Skip to main content

Advertisement

Log in

Effect of Cu and Ni on cellular energy allocation in Enchytraeus albidus

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Effects of nickel and copper on Enchytraeus albidus (Oligochaeta) were investigated using the cellular energy allocation approach. This methodology is used to evaluate the energetic status of an organism and is indicative of its overall condition. Enchytraeids were exposed to the reproduction Effect Concentrations (EC50 and EC90), and the parameters measured were the total energy reserves available (protein, carbohydrate and lipid budgets) and the energy consumption [based on electron transport system activity] which were further integrated to obtain the cellular energy allocation over different periods of exposure (0–2, 2–4 and 4–8 days). Carbohydrates (in comparison to lipids and proteins) were the only energy source mobilized in the case of nickel within 8 days of exposure. For copper exposure, protein budgets were also strongly reduced. Energy consumption increased in a time and dose-dependent way for copper and in the longer exposure period (4–8 days) at the EC90 for Ni exposure, indicating that this is a good biomarker for effects of short-time metal exposure, while cellular energy allocation was only significantly reduced for the EC90 of copper (4–8 days) and EC50 of nickel (2–4 days). The effects of nickel at concentrations causing 50 and 90 % decrease in reproduction were likely not due to the changes in cellular energy allocation within 8 days of exposure.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ameh AO, Mohammed-dabo IA, Ibrahim S et al (2012) Uptake and elimination kinetics of heavy metals by earthworm (Eudrilus eugenia) exposed to used engine oil-contaminated soil. African J Biotechnol 11:14805–14811. doi:10.5897/AJB12.1069

    CAS  Google Scholar 

  • Amorim MJB, Gomes SIL, Soares AMVM, Scott-Fordsmand JJ (2012) Energy basal levels and allocation among lipids, proteins, and carbohydrates in Enchytraeus albidus: changes related to exposure to Cu salt and Cu nanoparticles. Water, Air, Soil Pollut 223:477–482. doi:10.1007/s11270-011-0867-9

    Article  CAS  Google Scholar 

  • Amorim MJB, Rombke J, Schallna HJ, Soares AMVM (2005) Effect of soil properties and aging on the toxicity of copper for Enchytraeus albidus, Enchytraeus luxuriosus, and Folsomia candida. Environ Toxicol Chem 24:1875–1885

    Article  CAS  Google Scholar 

  • Beaumelle L, Lamy I, Cheviron N, Hedde M (2014) Is there a relationship between earthworm energy reserves and metal availability after exposure to field-contaminated soils? Environ Pollut 191:182–189. doi:10.1016/j.envpol.2014.04.021

    Article  CAS  Google Scholar 

  • Bednarska AJ, Gerhardt A, Laskowski R (2010) Locomotor activity and respiration rate of the ground beetle, Pterostichus oblongopunctatus (Coleoptera: Carabidae), exposed to elevated nickel concentration at different temperatures: novel application of Multispecies Freshwater Biomonitor. Ecotoxicology 19:864–871. doi:10.1007/s10646-010-0467-2

    Article  CAS  Google Scholar 

  • Bednarska AJ, Stachowicz I, Kuriańska L (2013) Energy reserves and accumulation of metals in the ground beetle Pterostichus oblongopunctatus from two metal-polluted gradients. Environ Sci Pollut Res Int 20:390–398. doi:10.1007/s11356-012-0993-y

    Article  CAS  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917. doi:10.1139/o59-099

    Article  CAS  Google Scholar 

  • Boeck GDe, Vlaeminck A, Blust R (1997) Environmental contamination and toxicology effects of sublethal copper exposure on copper accumulation, food consumption, growth, energy stores, and nucleic acid content in common carp. Arch Environ Contam Toxicol 422:415–422. doi:10.1007/s002449900271

    Article  Google Scholar 

  • Bradford MM (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3

    Article  CAS  Google Scholar 

  • Bundy JG, Sidhu JK, Rana F et al (2008) “Systems toxicology” approach identifies coordinated metabolic responses to copper in a terrestrial non-model invertebrate, the earthworm Lumbricus rubellus. Bmc Biol 6:25

    Article  Google Scholar 

  • Calow P (1991) Physiological costs of combating chemical toxicants: ecological implications. Comp Biochem Physiol C 100:3–6

