1H NMR-based metabolomic observation of a two-phased toxic mode of action in Eisenia fetida after sub-lethal phenanthrene exposure

Environmental Chemistry

Volumn 8, Issue 2, 2011, Pages 105-114

  Lankadurai, Brian P ^a   Wolfe, David M ^a   Simpson, André J ^a   Simpson, Myrna J ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

concentration dependence; contact tests; LC50; metabonomics

Indexed keywords

CONCENTRATION (COMPOSITION); DOSE-RESPONSE RELATIONSHIP; EARTHWORM; METABOLISM; METABOLITE; MULTIVARIATE ANALYSIS; NUCLEAR MAGNETIC RESONANCE; PHENANTHRENE; POLLUTION EXPOSURE; TOXICITY TEST;

EISENIA FETIDA;

EID: 79955619188     PISSN: 14482517     EISSN: None     Source Type: Journal    
DOI: 10.1071/EN10094     Document Type: Article

References (58)

1. J. G. Bundy, E. M. Lenz, N. J. Bailey, C. L. Gavaghan, C. Svendsen, D. Spurgeon, P. K. Hankard, D. Osborn, J. A. Weeks, S. A. Trauger, Metabonomic assessment of toxicity of 4-fluoroaniline, 3,5- difluoroaniline and 2-fluoro-4-methylaniline to the earthworm Eisenia veneta (Rosa): identification of new endogenous biomarkers. Environ. Toxicol. Chem. 2002, 21, 1966.
2. M. J. Simpson, J. R. McKelvie, Environmental metabolomics: new insights into earthworm ecotoxicity and contaminant bioavailability in soil. Anal. Bioanal. Chem. 2009, 394, 137. doi:10.1007/S00216- 009-2612-4
3. S. A. E. Brown, A. J. Simpson, M. J. Simpson, Evaluation of sample preparation methods for nuclear magnetic resonance metabolic profiling studies with Eisenia fetida. Environ. Toxicol. Chem. 2008, 27, 828. doi:10.1897/07-412.1 (Pubitemid 351518137)
4. C. A. Edwards, P. J. Bohlen, The effects of toxic-chemicals on earthworms. Rev. Environ. Contam. Toxicol. 1992, 125, 23.
5. L. C. Fitzpatrick, R. Sassani, B. J. Venables, A. J. Goven, Comparative toxicity of polychlorinated-biphenyls to earthworms Eisenia foetida and Lumbricus terrestris. Environ. Pollut. 1992, 77, 65. doi:10.1016/ 0269-7491(92)90159-8
6. M. R. Viant, Recent developments in environmental metabolomics. Mol. Biosyst. 2008, 4, 980. doi:10.1039/B805354E
7. M. Oldiges, S. Lutz, S. Pflug, K. Schroer, N. Stein, C. Wiendahl, Metabolomics: current state and evolving methodologies and tools. Appl. Microbiol. Biotechnol. 2007, 76, 495. doi:10.1007/S00253-007- 1029-2 (Pubitemid 47283107)
8. Y. Y. Mosleh, S. Paris-Palacios, M. Couderchet, G. Vernet, Acute and sublethal effects of two insecticides on earthworms (Lumbricus terrestris L.) under laboratory conditions. Environ. Toxicol. 2003, 18, 1. doi:10.1002/TOX. 10095 (Pubitemid 36322312)
9. E. F. Neuhauser, C. A. Callahan, Growth and reproduction of the earthworm Eisenia fetida exposed to sublethal concentrations of organic-chemicals. Soil Biol. Biochem. 1990, 22, 175. doi:10.1016/ 0038-0717(90)90083-C
10. D. R. Ekman, Q. Teng, D. L. Villeneuve, M. D. Kahl, K. M. Jensen, E. J. Durhan, G. T. Ankley, T. W. Collette, Investigating compensation and recovery of fathead minnow (Pimephales promelas) exposed to 17 alpha-ethynylestradiol with metabolite profiling. Environ. Sci. Technol. 2008, 42, 4188. doi:10.1021/ES8000618 (Pubitemid 351770082)
11. B. M. Beckwith-Hall, J. K. Nicholson, A. W. Nicholls, P. J. D. Foxall, J. C. Lindon, S. C. Connor, M. Abdi, J. Connelly, E. Holmes, Nuclear magnetic resonance spectroscopic and principal components analysis investigations into biochemical effects of three model hepatotoxins. Chem. Res. Toxicol. 1998, 11, 260. doi:10.1021/ TX9700679
