Energy-based modelling to assess effects of chemicals on Caenorhabditis elegans: A case study on uranium

Goussen, Benoit; Beaudouin, Rémy; Dutilleul, Morgan; Buisset-Goussen, Adeline; Bonzom, Jean‐Marc; Péry, Alexandre R.R.

doi:10.1016/j.chemosphere.2014.09.006

Cited by 31 publications

(29 citation statements)

References 42 publications

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“…Growing faster and becoming larger may allow individuals to detoxify their bodies, prevent internalization of the pollutant and reduce internal pollutant concentrations (Guedes et al., 2006; Sibly & Calow, 1989). For example, uranium severely affects the intestinal epithelium in the earthworm, Eisenia fetida (Giovanetti et al., 2010) and seems to decrease energy assimilation in C. elegans (Goussen et al., 2015). The presence of uranium in the environment increases the expression of metallothionein‐1 (mtl‐1), which interferes with U accumulation in cells, probably by sequestering and removing uranium from the cells (Jiang et al., 2009).…”

Section: Discussionmentioning

confidence: 99%

“…It accumulates in the cells and affects the intestinal epithelium (Giovanetti, Fesenko, Cozzella, Asencio, & Sansone, 2010), thus reducing energy and nutrient assimilation. In C. elegans , uranium is assumed to decrease the assimilation of energy from food (Goussen et al., 2015). Salt concentration has recently increased in several ecosystems with important sources of salt originating from winter road maintenance, wastewater and intensive irrigation (e.g., Dugan et al., 2017; Müller & Gächter, 2012; Rengasamy, 2006; Verwey & Vermeulen, 2011).…”

Section: Introductionmentioning

confidence: 99%

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Adaptation costs to constant and alternating polluted environments

Dutilleul

Réale

Goussen

et al. 2017

Evolutionary Applications

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Some populations quickly adapt to strong and novel selection pressures caused by anthropogenic stressors. However, this short‐term evolutionary response to novel and harsh environmental conditions may lead to adaptation costs, and evaluating these costs is important if we want to understand the evolution of resistance to anthropogenic stressors. In this experimental evolution study, we exposed Caenorhabditis elegans populations to uranium (U populations), salt (NaCl populations) and alternating uranium/salt treatments (U/NaCl populations) and to a control environment (C populations), over 22 generations. In parallel, we ran common‐garden and reciprocal‐transplant experiments to assess the adaptive costs for populations that have evolved in the different environmental conditions. Our results showed rapid evolutionary changes in life history characteristics of populations exposed to the different pollution regimes. Furthermore, adaptive costs depended on the type of pollutant: pollution‐adapted populations had lower fitness than C populations, when the populations were returned to their original environment. Fitness in uranium environments was lower for NaCl populations than for U populations. In contrast, fitness in salt environments was similar between U and NaCl populations. Moreover, fitness of U/NaCl populations showed similar or higher fitness in both the uranium and the salt environments compared to populations adapted to constant uranium or salt environments. Our results show that adaptive evolution to a particular stressor can lead to either adaptive costs or benefits once in contact with another stressor. Furthermore, we did not find any evidence that adaptation to alternating stressors was associated with additional adaption costs. This study highlights the need to incorporate adaptive cost assessments when undertaking ecological risk assessments of pollutants.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Adaptation costs to constant and alternating polluted environments

Dutilleul

Réale

Goussen

et al. 2017

Evolutionary Applications

Self Cite

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“…The three others have indirect effects on the reproduction in conjunction with effects on growth (assimilation, maintenance, and growth models). Our previous study demonstrated that the mode of action of the uranium on C. elegans is likely to be a decrease of energy assimilation from food 36 …”

Section: ■ Materials and Methodsmentioning

confidence: 99%

Transgenerational Adaptation to Pollution Changes Energy Allocation in Populations of Nematodes

Goussen

Péry

Bonzom

et al. 2015

Environ. Sci. Technol.

