Multigenerational Exposures of Daphnia Magna to Pristine and Aged Silver Nanoparticles: Epigenetic Changes and Phenotypical Ageing Related Effects

Abstract

Engineered nanoparticles (NPs) undergo physical, chemical, and biological transformation after environmental release, resulting in different properties of the "aged" versus "pristine" forms. While many studies have investigated the ecotoxicological effects of silver (Ag) NPs, the majority focus on "pristine" Ag NPs in simple exposure media, rather than investigating realistic environmental exposure scenarios with transformed NPs. Here, the effects of "pristine" and "aged" Ag NPs are systematically evaluated with different surface coatings on Daphnia magna over four generations, comparing continuous exposure versus parental only exposure to assess recovery potential for three generations. Biological endpoints including survival, growth and reproduction and genetic effects associated with Ag NP exposure are investigated. Parental exposure to "pristine" Ag NPs has an inhibitory effect on reproduction, inducing expression of antioxidant stress related genes and reducing survival. Pristine Ag NPs also induce morphological changes including tail losses and lipid accumulation associated with aging phenotypes in the heart, abdomen, and abdominal claw. These effects are epigenetic remaining two generations post-maternal exposure (F2 and F3). Exposure to identical Ag NPs (same concentrations) aged for 6 months in environmentally realistic water containing natural organic matter shows considerably reduced toxicological effects in continuously exposed generations and to the recovery generations.

Mechanistic insights into toxicity pathways induced by nanomaterials in Daphnia magna from analysis of the composition of the acquired protein corona

“…Increasing evidence suggests that the gradual increase in free radicals and oxidative stress with age is the Environmental Science: Nano Paper primary determinant of ageing. 64 The presence of ageing related proteins in the NMs coronas is consistent with the morphological evidence presented previously 34,65 that exposure to Ag NMs results in dramatic tail shortening and increased lipid droplets, two phenotypical traits of ageing, suggesting that the NMs induce accelerated ageing in the developing daphnids. Other proteins which have a high degree of species conservation that were linked to lipid transport, antioxidant processes and developmental processes are copper-zinc superoxide dismutase, vascular endothelial growth factor receptor, and S-adenosylmethionine synthase.…”

“…It was recently shown that the chronic (reproductive) ecotoxicity of Ag and TiO 2 NMs to Daphnia magna is dramatically reduced by environmental ageing of the NMs in media of different ionic strengths and natural organic matter contents. 33,34 Understanding the different proteins acquired by freshly dispersed (pristine engineered) and aged NMs in different environmentally relevant media, and their biological functions will provide important insights into their mechanisms of NM toxicity. Thus, as part of the overall assessment of the NMs chronic toxicity (Ellis et al, 2020 33 ), we characterised the secreted protein coronas that the NMs had acquired after 7 days in contact with Daphnia magna under each of the different medium conditions.…”

The Crucial Role of Environmental Coronas in Determining the Biological Effects of Engineered Nanomaterials

“…[216] Furthermore, after aging for six months in environmentally realistic water containing NOM, there was a considerable reduction in the inhibitory effects on reproduction and antioxidant stressrelated genes on D. magna over four generations from pristine Ag NPs. [217] www.advancedsciencenews.com www.small-journal.com…”

Species Sensitivity to Toxic Substances: Evolution, Ecology and Applications

“…Examples include the observation of the transfer of stress tolerance associated with gene expression changes linked with altered trimethylation of histone H3 lysine 9, identified as a mechanisms for transgenerational inheritance of the maintenance of stressor responses in C. elegans (Klosin et al, 2017) and heritable changes in a DNA methylation in Arabadopsis in response to nickel exposure (Li et al, 2015). A role of epigenetic mechanisms in heritable effects has also been identified in Daphnia magna in response to ionizing radiation (Jeremias et al, 2018;Trijau et al, 2018), silver nanoparticles (Ellis et al, 2020), uranium (Dias et al, 2008;Massarin et al, 2011;Dutilleul et al, 2014;Goussen et al, 2015) and a DNA methylation inhibitor (Lindeman et al, 2019). How these epigenetic mechanisms are linked to sensitivity is currently unknown.…”