12. S. A. E. Brown, A. J. Simpson,M. J. Simpson, 1HNMRmetabolomics of earthworm responses to sub-lethal PAH exposure. Environ. Chem. 2009, 6, 432. doi:10.1071/EN09054
13. J. G. Bundy, M. P. Davey, M. R. Viant, Environmental metabolomics: a critical review and future perspectives. Metabolomics 2009, 5, 3. doi:10.1007/S11306-008-0152-0
14. J. G. Bundy, D. Osborn, J. M. Weeks, J. C. Lindon, J. K. Nicholson, An NMR-based metabonomic approach to the investigation of coelomic fluid biochemistry in earthworms under toxic stress. FEBS Lett. 2001, 500, 31. doi:10.1016/S0014-5793(01)02582-0 (Pubitemid 32575313)
15. J. R. McKelvie, J. Yuk, Y. P. Xu, A. J. Simpson, M. J. Simpson, 1H NMR and GC/MS metabolomics of earthworm responses to sublethal DDT and endosulfan exposure. Metabolomics 2009, 5, 84. doi:10.1007/S11306-008-0122-6
16. O. A. H. Jones, D. J. Spurgeon, C. Svendsen, J. L. Griffin, A metabolomics based approach to assessing the toxicity of the polyaromatic hydrocarbon pyrene to the earthworm Lumbricus rubellus. Chemosphere 2008, 71, 601. doi:10.1016/J.CHEMOSPHERE.2007. 08.056
17. S. A. E. Brown, J. R. McKelvie, A. J. Simpson, M. J. Simpson, 1H NMR metabolomics of earthworm exposure to sub-lethal concentrations of phenanthrene in soil. Environ. Pollut. 2010, 158, 2117. doi:10.1016/J.ENVPOL.2010.02.023
18. S. Lundstedt, P. Haglund, L. Oberg, Simultaneous extraction and fractionation of polycyclic aromatic hydrocarbons and their oxygenated derivatives in soil using selective pressurized liquid extraction. Anal. Chem. 2006, 78, 2993. doi:10.1021/AC052178F (Pubitemid 43726117)
19. M. J. Smith, T. H. Flowers, H. J. Duncan, J. Alder, Effects of polycyclic aromatic hydrocarbons on germination and subsequent growth of grasses and legumes in freshly contaminated soil and soil with aged PAHs residues. Environ. Pollut. 2006, 141, 519. doi:10.1016/J.ENVPOL.2005.08.061
20. M. K. Chung, R. Hu, K. C. Cheung, M. H. Wong, Pollutants in Hong Kong soils: polycyclic aromatic hydrocarbons. Chemosphere 2007, 67, 464. doi:10.1016/J.CHEMOSPHERE.2006.09.062 (Pubitemid 46107597)
21. C. Svendsen, D. J. Spurgeon, P. K. Hankard, J. M. Weeks, Areview of lysosomal membrane stability measured by neutral red retention: is it a workable earthworm biomarker? Ecotoxicol. Environ. Saf. 2004, 57, 20. doi:10.1016/J.ECOENV.2003.08.009 (Pubitemid 37491382)
22. R. van der Oost, J. Beyer, N. P. E. Vermeulen, Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ. Toxicol. Pharmacol. 2003, 13, 57. doi:10.1016/S1382-6689(02) 00126-6
23. Earthworm acute toxicity tests, in OECD Guideline 207 1984 (Organisation for Economic Co-operation and Development: Paris).
24. M. L. Hannam, S. D. Bamber, T. S. Galloway, A. J. Moody, M. B. Jones, Effects of the model PAH phenanthrene on immune function and oxidative stress in the haemolymph of the temperate scallop Pecten maximus. Chemosphere 2010, 78, 779. doi:10.1016/J.CHEMO SPHERE.2009.12.049
25. C. M. Hurdzan, N. T. Basta, P. G. Hatcher, O. H. Tuovinen, Phenanthrene release from natural organic matter surrogates under simulated human gastrointestinal conditions. Ecotoxicol. Environ. Saf. 2008, 69, 525. doi:10.1016/J.ECOENV.2007.02.006 (Pubitemid 351305016)
26. Trimmed Spearman-Karber (TSK) Program, Version 1.5 1991 (Ecological Monitoring Research Division, Environmental Monitoring Systems Laboratory, US Environmental Protection Agency: Cincinnati, OH).
27. M. A. Hamilton, R. C. Russo, R. V. Thurston, Trimmed Spearman- Karber method for estimating median lethal concentrations in toxicity bioassays. Environ. Sci. Technol. 1977, 11, 714. doi:10.1021/ ES60130A004
