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Earthworm metabolomic responses after exposure to aged PCB contaminated soils

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Abstract

1H NMR metabolomics was used to measure earthworm sub-lethal responses to polychlorinated biphenyls (PCBs) in historically contaminated (>30 years) soils (91–280 mg/kg Aroclor 1254/1260) after two and 14 days of exposure. Although our previous research detected a distinct earthworm metabolic response to PCBs in freshly spiked soil at lower concentrations (0.5–25 mg/kg Aroclor 1254), the results of this study suggest only weak or non-significant relationships between earthworm metabolic profiles and soil PCB concentrations. This concurs with the expectation that decades of contaminant aging have likely decreased PCB bioavailability and toxicity in the field. Instead of being influenced by soil contaminant concentration, earthworm metabolic profiles were more closely correlated to soil properties such as total soil carbon and soil inorganic carbon. Overall, these results suggested that 1H NMR metabolomics may be capable of detecting both site specific responses and decreased contaminant bioavailability to earthworms after only two days of exposure, whereas traditional toxicity tests require much more time (e.g. 14 days for acute toxicity and >50 days for reproduction tests). Therefore, there is significant opportunity to develop earthworm metabolomics as a sensitive tool for rapid assessment of the toxicity associated with contaminated field soils.

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References

  • Alam TM, Alam MK, Neerathilingam M, Volk DE, Sarkar S, Shakeel Ansari GA, Luxon BA (2010) 1H NMR metabonomic study of rat response to tri-phenyl phosphate and tri-butyl phosphate exposure. Metabolomics 6:386–394

    Article  CAS  Google Scholar 

  • Alexander M (2000) Aging, bioavailability, and overestimation of risk from environmental pollutants. Environ Sci Technol 34:4259–4265

    Article  CAS  Google Scholar 

  • Belfroid A, Van den Berg M, Seinen W, Hermens J, Van Gestel K (1995) Uptake, bioavailability and elimination of hydrophobic compounds in earthworms (Eisenia andrei) in field-contaminated soil. Environ Toxicol Chem 14:605–612

    CAS  Google Scholar 

  • Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188

    Article  Google Scholar 

  • Bohus E, Rácz A, Noszál B, Coen M, Beckonert O, Keun HC, Ebbels TMD, Cantor GH, Wijsman JA, Holmes E, Lindon JC, Nicholson JK (2009) Metabonomic investigations into the global biochemical sequelae of exposure to the pancreatic toxin 1-cyano-2-hydroxy-3-butene in the rat. Magn Reson Chem 47:S26–S35

    Article  CAS  Google Scholar 

  • Bonnard M, Eom I-C, Morel J-L, Vasseur P (2009) Genotoxic and reproductive effects of an industrially contaminated soil on the earthworm Eisenia fetida. Environ Mol Mutagen 50:60–67

    Article  CAS  Google Scholar 

  • Bonnard M, Devin S, Leyval C, Morel J-L, Vasseur P (2010) The influence of thermal desorption on genotoxicity of multipolluted soil. Ecotoxicol Environ Saf 73:955–960

    Article  CAS  Google Scholar 

  • Broadhurst DI, Kell DB (2006) Statistical strategies for avoiding false discoveries in metabolomics and related experiments. Metabolomics 2:171–196

    Article  CAS  Google Scholar 

  • Brown SAE, Simpson AJ, Simpson MJ (2008) Evaluation of sample preparation methods for nuclear magnetic resonance metabolic profiling studies with Eisenia fetida. Environ Toxicol Chem 27:828–836

    Article  CAS  Google Scholar 

  • Brown SAE, Simpson AJ, Simpson MJ (2009) 1H NMR metabolomics of earthworm responses to sub-lethal PAH exposure. Environ Chem 6:432–440

    Article  CAS  Google Scholar 

  • Brown SAE, McKelvie JR, Simpson AJ, Simpson MJ (2010) 1H NMR metabolomics of earthworm exposure to sub-lethal concentrations of phenanthrene in soil. Environ Pollut 158:2117–2123

    Article  CAS  Google Scholar 

  • Bundy JG, Osborn D, Weeks JM, Lindon JC, Nicholson JK (2001) An NMR-based metabonomic approach to the investigation of coelomic fluid biochemistry in earthworms under toxic stress. FEBS Lett 500:31–35

