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Assessment of selenium toxicity on the life cycle of Caenorhabditis elegans

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Abstract

Selenium (Se) is a growing problem of global concern. Se can cause adverse effects on reproductive systems, which have been linked to declines in animal populations. The soil nematode Caenorhabditis elegans (C. elegans) is a ubiquitous soil organism that is increasingly utilized as a model organism in aquatic and soil toxicology. In the present study, the experimental data for individual body length, survival rate, brood size, and hatching rate were used to evaluate the possible effects of selenite [Se(IV)] on C. elegans. A stage-classified matrix model was applied to the experimental data to provide information on the population dynamics of C. elegans and to assess the Se(IV)-affected asymptotic population growth rate. Estimates of the survival probability showed significant decreases in survival at all stages when C. elegans was exposed to Se(IV). The growth probability of C. elegans in the L1 stage showed the most significant decline, from 0.11 h−1 (for the control) to 0.04 h−1 [for exposure to 3 mM Se(IV)]. These results showed that Se(IV) has a profound impact on C. elegans population dynamics. The asymptotic population growth rate (λ) was found to range from 1.00 to 0.64 h−1 for increasing Se(IV) concentrations, implying a potential risk of population decrease for C. elegans exposure to a Se(IV)-contaminated environment. Our study shows how a mechanistic view based on the Se(IV) effects on the soil nematode C. elegans can promote a life cycle toxicity assessment. An important implication of this analysis is that mathematical models can be used to produce a population stage structure, to give clarity to the analysis of the key population-level endpoint (the asymptotic population growth rate) of population dynamics, and to evaluate the influences for the response of other species to environmental Se. These models sequentially provide candidate environmental criteria for the evaluation of the population impact of Se.

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References

  • Álvarez OA, Jager T, Kooijman SALM, Kammenga JE (2005) Responses to stress of Caenorhabditis elegans populations with different reproductive strategies. Funct Ecol 19:656–664

    Article  Google Scholar 

  • Billoir E, da Silva Ferrao-Filho A, Laure Delignette-Muller M, Charles S (2009) DEBtox theory and matrix population models as helpful tools in understanding the interaction between toxic cyanobacteria and zooplankton. J Theor Biol 258:380–388

    Article  Google Scholar 

  • Boehler CJ, Raines AM, Sunde RA (2013) Deletion of thioredoxin reductase and effects of selenite and selenate toxicity in Caenorhabditis elegans. PLoS One 8:e71525

    Article  CAS  Google Scholar 

  • Brooks A, Lithgow GJ, Johnson TE (1994) Mortality rates in a genetically heterogeneous population of Caenorhabditis elegans. Science 263:668–671

    Article  CAS  Google Scholar 

  • Cartaxana A (2003) Growth of the prawn Palaemon longirostris (Decapoda, Palaemonidae) in Mira River and estuary, SW Portugal. J Crustacean Biol 23:251–257

    Article  Google Scholar 

  • Caswell H (2001) Matrix population models: construction, analysis, and interpretation. Sinauer Associates, Sunderland

    Google Scholar 

  • Chen BC, Liao CM (2004) Population models of farmed abalone Haliotis diversicolor supertexta exposed to waterborne zinc. Aquaculture 242:251–269

    Article  CAS  Google Scholar 

  • Chen J, Lewis EE, Carey JR, Caswell H, Caswell-Chen EP (2006) The ecology and biodemography of Caenorhabditis elegans. Exp Gerontol 41:1059–1065

    Article  CAS  Google Scholar 

  • Corsi AK (2006) A biochemist’s guide to C. elegans. Anal Biochem 359:1–17

    Article  CAS  Google Scholar 

  • Estevez AO, Mueller CL, Morgan KL, Szewczyk NJ, Teece L, Miranda-Vizuete A, Estevez M (2012) Selenium induces cholinergic motor neuron degeneration in Caenorhabditis elegans. Neurotoxicology 33:1021–1032

    Article  CAS  Google Scholar 

  • Hamilton SJ (2004) Review of selenium toxicity in the aquatic food chain. Sci Total Environ 326:1–31

    Article  CAS  Google Scholar 

  • Hill AV (1910) The possible effects of the aggregation of the molecules of haemoglobin on its dissociation curves. J Physiol 40:4–7

    Google Scholar 

  • Jager T, Crommentuijn T, van Gestel CA, Kooijman SA (2004) Simultaneous modeling of multiple end points in life-cycle toxicity tests. Environ Sci Technol 38:2894–2900

    Article  CAS  Google Scholar 

  • Jager T, Álvarez OA, Kammenga JE, Kooijman SALM (2005) Modelling nematode life cycles using dynamic energy budgets. Funct Ecol 19:136–144

    Article  Google Scholar 

  • Kaletta T, Hengartner MO (2006) Finding function in novel targets: C. elegans as a model organism. Nat Rev Drug Discov 5:387–398.