28. C. A. Edwards, J. E. Bater, The use of earthworms in environmentalmanagement, in The 4th International Symposium on Earthworm Ecology 1990, pp. 1683-1689 (Pergamon-Elsevier Science Ltd: Avignon, France).
29. A. J. Simpson, S. A. Brown, N. M. R. Purge, Effective and easy solvent suppression. J. Magn. Reson. 2005, 175, 340. doi:10.1016/J.JMR. 2005.05.008
30. J. G. Bundy, D. J. Spurgeon, C. Svendsen, P. K. Hankard, J. M. Weeks, D. Osborn, J. C. Lindon, J. K. Nicholson, Environmental metabonomics: Applying combination biomarker analysis in earthworms at a metal contaminated site. Ecotoxicology 2004, 13, 797. doi:10.1007/ S10646-003-4477-1
31. L. Eriksson, E. Johansson, N. Kettaneh-Wold, J. Trygg, C. Wikstrom, S. Wold, Multi- and Megavariate Data Analysis Part 1: Basic Principles and Applications 2006 (Umetrics AB: Umea, Sweden).
32. D. I. Broadhurst, D. B. Kell, Statistical strategies for avoiding false discoveries in metabolomics and related experiments. Metabolomics 2006, 2, 171. doi:10.1007/S11306-006-0037-Z (Pubitemid 46099798)
33. S. Wold, M. Sjostrom, L. Eriksson, PLS-regression: a basic tool of chemometrics. Chemometr. Intell. Lab. 2001, 58, 109. doi:10.1016/ S0169-7439(01)00155-1
34. S.Wold, J. Trygg, A. Berglund, H. Antti, Some recent developments in PLSmodel building. Chemometr. Intell. Lab. 2001, 58, 131. doi:10.1016/ S0169-7439(01)00156-3
35. S. Wold, L. Eriksson, Statistical validation of QSAR results, in Chemometrics Methods in Molecular Design (Ed. H. van de Waterbeemd) 1995, pp. 309-318 (VCH: Weinheim, Germany).
36. M. B. Brown, A. B. Forsythe, Robust Tests for Equality of Variances. J. Am. Stat. Assoc. 1974, 69, 364. doi:10.2307/2285659
37. A. F. B. Boroujerdi, M. I. Vizcaino, A. Meyers, E. C. Pollock, S. L. Huynh, T. B. Schock, P. J. Morris, D. W. Bearden, NMR-based microbial metabolomics and the temperature-dependent coral pathogen Vibrio coralliilyticus. Environ. Sci. Technol. 2009, 43, 7658. doi:10.1021/ES901675W
38. D. R. Ekman, Q. N. Teng, D. L. Villeneuve, M. D. Kahl, K. M. Jensen, E. J. Durhan, G. T. Ankley, T. W. Collette, Profiling lipid metabolites yields unique information on sex- and time-dependent responses of fathead minnows (Pimephales promelas) exposed to 17 alphaethynylestradiol. Metabolomics 2009, 5, 22. doi:10.1007/S11306- 008-0138-Y
39. J. G. Bundy, H. C. Keun, J. K. Sidhu, D. J. Spurgeon, C. Svendsen, P. Kille, A. J. Morgan, Metabolic profile biomarkers of metal contamination in a sentinel terrestrial species are applicable across multiple sites. Environ. Sci. Technol. 2007, 41, 4458. doi:10.1021/ES0700303 (Pubitemid 46981743)
40. W. Tuffnail, G. A. Mills, P. Cary, R. Greenwood, An environmental H-1 NMR metabolomic study of the exposure of the marine mussel Mytilus edulis to atrazine, lindane, hypoxia and starvation. Metabolomics 2009, 5, 33. doi:10.1007/S11306-008-0143-1
41. N. S. El-Shenawy, R. Greenwood, I. M. Ab-Del-Nabi, Z. I. Nabil, Effect of atrazine and lindane on the scope for growth of marine mussels Mytilus edulis. Acta Zool. Sin. 2006, 52, 712.
42. P. H. Yancey, M. E. Clark, S. C. Hand, R. D. Bowlus, G. N. Somero, Living with water-stress - evolution of osmolyte systems. Science 1982, 217, 1214. doi:10.1126/SCIENCE.7112124
43. S. A. S. Craig, Betaine in human nutrition. Am. J. Clin. Nutr. 2004, 80, 539.