    Article  CAS  Google Scholar 

  • Bundy JG, Lenz EM, Bailey NJ, Gavaghan CL, Svendsen C, Spurgeon D, Hankard PK, Osborn D, Weeks JM, Trauger SA, Speir P, Sanders I, Lindon JC, Nicholson JK, Tang H (2002) 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 21:1966–1972

    CAS  Google Scholar 

  • Bundy JG, Spurgeon DJ, Svendsen C, Hankard PK, Weeks JM, Osborn D, Lindon JC, Nicholson JK (2004) Environmental metabonomics: applying combination biomarker analysis in earthworms at a metal contaminated site. Ecotoxicology 13:797–806

    Article  CAS  Google Scholar 

  • Bundy JG, Keun HC, Sidhu JK, Spurgeon DJ, Svendsen C, Kille P, Morgan AJ (2007) Metabolic profile biomarkers of metal contamination in a sentinel terrestrial species are applicable across multiple sites. Environ Sci Technol 41:4458–4464

    Article  CAS  Google Scholar 

  • Bundy JG, Sidhu JK, Rana F, Spurgeon DJ, Svendsen C, Wren JF, Stürzenbaum SR, Morgan AJ, Kille P (2008) ‘Systems toxicology’ approach identifies coordinated metabolic responses to copper in a terrestrial non-model invertebrate, the earthworm Lumbricus rubellus. BMC Biol 6. doi:10.1186/1741-7007-6-25

  • Craig A, Cloarec O, Holmes E, Nicholson JK, Lindon JC (2006) Scaling and normalization effects in NMR spectroscopic metabonomic data sets. Anal Chem 78:2262–2267

    Article  CAS  Google Scholar 

  • Cramer RD (1993) Partial least squares (PLS): its strengths and limitations. Perspect Drug Discov Des 1:269–278

    Article  CAS  Google Scholar 

  • Cui Q, Lewis IA, Hegeman AD, Anderson ME, Li J, Schulte CF, Westler WM, Eghbalnia HR, Sussman MR, Markley JL (2008) Metabolite identification via the Madison Metabolomics Consortium Database. Nat Biotechnol 26:162–164

    Article  CAS  Google Scholar 

  • Dieterle F, Ross A, Schlotterbeck G, Senn H (2006) Probabilistic quotient normalization as robust method to account for dilution of complex biological mixtures. Application in 1H NMR metabonomics. Anal Chem 78:4281–4290

    Article  CAS  Google Scholar 

  • Edwards CA (1996) Biology and ecology of earthworms. Chapman & Hall, London

    Google Scholar 

  • Eijsackers H, Van Gestel CAM, De Jonge S, Muijs B, Slijkerman D (2001) Polycyclic aromatic hydrocarbon-polluted dredged peat sediments and earthworms: a mutual interference. Ecotoxicology 10:35–50

    Article  CAS  Google Scholar 

  • Environment Canada (2004) Biological test method. Tests for toxicity of contaminated soil to earthworms (Eisenia andrei, Eisenia fetida, or Lumbricus terrestris). Environment Canada, Ottawa

    Google Scholar 

  • Erickson ME (2001) Introduction: PCB properties, uses, occurrence, and regulatory history. In: Robertson LW, Hansen LG (eds) PCBs: recent advances in environmental toxicology and health effects. University Press of Kentucky, Lexington

    Google Scholar 

  • Eriksson L, Hermens JL, Johansson E, Verhaar HJ, Wold S (1995) Multivariate analysis of aquatic toxicity data with PLS. Aquat Sci 57:217–241

    Article  Google Scholar 

  • Eriksson L, Johansson E, Kettaneh-Wold N, Trygg J, Wikström C, Wold S (2006) Multi- and megavariate data analysis. Part I: basic principles and applications. Umetrics, Umeå

    Google Scholar 

  • Filzmoser P, Varmuza K (2010) Chemometrics: multivariate statistical analysis in chemometrics. R package version 0.8

  • Gibb JOT, Svendsen C, Weeks JM, Nicholson JK (1997) 1H NMR spectroscopic investigations of tissue metabolite biomarker response to Cu(II) exposure in terrestrial invertebrates: identification of free histidine as a novel biomarker of exposure to copper in earthworms. Biomarkers 2:295–302

    Article  CAS  Google Scholar 

  • Griffin JL, Shore RF (2007) Applications of metabonomics within environmental toxicology. In: Lindon JC, Nicholson JK, Holmes E (eds) The handbook of metabonomics and metabolomics. Elsevier Science B.V., Amsterdam, pp 517–532

