Long-term exposure of the isopod Porcellionides pruinosus to nickel: Costs in the energy budget and detoxification enzymes

Abstract

Terrestrial isopods from the species Porcellionides pruinosus were exposed to the maximum allowed nickel concentration in the Canadian framework guideline (50 mg Ni/kg soil) and to 5× this concentration (250 mg Ni/kg soil). The exposure lasted for 28 days and was followed by a recovery period of 14 days where organisms were changed to clean soil. Organisms were sampled after 24 h, 48 h, 96 h, 7 days, 14 days, 21 days, and 28 days of exposure, and at days 35 and 42 during the recovery period. For each sampling time the acetylcholinesterase (AChE), glutathione-S-transferases (GST), catalase (CAT), lactate dehydrogenase (LDH) activities were determined as well as lipid peroxidation rate (LPO) along with lipids, carbohydrates, proteins content, energy available (Ea), energy consumption (Ec) and cellular energy allocation (CEA). The integrated biomarker response (IBR) was calculated for each sampling time as well as for each one of the above parameters. In addition, mortality was also recorded throughout the assay. The results obtained showed that nickel induced oxidative stress, evidenced by results on GST, GPx, CAT or LPO, but also on changes in the energy reserves content of these organisms. In addition, this study showed that these organisms possess a specific strategy to handle nickel toxicity. In this case, biomarkers were associated with costs in the energy budget, and the increase of energy reserves has a compensation for that cost.

Metabolic responses of the isopod Porcellionides pruinosus to nickel exposure assessed by 1H NMR metabolomics

“…[20,25]). Recently, our group has addressed the response of terrestrial isopods to long-term Ni exposure by measuring changes in energy reserves and the activity of detoxification enzymes [12]. This study confirmed the induction of oxidative stress and further revealed that other modes of action should be responsible for Ni toxicity, thus calling for a more detailed understanding of Ni effects at the molecular level.…”

“…In particular, the metabolome was found to change in a dynamic, non-linear way with time and dose, showing, for most metabolites, distinct patterns between the initial and later time points tested (4 and 7/14 days). Interestingly, the mortality recorded in a parallel experiment using the same time points and doses [12] showed a similar number of dead animals in control and exposed conditions at day 4, but a significant increase in mortality upon Ni exposure for 14 days. It is thus likely that the metabolic profile characterizing the short-term (4 days) response to Ni reflects the ability of terrestrial isopods to cope with soil contamination.…”

“…Choline may result from the hydrolysis of acetylcholine, a neurotransmission mediator, through the action of the enzyme acetylcholinesterase (AChE) in the synaptic cleft [45,46]. Indeed, in a previous study on the same isopod species, we have found AChE activity to be elevated upon Ni exposure [12], possibly to prevent acetylcholine over-accumulation, which would lead to over-stimulation of cholinergic receptors and disruption of the nervous system function [47]. Furthermore, choline and phosphocholine are important constituents of cell membrane phospholipids and their variation may also relate to membrane degradation processes.…”

“…In previous studies using cell lines [21],d a p h n i d s [22] or fish [23],N i toxicity has been related to oxidative stress, a process commonly induced by metals, which reflects the imbalance between the production of reactive pro-oxidant species and the ability to neutralize their harmful effects. Moreover, Ni is considered a carcinogenic metal, as it has been reported to impact gene transcription and translation processes, and even the phosphate cycle [12,24]. Regarding Ni effects on soil invertebrates, the information available is still very scarce, being focused on bioaccumulation and mortality testing (e.g.…”

“…Terrestrial isopods are macro-invertebrates involved in decomposition processes, vegetal litter fragmentation and recycling of nutrients [8][9][10][11][12][13], therefore being essential to maintain the function and structure of the soil compartment. Exposure to xenobiotics may affect edaphic organisms, consequently changing the overall soil function, and decreasing soil quality and soil services [14].…”