    Article  CAS  Google Scholar 

  • Cedergreen N, Nørhave NJ, Nielsen K et al (2013) Low temperatures enhance the toxicity of copper and cadmium to Enchytraeus crypticus through different mechanisms. Environ Toxicol Chem 32:2274–2283. doi:10.1002/etc.2274

    Article  CAS  Google Scholar 

  • Chen C-Y, Lin T-K, Chang Y-C et al (2010) Nickel(II)-induced oxidative stress, apoptosis, G2/M arrest, and genotoxicity in normal rat kidney cells. J Toxicol Environ Health A 73:529–539. doi:10.1080/15287390903421250

    Article  CAS  Google Scholar 

  • De Coen WM, Janssen CR (1997) The use of biomarkers in Daphnia magna toxicity testing. IV. Cellular Energy Allocation: a new methodology to assess the energy budget of toxicant-stressed Daphnia populations. J Aquat Ecosyst Stress Recover 6:43–55. doi:10.1023/A:1008228517955

    Article  Google Scholar 

  • De Coen WM, Janssen CR (2003) The missing biomarker link: relationships between effects on the cellular energy allocation biomarker of toxicant-stressed Daphnia magna and corresponding population characteristics. Env Toxicol Chem 22:1632–1641. doi:10.1002/etc.5620220727

    Article  Google Scholar 

  • De Schamphelaere KAC, Janssen CR (2004) Effects of chronic dietary copper exposure on growth and reproduction of Daphnia magna. Environ Toxicol Chem 23:2038–2047

    Article  Google Scholar 

  • Einicker-Lamas M, Mezian GA, Fernandes TB et al (2002) Euglena gracilis as a model for the study of Cu2+ and Zn2+ toxicity and accumulation in eukaryotic cells. Environ Pollut 120:779–786. doi:10.1016/S0269-7491(02)00170-7

    Article  CAS  Google Scholar 

  • Erk M, Ivanković D, Strižak Ž (2011) Cellular energy allocation in mussels (Mytilus galloprovincialis) from the stratified estuary as a physiological biomarker. Mar Pollut Bull 62:1124–1129. doi:10.1016/j.marpolbul.2011.02.056

    Article  CAS  Google Scholar 

  • Gnaiger E (1983) Calculation of energetic and biochemical equivalents of respiratory oxygen consumption. In: Gnaiger E, Forstner H (eds) Polarographic Oxygen sensors SE–30. Springer, Berlin Heidelberg, pp 337–345

  • Gomes SIL, Novais SC, Gravato C et al (2012a) Effect of Cu-nanoparticles versus one Cu-salt: analysis of stress and neuromuscular biomarkers response in Enchytraeus albidus (Oligochaeta). Nanotoxicology 6:134–143. doi:10.3109/17435390.2011.562327

    Article  CAS  Google Scholar 

  • Gomes SIL, Novais SC, Scott-Fordsmand JJ et al (2012b) Effect of Cu-nanoparticles versus Cu-salt in Enchytraeus albidus (Oligochaeta): Differential gene expression through microarray analysis. Comp Biochem Physiol Part C 155:219–227. doi:10.1016/j.cbpc.2011.08.008

    CAS  Google Scholar 

  • Gomes SIL, Scott-Fordsmand JJ, Amorim MJB (2014) Profiling transcriptomic response of Enchytraeus albidus to Cu and Ni: comparison with Cd and Zn. Environ Pollut 186:75–82. doi:10.1016/j.envpol.2013.11.031

    Article  CAS  Google Scholar 

  • Gomes SIL, Soares AMVM, AmorimMJB (2016) Energy reserves and cellular energy allocation studies: should food supply be provided? Submitted.