    Google Scholar 

  • Guo Q, Sidhu JK, Ebbels TMD, Rana F, Spurgeon DJ, Svendsen C, Stürzenbaum SR, Kille P, Morgan AJ, Bundy JG (2009) Validation of metabolomics for toxic mechanism of action screening with the earthworm Lumbricus rubellus. Metabolomics 5:72–83

    Article  CAS  Google Scholar 

  • Hallgren P, Westbom R, Nilsson T, Sporring S, Björklund E (2006) Measuring bioavailability of polychlorinated biphenyls in soil to earthworms using selective supercritical fluid extraction. Chemosphere 63:1532–1538

    Article  CAS  Google Scholar 

  • Hawkins DM, Basak SC, Mills D (2003) Assessing model fit by cross-validation. J Chem Inf Comput Sci 43:579–586

    Article  CAS  Google Scholar 

  • Hines A, Staff FJ, Widdows J, Compton RM, Falciani F, Viant MR (2010) Discovery of metabolic signatures for predicting whole organism toxicology. Toxicol Sci 115:369–378

    Article  CAS  Google Scholar 

  • Hughes SL, Bundy JG, Want EJ, Kille P, Stürzenbaum SR (2009) 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 8:3512–3519

    Article  CAS  Google Scholar 

  • Ilyas M, Sudaryanto A, Setiawan IE, Riyadi AS, Isobe T, Ogawa S, Takahashi S, Tanabe S (2011) Characterization of polychlorinated biphenyls and brominated flame retardants in surface soils from Surabaya, Indonesia. Chemosphere 83:783–791

    Article  CAS  Google Scholar 

  • Jackson JE (1991) A user’s guide to principal components. John Wiley and Sons, New York

    Book  Google Scholar 

  • Jones OAH, Spurgeon DJ, Svendsen C, Griffin JL (2008) A metabolomics based approach to assessing the toxicity of the polyaromatic hydrocarbon pyrene to the earthworm Lumbricus rubellus. Chemosphere 71:601–609

    Article  CAS  Google Scholar 

  • Kaisarevic S, Hilscherova K, Weber R, Sundqvist KL, Tysklind M, Voncina E, Bobic S, Andric N, Pogrmic-Majkic K, Vojinovic-Miloradov M, Giesy JP, Kovacevic R (2011) Characterization of dioxin-like contamination in soil and sediments from the “hot spot” area of petrochemical plant in Pancevo (Serbia). Environ Sci Pollut Res 18:677–686

    Article  CAS  Google Scholar 

  • Krauss M, Wilcke W, Zech W (2000) Availability of polycyclic aromatic hydrocarbons (PAHs) and polychlorinated biphenyls (PCBs) to earthworms in urban soils. Environ Sci Technol 34:4335–4340

    Article  CAS  Google Scholar 

  • Lankadurai BP, Wolfe DM, Simpson AJ, Simpson MJ (2011a) 1H NMR-based metabolomics of time-dependent responses of Eisenia fetida to sub-lethal phenanthrene exposure. Environ Pollut 159:2845–2851

    Article  CAS  Google Scholar 

  • Lankadurai BP, Wolfe DM, Simpson AJ, Simpson MJ (2011b) 1H NMR-based metabolomic observation of a two-phased toxic mode of action in Eisenia fetida after sub-lethal phenanthrene exposure. Environ Chem 8:105–114

    Article  CAS  Google Scholar 

  • Lenz EM, Weeks JM, Lindon JC, Osborn D, Nicholson JK (2005) Qualitative high field 1H-NMR spectroscopy for the characterization of endogenous metabolites in earthworms with biochemical biomarker potential. Metabolomics 1:123–136

    Article  CAS  Google Scholar 

  • Lin D, Zhou Q, Xie X, Liu Y (2010) Potential biochemical and genetic toxicity of triclosan as an emerging pollutant on earthworms (Eisenia fetida). Chemosphere 81:1328–1333

    Article  CAS  Google Scholar 

  • Liu Y, Zhou Q, Xie X, Lin D, Dong L (2010) Oxidative stress and DNA damage in the earthworm Eisenia fetida induced by toluene, ethylbenzene and xylene. Ecotoxicology 19:1–9

    Article  Google Scholar 

  • Lopez BN, Man YB, Zhao YG, Zheng JS, Leung AOW, Yao J, Wong MH (2011) Major pollutants in soils of abandoned agricultural land contaminated by e-waste activities in Hong Kong. Arch Environ Contam Toxicol 61:101–114

