Integrative assessment of low-dose gamma radiation effects on Daphnia magna reproduction: Toxicity pathway assembly and AOP development

You Song,Li Xie,Yeonkyeong Lee,Dag Anders Brede,Fern Lyne,Yetneberk Kassaye,Jens Thaulow,Gary Caldwell,Brit Salbu,Knut Erik Tollefsen

doi:10.1016/j.scitotenv.2019.135912

Abstract

High energy gamma radiation is potentially hazardous to organisms, including aquatic invertebrates. Although extensively studied in a number of invertebrate species, knowledge on effects induced by gamma radiation is to a large extent limited to the induction of oxidative stress and DNA damage at the molecular/cellular level, or survival, growth and reproduction at the organismal level. As the knowledge of causal relationships between effects occurring at different levels of biological organization is scarce, the ability to provide mechanistic explanation for observed adverse effects is limited, and thus development of Adverse Outcome Pathways (AOPs) and larger scale implementation into next generation hazard and risk predictions is restricted. The present study was therefore conducted to assess the effects of high-energy gamma radiation from cobalt-60 across multiple levels of biological organization (i.e., molecular, cellular, tissue, organ and individual) and characterize the major toxicity pathways leading to impaired reproduction in the model freshwater crustacean Daphnia magna (water flea). Following gamma exposure, a number of bioassays were integrated to measure relevant toxicological endpoints such as gene expression, reactive oxygen species (ROS), lipid peroxidation (LPO), neutral lipid storage, adenosine triphosphate (ATP) content, apoptosis, ovary histology and reproduction. A non-monotonic pattern was consistently observed across the levels of biological organization, albeit with some variation at the lower end of the dose-rate scale, indicating a complex response to radiation doses. By integrating results from different bioassays, a novel pathway network describing the key toxicity pathways involved in the reproductive effects of gamma radiation were proposed, such as DNA damage-oocyte apoptosis pathway, LPO-ATP depletion pathway, calcium influx-endocrine disruption pathway and DNA hypermethylation pathway. Three novel AOPs were proposed for oxidative stressor-mediated excessive ROS formation leading to reproductive effect, and thus introducing the world's first AOPs for non-chemical stressors in aquatic invertebrates.

Highlights

Regulatory and public concerns for the environmental impact of ionizing radiation have been raised after major nuclear events such as the Chernobyl and Fukushima accidents
Crustaceans are key primary consumers connecting primary producers and higher consumers in many food webs (Burns and Schallenberg, 1996; Covich et al, 1999). Aquatic crustaceans such as the water flea Daphnia magna have been widely used as indicators for ecosystem health and as standard species in regulatory toxicity tests for ecological hazard and risk assessment (OECD, 2012). Freshwater crustaceans such as Asellus aquaticus and Daphnia occur in contaminated lakes and ponds in Chernobyl (Fuller et al, 2017; Goodman et al, 2019), with the frequency of studies on the adverse effects of ionizing radiation increasing over the past decades to reflect their high ecological relevance (reviewed in Dallas et al (2012) and Fuller et al (2015))
Ubiquitinconjugating enzyme E2–17 kDa (Ube2) displayed monotonic dosedependent up-regulation (Fig. 1). Other genes such as Cu/Zn superoxide dismutase (Sod), H+ transporting mitochondrial F1 complex ATP synthase alpha subunit 1 (Atp5a1), peroxisome proliferator-activated receptor gamma coactivator-related protein (Ppar-g), vitellogenin fused with superoxide dismutase (Vtg1), glycine N-methyltransferase (Gnmt) and ten-eleven translocation-2 (Tet2) showed more complex patterns of dose-response relationships

Summary

Introduction

Regulatory and public concerns for the environmental impact of ionizing radiation have been raised after major nuclear events such as the Chernobyl and Fukushima accidents. Crustaceans are key primary consumers (herbivores) connecting primary producers and higher consumers (carnivores) in many food webs (Burns and Schallenberg, 1996; Covich et al, 1999) Aquatic crustaceans such as the water flea Daphnia magna have been widely used as indicators for ecosystem health and as standard species in regulatory toxicity tests for ecological hazard and risk assessment (OECD, 2012). Freshwater crustaceans such as Asellus aquaticus and Daphnia occur in contaminated lakes and ponds in Chernobyl (Fuller et al, 2017; Goodman et al, 2019), with the frequency of studies on the adverse effects of ionizing radiation increasing over the past decades to reflect their high ecological relevance (reviewed in Dallas et al (2012) and Fuller et al (2015))

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