Epigenetic, transcriptional and phenotypic responses in Daphnia magna exposed to low-level ionizing radiation

Jens Thaulow,You Song,Leif C Lindeman,Jorke H Kamstra,Yeonkyeong Lee,Li Xie,Peter Aleström,Brit Salbu,Knut Erik Tollefsen

doi:10.1016/j.envres.2020.109930

Abstract

Ionizing radiation is known to induce oxidative stress and DNA damage as well as epigenetic effects in aquatic organisms. Epigenetic changes can be part of the adaptive responses to protect organisms from radiation-induced damage, or act as drivers of toxicity pathways leading to adverse effects. To investigate the potential roles of epigenetic mechanisms in low-dose ionizing radiation-induced stress responses, an ecologically relevant crustacean, adult Daphnia magna were chronically exposed to low and medium level external 60Co gamma radiation ranging from 0.4, 1, 4, 10, and 40 mGy/h for seven days. Biological effects at the molecular (global DNA methylation, histone modification, gene expression), cellular (reactive oxygen species formation), tissue/organ (ovary, gut and epidermal histology) and organismal (fecundity) levels were investigated using a suite of effect assessment tools. The results showed an increase in global DNA methylation associated with loci-specific alterations of histone H3K9 methylation and acetylation, and downregulation of genes involved in DNA methylation, one-carbon metabolism, antioxidant defense, DNA repair, apoptosis, calcium signaling and endocrine regulation of development and reproduction. Temporal changes of reactive oxygen species (ROS) formation were also observed with an apparent transition from ROS suppression to induction from 2 to 7 days after gamma exposure. The cumulative fecundity, however, was not significantly changed by the gamma exposure. On the basis of the new experimental evidence and existing knowledge, a hypothetical model was proposed to provide in-depth mechanistic understanding of the roles of epigenetic mechanisms in low dose ionizing radiation induced stress responses in D. magna.

Highlights

Organisms are constantly exposed to gamma radiation, a high energy penetrating electromagnetic radiation, from naturally occurring radio nuclides such as uranium and thorium and their progenies, or from artificially produced radionuclides such as nuclear fission (e.g., 137Cs) or activation products (e.g., 60Co) being released to the environments following nuclear weapons tests or nuclear accidents
As a quality control for the analysis, the H3K9ac of the housekeeping gene Actin was found to be highly enriched compared to H3K9me3, whereas no significant differences were found between the treatment groups
Dose-rate dependent increases in histone H3K9me3 enrichment were observed for Dnmt3a1, Dnmt3a2, glycine N-methyl transferase (Gnmt), and methylenetetrahydrofolate reductase (Mthfr), whereas doserate dependent increases in histone H3K9ac enrichment were found for Dnmt3a1, Dnmt3a2 and Gnmt (Fig. 2)

Summary

Introduction

Organisms are constantly exposed to gamma radiation, a high energy penetrating electromagnetic radiation, from naturally occurring radio nuclides such as uranium and thorium and their progenies, or from artificially produced radionuclides such as nuclear fission (e.g., 137Cs) or activation products (e.g., 60Co) being released to the environments following nuclear weapons tests or nuclear accidents. In contaminated areas such as the exclusion zones of Chernobyl and Fukushima, the external dose to living organisms is attributed to gamma radiation from man-made radionuclides. Due to the rather long half-lives of 60Co (5.27 years) and 137Cs (30.17 years) environmental exposure is in most cases long-term and thereby of great concern to both terrestrial and aquatic organisms

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