    Article  CAS  Google Scholar 

  • McKelvie JR, Yuk J, Xu Y, Simpson AJ, Simpson MJ (2009) 1H NMR and GC/MS metabolomics of earthworm responses to sub-lethal DDT and endosulfan exposure. Metabolomics 5:84–94

    Article  CAS  Google Scholar 

  • McKelvie JR, Wolfe DM, Celejewski M, Simpson AJ, Simpson MJ (2010) Correlations of Eisenia fetida metabolic responses to extractable phenanthrene concentrations through time. Environ Pollut 158:2150–2157

    Article  CAS  Google Scholar 

  • Morgenthal K, Weckwerth W, Steuer R (2006) Metabolomic networks in plants: transitions from pattern recognition to biological interpretation. Biosystems 83:108–117

    Article  CAS  Google Scholar 

  • Morrison DE, Robertson BK, Alexander M (2000) Bioavailability to earthworms of aged DDT, DDE, DDD, and dieldrin in soil. Environ Sci Technol 34:709–713

    Article  CAS  Google Scholar 

  • Nicholson JK, Lindon JC, Holmes E (1999) ‘Metabonomics’: understanding the metabolic responses of living systems to pathophysiological stimuli via multivariate statistical analysis of biological NMR spectroscopic data. Xenobiotica 29:1181–1189

    Article  CAS  Google Scholar 

  • Nyholm JR, Asamoah RK, Van Der Wal L, Danielsson C, Andersson PL (2010) Accumulation of polybrominated diphenyl ethers, hexabromobenzene, and 1,2-dibromo-4-(1,2-dibromoethyl)cyclohexane in earthworm (Eisenia fetida). Effects of soil type and aging. Environ Sci Technol 44:9189–9194

    Article  CAS  Google Scholar 

  • OECD (Organisation for Economic Co-operation and Development) (1984) Guideline for testing of chemicals No. 207. Earthworm acute toxicity test. OECD, Paris

    Google Scholar 

  • OECD (Organisation for Economic Co-operation and Development) (2004) Guideline for testing of chemicals No. 222. Earthworm reproduction test. OECD, Paris

    Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rochfort SJ, Ezernieks V, Yen AL (2009) NMR-based metabolomics using earthworms as potential indicators for soil health. Metabolomics 5:95–107

    Article  CAS  Google Scholar 

  • Semple KT, Morriss AWJ, Paton GI (2003) Bioavailability of hydrophobic organic contaminants in soils: fundamental concepts and techniques for analysis. Eur J Soil Sci 54:809–818

    Article  CAS  Google Scholar 

  • Simpson AJ, Brown SA (2005) Purge NMR: effective and easy solvent suppression. J Magn Reson 175:340–346

    Article  CAS  Google Scholar 

  • Spiegel MR (1991) Schaum’s outline of theory and problems of statistics. McGraw-Hill, New York

    Google Scholar 

  • Sun H-W, Li J-G (2005) Availability of pyrene in unaged and aged soils to earthworm uptake, butanol extraction and SFE. Water Air Soil Pollut 166:353–365

    Article  CAS  Google Scholar 

  • Taylor NS, Weber RJM, Southam AD, Payne TG, Hrydziuszko O, Arvanitis TN, Viant MR (2009) A new approach to toxicity testing in Daphnia magna: application of high throughput FT-ICR mass spectrometry metabolomics. Metabolomics 5:44–58

    Article  CAS  Google Scholar 

  • Varmuza K, Filzmoser P (2009) Introduction to multivariate statistical analysis in Chemometrics. CRC Press, Boca Raton

    Book  Google Scholar 

  • Vendeginste BGM, Massart DL, Buydens LMC, de Jong S, Lewi PJ, Smeyers-Verbeke J (1998) Handbook of Chemometrics and Qualimetrics: part B. Elsevier, Amsterdam

    Google Scholar 

  • Verouden MPH, Westerhuis JA, van der Werf MJ, Smilde AK (2009) Exploring the analysis of structured metabolomics data. Chemometr Intell Lab Syst 98:88–96

    Article  CAS  Google Scholar 

  • Viant MR (2008) Recent developments in environmental metabolomics. Mol Biosyst 4:980–986

    Article  CAS  Google Scholar 

  • Viant MR, Rosenblum ES, Tjeerdema RS (2003) NMR-based metabolomics: a powerful approach for characterizing the effects of environmental stressors on organism health. Environ Sci Technol 37:4982–4989

