Dynamics of Cadmium Acclimation in Daphnia pulex: Linking Fitness Costs, Cross-Tolerance, and Hyper-Induction of Metallothionein

Abstract

Acclimation increases tolerance to stress in individuals but is assumed to contribute fitness costs when the stressor is absent, though data supporting this widely held claim are sparse. Therefore, using clonal (i.e., genetically identical) cultures of Daphnia pulex, we isolated the contributions of acclimation to the regulation of the metal response gene, metallothionein 1 (MT1), and defined the reproductive benefits and costs of cadmium (Cd)-acclimation. Daphnia pulex were exposed for 50 parthenogenetic generations to environmentally realistic levels (1 μg Cd/L), and tolerance to Cd and other metals assessed during this period via standard toxicity tests. These tests revealed (1) increased tolerance to Cd compared to genetically identical nonacclimated cultures, (2) fitness costs in Cd-acclimated Daphnia when Cd was removed, and (3) cross-tolerance of Cd-acclimated Daphnia to zinc and silver, but not arsenic, thereby defining a functional role for metallothionein. Indeed, Cd-acclimated clones had significantly higher expression of MT1 mRNA than nonacclimated clones, when Cd exposed. Both the enhanced induction of MT1 and tolerant phenotype were rapidly lost when Cd was removed (1−2 generations), which is further evidence of acclimation costs. These findings provide evidence for the widely held view that acclimation is costly and are important for investigating evolutionary principles of genetic assimilation and the survival mechanisms of natural populations that face changing environments.

Ecological Risk Assessment of Cadmium in Karst Lake Sediments Based on Daphnia pulex Ecotoxicology

“…Cadmium (Cd) is not an essential element for either plant or animal survival and yet one of the most toxic metals [54,55]. However, similar to a previous report [57], this study also found that the less toxicity for the tested daphniids may very likely be due to the Cd competing with calcium (Ca 2+ ) at enzymatic locations in organisms.…”

“…The 96 h LC 50 value is found to be 6.43 × 10 −3 -1753.8 mg L −1 , and its Safe Concentration was evaluated based on the formula SC = 96 h − LC 50 × AF (value of 0.01), calculated as 6.43 × 10 −5 -17.54, or 0.05-14,615 times the D. pulex 96 h LC 50 (0.12 mg L −1 ) and the Safe Concentration (1.20 × 10 -3 mg L −1 ). In comparison to the collected aquatic organisms mentioned above, the D. pulex is one of the most sensitive aquatic species models in particular for cadmium toxicity [54,55]. Moreover, the 96 h LC 50 of some organisms can only be obtained in harsh environments, as highlighted in the literature [51], with the lowest value of 6.43 × 10 −3 mg L −1 .…”

Species Sensitivity to Toxic Substances: Evolution, Ecology and Applications

“…The induction of metallothionein and other metal chaperones following exposure has been widely demonstrated (Scott-Fordsmand and Weeks, 1998;Weeks et al, 2004;Amiard et al, 2006), and as discussed above, basal metallothionein expression has also been linked to metal tolerance (Deeds and Klerks, 1999;Costa et al, 2012). Hence, there is expectation that basal metallothionein expression levels and induction potential could be linked to sensitivity (Shaw et al, 2019). Although systematic studies are lacking, small scale studies have highlighted a potential role for metal binding systems in species response to exposure.…”

“…There is a significant body of evidence for the development of population tolerances to metals in long-term exposed invertebrates, plants and microbial populations (see review of Posthuma and Van Straalen, 1993;Meharg, 2005;Singh et al, 2016;Chandrangsu et al, 2017). Tolerance to metal exposure in animals has been associated with microevolutionary processes that change the expression of metallothioneins and in plants to changes in phytochelatins synthases that together alter the TK processes of metal uptake, transport and detoxification in the adapted species (Dallinger and Hockner, 2013;Weng and Wang, 2014;Zanella et al, 2016;Shaw et al, 2019;Lwalaba et al, 2020;Mekawy et al, 2020). For example, in populations of the Collembola O. cincta, Costa et al (2012) showed that a metal-tolerant phenotype was mainly influenced by cis-genetic factors acting on metallothionein expression, with specific promoter genotypes found dominantly in cadmium tolerant populations.…”

Genome-Wide Analysis of Cadmium-Induced, Germline Mutations in a Long-Term Daphnia pulex Mutation-Accumulation Experiment

“…Primary stocks were made annually by dissolving (analytical grade, Fischer Scientific) in ultrapure water. Test Cd concentrations were verified annually using a magnetic sector inductively coupled plasma/mass spectrometer (ELEMENT; ThermoElectron) fitted with a standard liquid sample introduction system [microconcentric nebulizer (MCN–2; CETAC) and cooled Scott-type spray chamber] at the Dartmouth Trace Element Analysis Core ( Shaw et al. 2019 ).…”