380)
72. Roelofs, D., Aarts, M.G.M., Schat, H., van Straalen, N.M., 2008. Functional ecological genomics to demonstrate general and specific responses to abiotic stress. Functional Ecology 22, 8-18.
73. Rombke, J., Jansch, S., Didden, W., 2005. The use of earthworms in ecological soil classification and assessment concepts. Ecotoxicology and Environmental Safety 62, 249-265. (Pubitemid 41199811)
74. Rozen, A., 2006. Effect of cadmium on life-history parameters in Dendrobaena octaedra (Lumbricidae: Oligochaeta) populations originating from forests differently polluted with heavy metals. Soil Biology and Biochemistry 38, 489-503. (Pubitemid 43234193)
75. Sanchez-Hernandez, J.C., 2006. Earthworm biomarkers in ecological risk assessment. Reviews of Environmental Contamination and Toxicology 188, 85-126.
76. Satchell, J.E., 1967. Lumbricidae. In: Burges, A., Raw, F. (Eds.), Soil Biology. Academic Press, London New York, pp. 259-322.
77. Seeber, J., Seeber, G.U.H., Kössler, W., Langel, R., Scheu, S., Meyer, E., 2005. Abundance and trophic structure of macro-decomposers on alpine pastureland (Central Alps, Tyrol): effects of abandonment of pasturing. Pedobiologia 49, 221-228. (Pubitemid 40697290)
78. Smith, B., Egeler, P., Gilberg, D., Hendershot, W., Stephenson, G., 2010. Uptake and elimination of cadmium and zinc by Eisenia andrei during exposure to low concentrations in artificial soil. Archives of Environmental Contamination and Toxicology 59, 264-273.
79. Spurgeon, D.J., Lister, L., Kille, P., Pereira, M.G., Wright, J., Svendsen, C., 2011. Toxicokinetic studies reveal variability in earthworm pollutant handling. Pedobiologia 54 (Suppl.), S217-S222.
80. Spurgeon, D.J., Svendsen, C., Kille, P., Morgan, A.J., Weeks, J.M., 2004. Responses of earthworms (Lumbricus rubellus) to copper and cadmium as determined by measurement of juvenile traits in a specifically designed test system. Ecotoxicology and Environmental Safety 57, 54-64. (Pubitemid 37491386)
81. Spurgeon, D.J., Weeks, J.M., Van Gestel, C.A.M., 2003. A summary of eleven years progress in earthworm ecotoxicology. Pedobiologia 47, 588-606. (Pubitemid 38105596)
82. Sterenborg, I., Roelofs, D., 2003. Field-selected cadmium tolerance in the springtail Orchesella cincta is correlated with increased metallothionein mRNA expression. Insect Biochemistry and Molecular Biology 33, 741-747. (Pubitemid 36821099)
83. Stork, N.E., Eggleton, P., 1992. Invertebrates as determinants and indicators of soil quality. American Journal of Alternative Agriculture 7, 38-45.
84. Stürzenbaum, S.R., Georgiev, O., Morgan, A.J., Kille, P., 2004. Cadmium detoxification in earthworms: from genes to cells. Environmental Science & Technology 38, 6283-6289. (Pubitemid 39578641)
85. Suthar, S., Singh, S., Dhawan, S., 2008. Earthworms as bioindicator of metals (Zn, Fe, Mn, Cu, Pb and Cd) in soils: Is metal bioaccumulation affected by their ecological category? Ecological Engineering 32, 99-107.
86. Timmermans, M.J.T.N., Ellers, J., Roelofs, D., Van Straalen, N.M., 2005. Metallothionein mRNA expression and cadmium tolerance in metal-stressed and reference populations of the springtail Orchesella cincta. Ecotoxicology 14, 727-739. (Pubitemid 41426239)
87. Tischer, S., 2009. Earthworms (Lumbricidae) as bioindicators: the relationship between in-soil and in-tissue heavy metal content. Polish Journal of Ecology 57, 513-523.
88. Uba, S., Uzairu, A., Okunola, O.J., 2009. Content of heavy metals in Lumbricus terrestris and associated soils in dump sites. International Journal of Environmental Research 3, 353-358.
89. Van Der Schalie, W.H., Gardner Jr., H.S., Bantle, J.A., De Rosa, C.T., Finch, R.A., Reif, J.S., Reuter, R.H., Backer, L.C., Burger, J., Folmar, L.C., Stokes, W.S., 1999. Animals as sentinels of human health hazards of environmental chemicals. Environmental Health Perspectives 107, 309-315. (Pubitemid 29231635)
90. van Gestel, C.A.M., van Brummelen, T.C., 1996. Incorporation of the biomarker concept in ecotoxicology calls for a redefinition of terms. Ecotoxicology 5, 217-225.
91. Van Kleunen, M., Fischer, M., 2005. Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytologist 166, 49-60. (Pubitemid 40428132)
92. Van Straalen, N.M., 1998. Evaluation of bioindicator systems derived from soil arthropod communities. Applied Soil Ecology 9, 429-437. (Pubitemid 128424681)
93. Weeks, J.M., 1995. The value of biomarkers for ecological risk assessment: academic toys or legislative tools? Applied Soil Ecology 2, 215-216.