    Article  CAS  Google Scholar 

  • Ville P, Roch P, Cooper EL, Masson P, Narbonne J-F (1995) PCBs increase molecular-related activities (lysozyme, antibacterial, hemolysis, proteases) but inhibit macrophage-related functions (phagocytosis, wound healing) in earthworms. J Invertebr Pathol 65:217–224

    Article  CAS  Google Scholar 

  • Vlčková K, Hofman J (2012) A comparison of POPs bioaccumulation in Eisenia fetida in natural and artificial soils and the effects of aging. Environ Pollut 160:49–56

    Article  Google Scholar 

  • Vulimiri SV, Berger A, Sonawane B (2011) The potential of metabolomic approaches for investigating mode(s) of action of xenobiotics: case study with carbon tetrachloride. Mutat Res Genet Toxicol Environ Mutagen 722:147–153

    Article  CAS  Google Scholar 

  • Warne MA, Lenz EM, Osborn D, Weeks JM, Nicholson JK (2000) An NMR-based metabonomic investigation of the toxic effects of 3-trifluoromethyl-aniline on the earthworm Eisenia veneta. Biomarkers 5:56–72

    Article  CAS  Google Scholar 

  • Weber R, Gaus C, Tysklind M, Johnston P, Forter M, Hollert H, Heinisch E, Holoubek I, Lloyd-Smith M, Masunaga S, Moccarelli P, Santillo D, Seike N, Symons R, Torres JPM, Verta M, Varbelow G, Vijgen J, Watson A, Costner P, Woelz J, Wycisk P, Zennegg M (2008) Dioxin- and POP-contaminated sites—contemporary and future relevance and challenges: overview on background, aims and scope of the series. Environ Sci Pollut Res 15:363–393

    Article  CAS  Google Scholar 

  • Westerhuis JA, Hoefsloot HCJ, Smit S, Vis DJ, Smilde AK, Velzen EJJ, Duijnhoven JPM, Dorsten FA (2008) Assessment of PLSDA cross validation. Metabolomics 4:81–89

    Article  CAS  Google Scholar 

  • Whitfield Åslund ML, Zeeb BA, Rutter A, Reimer KJ (2007) In situ phytoextraction of polychlorinated biphenyl—(PCB)contaminated soil. Sci Total Environ 374:1–12

    Article  Google Scholar 

  • Whitfield Åslund ML, Rutter A, Reimer KJ, Zeeb BA (2008) The effects of repeated planting, planting density, and specific transfer pathways on PCB uptake by Cucurbita pepo grown in field conditions. Sci Total Environ 405:14–25

    Article  Google Scholar 

  • Whitfield Åslund ML, Simpson AJ, Simpson MJ (2011) 1H NMR metabolomics of earthworm responses to polychlorinated biphenyls (PCBs) exposure in soil. Ecotoxicology 20:836–846

    Article  Google Scholar 

  • Yuk J, Simpson MJ, Simpson AJ (2011) 1-D and 2-D NMR metabolomics of earthworm responses to sub-lethal trifluralin and endosulfan exposure. Environ Chem 8:281–294

    Article  CAS  Google Scholar 

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Acknowledgments

We gratefully acknowledge funding for this research from the Natural Science and Engineering Research Council (NSERC) of Canada in the form of Strategic and Discovery Grants to MJS. We also thank Dr. Jennifer McKelvie, Brian Lankadurai, and Jimmy Yuk for valuable discussions.

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Authors and Affiliations

  1. Department of Physical and Environmental Sciences, University of Toronto, 1265 Military Trail, Toronto, ON, M1C 1A4, Canada

    Melissa Whitfield Åslund, Myrna J. Simpson & André J. Simpson

  2. Department of Chemistry and Chemical Engineering, Royal Military College of Canada, Kingston, ON, Canada

    Barbara A. Zeeb

  3. School of Environmental Studies, Queen’s University, Kingston, ON, Canada

    Allison Rutter

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  1. Melissa Whitfield Åslund
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  2. Myrna J. Simpson
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Correspondence to Myrna J. Simpson.

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Whitfield Åslund, M., Simpson, M.J., Simpson, A.J. et al. Earthworm metabolomic responses after exposure to aged PCB contaminated soils. Ecotoxicology 21, 1947–1956 (2012). https://doi.org/10.1007/s10646-012-0928-x

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