Development of an ecotoxicological protocol for the deep-sea fauna using the hydrothermal vent shrimp Rimicaris exoculata

Abstract

In light of deep-sea mining industry development, particularly interested in massive-sulphide deposits enriched in metals with high commercial value, efforts are increasing to better understand potential environmental impacts to local fauna. The aim of this study was to assess the natural background levels of biomarkers in the hydrothermal vent shrimp Rimicaris exoculata and their responses to copper exposure at in situ pressure (30MPa) as well as the effects of depressurization and pressurization of the high-pressure aquarium IPOCAMP. R. exoculata were collected from the chimney walls of the hydrothermal vent site TAG (Mid Atlantic Ridge) at 3630m depth during the BICOSE cruise in 2014. Tissue metal accumulation was quantified in different tissues (gills, hepatopancreas and muscle) and a battery of biomarkers was measured: metal exposure (metallothioneins), oxidative stress (catalase, superoxide dismutase, glutathione-S-transferase and glutathione peroxidase) and oxidative damage (lipid peroxidation). Data show a higher concentration of Cu in the hepatopancreas and a slight increase in the gills after incubations (for both exposed groups). Significant induction of metallothioneins was observed in the gills of shrimps exposed to 4μM of Cu compared to the control group. Moreover, activities of enzymes were detected for the in situ group, showing a background protection against metal toxicity. Results suggest that the proposed method, including a physiologically critical step of pressurizing and depressurizing the test chamber to enable the seawater exchange during exposure to contaminants, is not affecting metal accumulation and biomarkers response and may prove a useful method to assess toxicity of contaminants in deep-sea species.

Biogeochemical Regeneration of a Nodule Mining Disturbance Site: Trace Metals, DOC and Amino Acids in Deep-Sea Sediments and Pore Waters

“…LC 50 values for Cd ranged between 521 and 548 µmol/L for shrimp (Brown et al, 2017a). Experiments are usually carried out with spiked Cu and Cd concentrations in the µmol/L range (Auguste et al, 2016;Martins et al, 2017;Mevenkamp et al, 2017). Trace metals are an important part of the biogeochemical cycle of the surface sediment and should be well understood before mining commences.…”

Identifying Toxic Impacts of Metals Potentially Released during Deep-Sea Mining—A Synthesis of the Challenges to Quantifying Risk

“…This differential response may be related to the prominent role of the gill in harboring chemosynthetic symbionts and located at the interface between the internal milieu and external vent environment. Similarly, whilst the induction of metallothionein was significant in Rimicaris exoculata gill tissue after 72 h, this was not the case in muscle tissue (Auguste et al, 2016). In this latter case the differential response seen in different tissues of the shrimp was considered to result from differences in the route of uptake of the metal over the time course of the experiment.…”

“…For example, copper concentrations from the mussel Bathymodiolus azoricus habitat on the Mid-Atlantic Ridge (MAR) have been recorded between 0.17 µM at ∼850 m water depth at Menez Gwen to 2 µM at ∼2,300 m water depth at Rainbow (Kádár et al, 2005) hydrothermal vent sites. Auguste et al (2016) established the effects of copper exposure on the expression of tissue metallothioneins and lipid peroxidation as well as effects of the activity of key antioxidant enzymes in different tissues of the hydrothermal vent shrimp Rimicaris exoculata collected from the TAG hydrothermal vent field on the MAR and maintained at 30 MPa and 10 • C. Shrimp were held in solutions of either ∼25 or ∼250 µg l −1 copper for 72 h, which were at least two orders of magnitude less than the 72-h LC 50 concentration of ∼35,000 µg l −1 for Palaemon varians at 0.1 MPa and 10 • C reported by Brown et al (2017a). Auguste et al (2016) demonstrated that even shrimp that have evolved to live in the metal-rich environment of a hydrothermal vent field (R. exoculata) are sensitive to copper exposure in solution.…”

“…Auguste et al (2016) established the effects of copper exposure on the expression of tissue metallothioneins and lipid peroxidation as well as effects of the activity of key antioxidant enzymes in different tissues of the hydrothermal vent shrimp Rimicaris exoculata collected from the TAG hydrothermal vent field on the MAR and maintained at 30 MPa and 10 • C. Shrimp were held in solutions of either ∼25 or ∼250 µg l −1 copper for 72 h, which were at least two orders of magnitude less than the 72-h LC 50 concentration of ∼35,000 µg l −1 for Palaemon varians at 0.1 MPa and 10 • C reported by Brown et al (2017a). Auguste et al (2016) demonstrated that even shrimp that have evolved to live in the metal-rich environment of a hydrothermal vent field (R. exoculata) are sensitive to copper exposure in solution. Similarly, copper exposure in hydrothermal vent mussels Bathymodioulus azoricus collected from the "Lucky Strike" hydrothermal vent site on the MAR and maintained at 17.5 MPa at ∼6 • C for 96 h caused elevated lipid peroxidation at copper concentrations in excess of 300 µg l −1 , indicating lipid membrane damage within these tissues.…”

“…Reactive species are variously detoxified by enzymes including: superoxide dismutase (SOD), catalase (CAT), and peroxidases (PEROXs) (e.g., Company et al, 2004Company et al, , 2006aCompany et al, ,b, 2007Company et al, , 2008Bebianno et al, 2005;Gonzalez-Rey et al, 2008). Recently, Auguste et al (2016), Martins et al (2017) and Mestre et al (2017) have assessed the potential sub-lethal impacts of exposure to dissolved metals specifically in a range of deep sea species, including molluscs and echinoderms that do not inhabit metal-rich environments, and molluscs and crustaceans from hydrothermal-vent habitats; habitats that are naturally metal rich. For example, copper concentrations from the mussel Bathymodiolus azoricus habitat on the Mid-Atlantic Ridge (MAR) have been recorded between 0.17 µM at ∼850 m water depth at Menez Gwen to 2 µM at ∼2,300 m water depth at Rainbow (Kádár et al, 2005) hydrothermal vent sites.…”