  • Klasing KC (1998) Nutritional modulation of resistance to infectious diseases. Poult Sci 77:1119–1125

    Article  CAS  Google Scholar 

  • Klok C (2008) Gaining insight in the interaction of zinc and population density with a combined dynamic energy budget and population model. Environ Sci Technol 42:8803–8808

    Article  CAS  Google Scholar 

  • Knight CG, Patel MN, Azevedo RB, Leroi AM (2002) A novel mode of ecdysozoan growth in Caenorhabditis elegans. Evol Dev 4:16–27

    Article  Google Scholar 

  • Leacock SW, Reinke V (2006) Expression profiling of MAP kinase-mediated meiotic progression in Caenorhabditis elegans. PLoS Genet 2:e174

    Article  Google Scholar 

  • Lemly AD (1997) Environmental implications of excessive selenium: a review. Biomed Environ Sci 10:415–435

    CAS  Google Scholar 

  • Lemly AD (2004) Aquatic selenium pollution is a global environmental safety issue. Ecotoxicol Environ Saf 59:44–56

    Article  CAS  Google Scholar 

  • Lenaerts I, van Eygen S, van Fleteren J (2007) Adult-limited dietary restriction slows gompertzian aging in Caenorhabditis elegans. Ann N Y Acad Sci 1100:442–448

    Article  Google Scholar 

  • Leung MC, Williams PL, Benedetto A, Au C, Helmcke KJ, Aschner M et al (2008) Caenorhabditis elegans: an emerging model in biomedical and environmental toxicology. Toxicol Sci 106:5–28

    Article  CAS  Google Scholar 

  • Li WH, Hsu FK, Liu JT, Liao VH (2011) The ameliorative and toxic effects of selenite on Caenorhabditis elegans. Food Chem Toxicol 49:812–819

    Article  CAS  Google Scholar 

  • Liao CM, Chiang KC, Tsai JW (2006) Bioenergetics-based matrix population modeling enhances life-cycle toxicity assessment of tilapia Oreochromis mossambicus exposed to arsenic. Environ Toxicol 21:154–165

    Article  CAS  Google Scholar 

  • Lin BL, Meng Y (2009) Extrapolation of available acute and chronic toxicity test data to population-level effects for ecological risk management of chemicals. Environ Toxicol Chem 28:1557–1566

    Article  CAS  Google Scholar 

  • Lopes C, Péry ARR, Chaumot A, Charles S (2005) Ecotoxicology and population dynamics: using DEBtox models in a Leslie modeling approach. Ecol Model 188:30–40

    Article  CAS  Google Scholar 

  • Morgan KL, Estevez AO, Mueller CL, Cacho-Valadez B, Miranda-Vizuete A, Szewczyk NJ et al (2010) The glutaredoxin GLRX-21 functions to prevent selenium-induced oxidative stress in Caenorhabditis elegans. Toxicol Sci 118:530–543

    Article  CAS  Google Scholar 

  • Muschiol D, Schroeder F, Traunspurger W (2009) Life cycle and population growth rate of Caenorhabditis elegans studied by a new method. BMC Ecol 9:14

    Article  Google Scholar 

  • Nuttall KL (2006) Evaluating selenium poisoning. Ann Clin Lab Sci 36:409–420

    CAS  Google Scholar 

  • Saiki R, Lunceford AL, Bixler T, Dang P, Lee W, et al. (2008) Altered bacterial metabolism, not coenzyme Q content, is responsible for the lifespan extension in Caenorhabditis elegans fed an Escherichia coli diet lacking coenzyme Q. Aging Cell 7:291–304.

  • Schafer WR (2006) Neurophysiological methods in C. elegans: an introduction. WormBook. doi:10.1895/wormbook.1.111.1

    Google Scholar 

  • Stark JD, Banks JE, Vargas R (2004) How risky is risk assessment: the role that life history strategies play in susceptibility of species to stress. Proc Natl Acad Sci U S A 101:732–736

    Article  CAS  Google Scholar 

  • Sulston J, Hodgkin J (1998) Methods. In: Wood WB (ed) The Nematode Caenorhabditis elegans. Cold Spring Harbor Laboratory Press, New York, pp 587–606

    Google Scholar 

  • Vanfleteren JR, De Vreese A, Braeckman BP (1998) Two-parameter logistic and Weibull equations provide better fits to survival data from isogenic populations of Caenorhabditis elegans in axenic culture than does the Gompertz model. J Gerontol A Biol Sci Med Sci 53:B393–B403; discussion B404–B408

  • Weeks BS, Hanna MS, Cooperstein D (2012) Dietary selenium and selenoprotein function. Med Sci Monit 18(8):RA127–RA132

    Article  CAS  Google Scholar 

  • Williams PL, Dusenbery DB (1990) A promising indicator of neurobehavioral toxicity using the nematode Caenorhabditis elegans and computer tracking. Toxicol Ind Health 6:425–440

    Article  CAS  Google Scholar 

  • Wren JF, Kille P, Spurgeon DJ, Swain S, Sturzenbaum SR, Jager T (2011) Application of physiologically based modelling and transcriptomics to probe the systems toxicology of aldicarb for Caenorhabditis elegans (Maupas 1900). Ecotoxicology 20:397–408

    Article  CAS  Google Scholar 

  • Wu D, Cypser JR, Yashin AI, Johnson TE (2008) The U-shaped response of initial mortality in Caenorhabditis elegans to mild heat shock: does it explain recent trends in human mortality? J Gerontol A Biol Sci Med Sci 63:660–668

    Google Scholar 

  • Yen K, Steinsaltz D, Mobbs CV (2008) Validated analysis of mortality rates demonstrates distinct genetic mechanisms that influence lifespan. Exp Gerontol 43:1044–1051

    Article  Google Scholar 

Download references

Acknowledgments

This work was financially supported in part by Grants (NSC 100-2313-B-002-013 and NSC 101-2313-B-002-041-MY3) from the National Science Council of Taiwan to V. H.-C. Liao.

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The authors declare that they have no conflict of interest.

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Correspondence to Vivian Hsiu-Chuan Liao.

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Li, WH., Ju, YR., Liao, CM. et al. Assessment of selenium toxicity on the life cycle of Caenorhabditis elegans . Ecotoxicology 23, 1245–1253 (2014). https://doi.org/10.1007/s10646-014-1267-x

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  • DOI: https://doi.org/10.1007/s10646-014-1267-x

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