44. L. Eriksson, P. L. Andersson, E. Johansson, M. Tysklind, Megavariate analysis of environmental QSAR data. Part I - A basic framework founded on principal component analysis (PCA), partial least squares (PLS), and statistical molecular design (SMD). Mol. Divers. 2006, 10, 169. doi:10.1007/S11030-006- 9024-6 (Pubitemid 44092207)
45. L. Eriksson, P. L. Andersson, E. Johansson, M. Tysklind, Megavariate analysis of environmental QSAR data. Part II - Investigating very complex problem formulations using hierarchical, non-linear and batch-wise extensions of PCA and PLS. Mol. Divers. 2006, 10, 187. doi:10.1007/S11030-006-9026-4 (Pubitemid 44092208)
46. M. Henningsson, E. Sundbom, B. A. Armelius, P. Erdberg, PLS model building: a multivariate approach to personality test data. Scand. J. Psychol. 2001, 42, 399. doi:10.1111/1467-9450.00252
47. S. Carraro, S. Rezzi, F. Reniero, K. Heberger, G. Giordano, S. Zanconato, C. Guillou, E. Baraldi, Metabolomics applied to exhaled breath condensate in childhood asthma. Am. J. Resp. Crit. Care 2007, 175, 986. doi:10.1164/RCCM. 200606-769OC (Pubitemid 46741749)
48. P. Geladi, B. R. Kowalski, Partial least-squares regression - a tutorial. Anal. Chim. Acta 1986, 185, 1. doi:10.1016/0003-2670(86)80028-9
49. M. R. Viant, J. G. Bundy, C. A. Pincetich, J. S. de Ropp, R. S. Tjeerdema, NMR-derived developmental metabolic trajectories: an approach for visualizing the toxic actions of trichloroethylene during embryogenesis. Metabolomics 2005, 1, 149. doi:10.1007/S11306- 005-4429-2
50. O. Beckonert, H. C. Keun, T. M. D. Ebbels, J. G. Bundy, E. Holmes, J. C. Lindon, J. K. Nicholson, Metabolic profiling, metabolomic and metabonomic procedures for NMR spectroscopy of urine, plasma, serum and tissue extracts. Nat. Protoc. 2007, 2, 2692. doi:10.1038/ NPROT.2007.376
51. G. Balcerowska, R. Siuda, H. Czarnik-Matusewicz, Orthogonal signal correction to PLS modelling in application to spectral data. Acta Agrophysica 2005, 6, 7.
52. M. Saint-Denis, J. F. Narbonne, C. Arnaud, E. Thybaud, D. Ribera, Biochemical responses of the earthworm Eisenia fetida andrei exposed to contaminated artificial soil: effects of benzo(a)pyrene. Soil Biol. Biochem. 1999, 31, 1837. doi:10.1016/S0038-0717(99) 00106-6
53. W. W. Zhang, Y. F. Y. F. Song, P. P. Gong, T. H. T. H. Sun, Q. X. Zhou, M. M. Liu, Earthworm cytochrome P450 determination and application as a biomarker for diagnosing PAH exposure. J. Environ. Monit. 2006, 8, 963. doi:10.1039/B605450A (Pubitemid 44327584)
54. R. K. Achazi, C. Flenner, D. R. Livingstone, L. D. Peters, K. Schaub, E. Scheiwe, Cytochrome P450 and dependent activities in unexposed and PAH-exposed terrestrial annelids. Comp. Biochem. Phys. C 1998, 121, 339.
55. P. J. Brown, S. M. Long, D. J. Spurgeon, C. Svendsen, P. K. Hankard, Toxicological and biochemical responses of the earthworm Lumbricus rubellus to pyrene, a non-carcinogenic polycyclic aromatic hydrocarbon. Chemosphere 2004, 57, 1675. doi:10.1016/J.CHEMO SPHERE.2004.05.041
56. J. J. Whyte, R. E. Jung, C. J. Schmitt, D. E. Tillitt, Ethoxyresorufin- O-deethylase (EROD) activity in fish as a biomarker of chemical exposure. Crit. Rev. Toxicol. 2000, 30, 347. doi:10.1080/ 10408440091159239
57. R. F. Lee, Annelid cytochrome P-450. Comp. Biochem. Phys. C 1998, 121, 173.
58. E. Gasteiger, C. Hoogland, A. Gattiker, S. Duvaud, M. R. Wilkins, R. D. Appel, A. Bairoch, Protein identification and analysis tools on the ExPASy server, in The Proteomics Protocols Handbook (Ed. J. M. Walker) 2005, pp. 571-607 (Humana Press: Totowa, NJ).