Multigenerational exposure to silver ions and silver nanoparticles reveals heightened sensitivity and epigenetic memory inCaenorhabditis elegans

Abstract

The effects from multigenerational exposures to engineered nanoparticles (ENPs) in their pristine and transformed states are currently unknown despite such exposures being an increasingly common scenario in natural environments. Here, we examine how exposure over 10 generations affects the sensitivity of the nematode Caenorhabditis elegans to pristine and sulfidized Ag ENPs and AgNO 3 . We also include populations that were initially exposed over six generations but kept unexposed for subsequent four generations to allow recovery from exposure. Toxicity of the different silver forms decreased in the order AgNO 3 , Ag ENPs and Ag 2 S ENPs. Continuous exposure to Ag ENPs and AgNO 3 caused pronounced sensitization (approx. 10-fold) in the F2 generation, which was sustained until F10. This sensitization was less pronounced for Ag 2 S ENP exposures, indicating different toxicity mechanisms. Subtle changes in size and lifespan were also measured. In the recovery populations, the sensitivity to Ag ENPs and AgNO 3 resulting from the initial multigenerational exposure persisted. Their response sensitivity for all endpoints was most closely related to the last ancestral exposed generation (F5), rather than unexposed controls. The mechanisms of transgenerational transfer of sensitivity are probably organized through the epigenome, and we encourage others to investigate such effects as a priority for mechanistic toxicology.

Transgenerational interactions between pesticide exposure and warming in a vector mosquito

“…Together, our results underscore the importance of considering transgenerational plasticity not only when assessing the impact of warming (e.g., Donelson et al., ; Shama et al., ; Veilleux et al., ) and of pollutants (e.g., Costa et al., ; Pölkki et al., ; Schultz et al., ), but also when considering the impact of pollutants in a warming world. Our results thereby highlight the importance of integrating the emerging views of multistressor studies (Liess et al., ; Stoks, Geerts, & De Meester, ) and studies on transgenerational plasticity (Donelson et al., ; Guillaume et al., ) to understand the fate of species under global change.…”

“…Again, these differences may be due to the magnitude of the warming imposed (Donelson et al., ). Also for contaminants, there is mixed evidence in invertebrates: some studies showed parental exposure increasing the tolerance of the offspring (e.g., Brausch & Salice, ; Kim et al., ; Reátegui‐Zirena et al., ), while other studies showed the opposite (Pölkki et al., ; Schultz et al., ; Yu et al., ).…”

“…Transgenerational effects have been described both in response to warming (e.g., Munday, ; Salinas & Munch, ; Shama et al., ) and to pesticide exposure (e.g., Brausch & Salice, ; Kim, Yu, Jeong, & Kim, ) and raise the concern whether we can reliably predict the biological impact of these stressors based on single‐generation experiments (Kim et al., ; Yu, Zhang, & Yin, ). Indeed, transgenerational effects can make offspring both more (e.g., Pölkki, Kangassalo, & Rantala, ; Schultz et al., ) or less (e.g., Brausch & Salice, ; Kim et al., ; Reátegui‐Zirena et al., ) vulnerable to stressors compared to the parental generation. The emerging view based on recent empirical studies on warming is that transgenerational plasticity may buffer the negative effects of warming on ectotherms (Munday, ; Shama et al., ), yet this may be biased because of methodological weaknesses in the design of the studies (Kielland, Bech, & Einum, ).…”

Multigenerational exposure of populations of Oppia nitens to zinc under pulse and continuous exposure scenarios

“…One of such mechanism is epigenesis. Histome modification, another epigenetic mechanism, caused inhibition of vulval development in C. elegans (Andersen and Horvitz 2007;Schultz et al 2016). For example, the earthworm Lumbricus rubellus from an arseniccontaminated field soil tolerated arsenic exposure because its altered DNA methylation was transferred from the parents (Kille et al 2013).…”

“…In addition to epigenesis, multigenerational exposure can cause teratogenesis, in which the embryo or fetus is malformed due to embryo exposure to chemicals (Vargesson and Fraga 2017). There can also be a direct maternal transfer of metals to other generations (Kim et al 2013;Schultz et al 2016). For example, exposure to lead caused leg malformation in the larval and nymphal stage of the mite A. longisetosus (Kohler et al 2005).…”