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Assessing the evolutionary responses of long-term exposed populations requires multigeneration ecotoxicity tests. However, the analysis of the data from these tests is not straightforward. Mechanistic models allow the in-depth analysis of the variation of physiological traits over many generations, by quantifying the trend of the physiological and toxicological parameters of the model. In the present study, a bioenergetic mechanistic model has been used to assess the evolution of two populations of the nematode Caenorhabditis elegans in control conditions or exposed to uranium. This evolutionary pressure resulted in a brood size reduction of 60%. We showed an adaptation of individuals of both populations to experimental conditions (increase of maximal length, decrease of growth rate, decrease of brood size, and decrease of the elimination rate). In addition, differential evolution was also highlighted between the two populations once the maternal effects had been diminished after several generations. Thus, individuals that were greater in maximal length, but with apparently a greater sensitivity to uranium were selected in the uranium population. In this study, we showed that this bioenergetics mechanistic modeling approach provided a precise, certain, and powerful analysis of the life strategy of C. elegans populations exposed to heavy metals resulting in an evolutionary pressure across successive generations.

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“…37,75 However, it has been found that some of these physiological parameters do not have significant influence on sublethal endpoints, such as growth and reproduction, in worms. 75 It has been suggested that variations in any TBTK data set could be associated with biological variation, experimental, and analytical errors. 76 To determine biomass of small organisms more rigorously, a previous study proposed a method by using tissue-element contents as a proxy for biomass determination.…”

Section: Limitations and Implicationsmentioning

confidence: 99%

“…81 It was found that uranium affected assimilation of energy from food and disrupted growth and reproduction in C. elegans based on the DEBtox model. 75 Taken together, although there are plausible uncertainties in the experiments and the modeling, our toxicity bioassays and the TBTK/TD modeling in worms could be extensively applied in environmental and health-risk analysis. By adopting exposure-and field-based information of Fe 0 NPs, the concentration-response relationships constructed in worms will make substantial progress in a quantitative risk assessment.…”

Section: Limitations and Implicationsmentioning

confidence: 99%

Toxicity-based toxicokinetic/toxicodynamic assessment of bioaccumulation and nanotoxicity of zerovalent iron nanoparticles in <em>Caenorhabditis elegans</em>

Yang¹,

Lin²,

Liao³

2017

IJN

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Elucidating the relationships between the toxicity-based-toxicokinetic (TBTK)/toxicodynamic (TD) properties of engineered nanomaterials and their nanotoxicity is crucial for human health-risk analysis. Zerovalent iron (Fe 0 ) nanoparticles (NPs) are one of the most prominent NPs applied in remediating contaminated soils and groundwater. However, there are concerns that Fe 0 NP application contributes to long-term environmental and human health impacts. The nematode Caenorhabditis elegans is a surrogate in vivo model that has been successfully applied to assess the potential nanotoxicity of these nanomaterials. Here we present a TBTK/TD approach to appraise bioaccumulation and nanotoxicity of Fe 0 NPs in C. elegans . Built on a present C. elegans bioassay with estimated TBTK/TD parameters, we found that average bioconcentration factors in C. elegans exposed to waterborne and food-borne Fe 0 NPs were ~50 and ~5×10 −3 , respectively, whereas 10% inhibition concentrations for fertility, locomotion, and development, were 1.26 (95% CI 0.19–5.2), 3.84 (0.38–42), and 6.78 (2.58–21) μg·g −1 , respectively, implicating that fertility is the most sensitive endpoint in C. elegans . Our results also showed that biomagnification effects were not observed in waterborne or food-borne Fe 0 NP-exposed worms. We suggest that the TBTK/TD assessment for predicting NP-induced toxicity at different concentrations and conditions in C. elegans could enable rapid selection of nanomaterials that are more likely to be nontoxic in larger animals. We conclude that the use of the TBTK/TD scheme manipulating C. elegans could be used for rapid evaluation of in vivo toxicity of NPs or for drug screening in the field of nanomedicine.

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Energy-based modelling to assess effects of chemicals on Caenorhabditis elegans: A case study on uranium

Cited by 31 publications

References 42 publications

Adaptation costs to constant and alternating polluted environments

Adaptation costs to constant and alternating polluted environments

Transgenerational Adaptation to Pollution Changes Energy Allocation in Populations of Nematodes

Toxicity-based toxicokinetic/toxicodynamic assessment of bioaccumulation and nanotoxicity of zerovalent iron nanoparticles in <em>Caenorhabditis elegans</em>

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