  • He E, van Gestel CAM (2013) Toxicokinetics and toxicodynamics of nickel in Enchytraeus crypticus. Environ Toxicol Chem 32:1835–1841. doi:10.1002/etc.2253

    Article  CAS  Google Scholar 

  • Holmstrup M, Sørensen JG, Overgaard J et al (2011) Body metal concentrations and glycogen reserves in earthworms (Dendrobaena octaedra) from contaminated and uncontaminated forest soil. Environ Pollut 159:190–197. doi:10.1016/j.envpol.2010.09.005

    Article  CAS  Google Scholar 

  • Howcroft CF, Amorim MJB, Gravato C et al (2009) Effects of natural and chemical stressors on Enchytraeus albidus: Can oxidative stress parameters be used as fast screening tools for the assessment of different stress impacts in soils? Environ Int 35:318–324

    Article  CAS  Google Scholar 

  • ISO (2005) Soil Quality - Effects of pollutants on Enchytraeidae (Enchytraeus sp.). Determination of effects on reproduction and survival. International Organization for Standardization, Geneva,Switzerland, Guideline No. 16387

  • Jager T, Barsi A, Hamda NT et al (2014) Dynamic energy budgets in population ecotoxicology: applications and outlook. Ecol Modell 280:140–147. doi:10.1016/j.ecolmodel.2013.06.024

    Article  Google Scholar 

  • King F, Packard T (1975) Respiration and the activity of the respiratory electron transport system in marine zooplankton. Limnol Oceanogr 20(5):849–854

    Article  Google Scholar 

  • Kozlov MV, Zvereva EL (2006) Industrial barrens: extreme habitats created by non-ferrous metallurgy. Rev Environ Sci Bio/Technology 6:231–259. doi:10.1007/s11157-006-9117-9

    Article  Google Scholar 

  • Lister LJ, Svendsen C, Wright J et al (2011) Modelling the joint effects of a metal and a pesticide on reproduction and toxicokinetics in Lumbricid earthworms. Environ Int 37:663–670. doi:10.1016/j.envint.2011.01.006

    Article  CAS  Google Scholar 

  • Misra M, Rodriguez RE, North SL, Kasprzak KS (1991) Nickel-induced renal lipid peroxidation in different strains of mice: concurrence with nickel effect on antioxidant defense systems. Toxicol Lett 58:121–133

    Article  CAS  Google Scholar 

  • Moolman L, Van Vuren JHJ, Wepener V (2007) Comparative studies on the uptake and effects of cadmium and zinc on the cellular energy allocation of two freshwater gastropods. Ecotoxicol Environ Saf 68:443–450. doi:10.1016/j.ecoenv.2006.12.017

    Article  CAS  Google Scholar 

  • Muyssen BTA, Janssen CR (2001) Multigeneration zinc acclimation and tolerance in Daphnia magna : Implications for water-quality guidelines and ecological risk assessment. Environ Toxicol Chem 20:2053–2060. doi:10.1002/etc.5620200926

    Article  CAS  Google Scholar 

  • Novais SC, Amorim MJB (2013) Changes in cellular energy allocation in Enchytraeus albidus when exposed to dimethoate, atrazine, and carbendazim. Environ Toxicol Chem 32:2800–2807. doi:10.1002/etc.2368

    Article  CAS  Google Scholar 

  • Novais SC, Gomes SIL, Gravato C et al (2011) Reproduction and biochemical responses in Enchytraeus albidus (Oligochaeta) to zinc or cadmium exposures. Environ Pollut 159:1836–1843. doi:10.1016/j.envpol.2011.03.031

    Article  CAS  Google Scholar 

  • Novais SC, Soares AMVM, De Coen W, Amorim MJB (2013) Exposure of Enchytraeus albidus to Cd and Zn – Changes in cellular energy allocation (CEA) and linkage to transcriptional, enzymatic and reproductive effects. Chemosphere 90:1305–1309. doi:10.1016/j.chemosphere.2012.09.030

    Article  CAS  Google Scholar 

  • OECD (2004) Guidelines for the testing of chemicals No. 220. Enchytraeid Reproduction Test. Organization for Economic Cooperation and Development, Paris

    Book  Google Scholar 

  • Pan JJ, Chang QS, Wang X et al (2010) Reactive oxygen species-activated Akt/ASK1/p38 signaling pathway in nickel compound-induced apoptosis in BEAS 2B Cells. Chem Res Toxicol 23:568–577. doi:10.1021/Tx9003193

    Article  CAS  Google Scholar 

  • Pane EF, McGeer JC, Wood CM (2004) Effects of chronic waterborne nickel exposure on two successive generations of Daphnia magna. Environ Toxicol Chem 23:1051–1056

    Article  CAS  Google Scholar 

  • Phipps T, Tank SL, Wirtz J et al (2002) Essentiality of nickel and homeostatic mechanisms for its regulation in terrestrial organisms. Environ Rev 10:209–261. doi:10.1139/a02-009

    Article  CAS  Google Scholar 

  • Scott-Fordsmand J, Weeks J, Hopkin S (1998) Toxicity of nickel to the earthworm and the applicability of the neutral red retention assay. Ecotoxicology 7:291–295. doi:10.1023/A:1008824531114

    Article  CAS  Google Scholar 

  • SigmaPlot 11.0 (2009) Copyright © Systat Software Inc.

  • Smolders R, Bervoets L, De Coen W, Blust R (2004) Cellular energy allocation in zebra mussels exposed along a pollution gradient: linking cellular effects to higher levels of biological organization. Environ Pollut 129:99–112. doi:10.1016/j.envpol.2003.09.027

    Article  CAS  Google Scholar 

  • Smolders R, De Boeck G, Blust R (2003) Changes in cellular energy budget as a measure of whole effluent toxicity in zebrafish (Danio rerio). Environ Toxicol Chem 22:890–899. doi:10.1002/etc.5620220429

    Article  CAS  Google Scholar 

  • Sroda S, Cossu-Leguille C (2011) Effects of sublethal copper exposure on two gammarid species: which is the best competitor? Ecotoxicology 20:264–273. doi:10.1007/s10646-010-0578-9

    Article  CAS  Google Scholar 

  • Surendra Nath B (2002) Shifts in glycogen metabolism in hemolymph and fat body of the silkworm, Bombyx mori (Lepidoptera: Bombycidae) in response to organophosphorus insecticides toxicity. Pestic Biochem Physiol 74:73–84. doi:10.1016/S0048-3575(02)00152-9

    Article  CAS  Google Scholar 

  • Svendsen C, Weeks JM (1997) Relevance and applicability of a simple earthworm biomarker of copper exposure. II. Validation and applicability under field conditions in a mesocosm experiment with Lumbricus rubellus. Ecotoxicol Environ Saf 36:80–88. doi:10.1006/eesa.1996.1492

    Article  CAS  Google Scholar 

  • Tripathi PK, Singh A (2002) Toxic Effects of Dimethoate and Carbaryl Pesticides on Carbohydrate Metabolism of Freshwater Snail Lymnaea acuminata. Bull Environ Contam Toxicol 68:606–611. doi:10.1007/s001280297

    Article  CAS  Google Scholar 

  • Vandenbrouck T, Soetaert A, van der Ven K et al (2009) Nickel and binary metal mixture responses in Daphnia magna: Molecular fingerprints and (sub) organismal effects. Aquat Toxicol 92:18–29. doi:10.1016/j.aquatox.2008.12.012

    Article  CAS  Google Scholar 

  • Vijayavel K, Balasubramanian MP (2006) Fluctuations of biochemical constituents and marker enzymes as a consequence of naphthalene toxicity in the edible estuarine crab Scylla serrata. Ecotoxicol Environ Saf 63:141–147. doi:10.1016/j.ecoenv.2005.02.004

    Article  CAS  Google Scholar 

  • Zhou C-F, Wang Y-J, Li C-C et al (2013) Subacute toxicity of copper and glyphosate and their interaction to earthworm (Eisenia fetida). Environ Pollut 180:71–77. doi:10.1016/j.envpol.2013.05.016

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by funding FEDER through COMPETE-Programa Operacional Factores de Competitividade, and by National funding through FCT-Fundação para a Ciência e Tecnologia, within the research project PEst-C/MAR/LA0017/2013 and a post-doc grant to Susana Gomes (SFRH/BPD/95775/2013). The authors acknowledge the help provided by Sara Novais.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Susana I.L. Gomes.

Ethics declarations

Conflictof interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gomes, S.I., Soares, A.M. & Amorim, M.J. Effect of Cu and Ni on cellular energy allocation in Enchytraeus albidus . Ecotoxicology 25, 1523–1530 (2016). https://doi.org/10.1007/s10646-016-1706-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-016-1706-y

Keywords

Navigation