Role of cellular compartmentalization in the trophic transfer of mercury species in a freshwater plant-crustacean food chain

Abstract

Mercury (Hg) represents an important risk for human health through the food webs contamination. Macrophytes bioaccumulate Hg and play a role in Hg transfer to food webs in shallow aquatic ecosystems. Nevertheless, the compartmentalization of Hg within macrophytes, notably major accumulation in the cell wall and its impact on trophic transfer to primary consumers are overlooked. The present work focusses on the trophic transfer of inorganic Hg (IHg) and monomethyl-Hg (MMHg) from the intracellular and cell wall compartments of the macrophyte Elodea nuttallii - considered a good candidate for phytoremediation - to the crustacean Gammarus fossarum. The results demonstrated that Hg accumulated in both compartments was trophically bioavailable to gammarids. Besides IHg from both compartments were similarly transferred to G. fossarum, while for MMHg, uptake rates were ∼2.5-fold higher in G. fossarum fed with the cell wall vs the intracellular compartment. During the depuration phase, Hg concentrations in G. fossarum varied insignificantly suggesting that both IHg and MMHg were strongly bound to biological ligands in the crustacean. Our data imply that cell walls have to be considered as an important source of Hg to consumers in freshwater food webs when developing procedures for enhancing aquatic environment protection during phytoremediation programs.

Effects of cadmium, inorganic mercury and methyl-mercury on the physiology and metabolomic profiles of shoots of the macrophyte Elodea nuttallii

“…High levels of Cd, inorganic Hg (IHg) and methyl-Hg (MeHg) can be observed in aquatic ecosystems colonized by plants (Samecka-Cymerman and Kempers, 2003;Castro et al, 2009;Regier et al, 2013b). Therefore, bioaccumulation of metals in macrophytes represents a significant and current environmental concern (Beauvais-Fluck et al, 2016;Beauvais-Fluck et al, 2017).…”

Subcellular Distribution of Dietary Methyl-Mercury in Gammarus fossarum and Its Impact on the Amphipod Proteome

“…To ensure exclusive exposure of gammarids through plant consumption, water renewal and daily removal of dead individuals was done to avoid exposure to Hg through water or cannibalism, respectively. We observed a weak (15%) mortality of gammarids during exposure in all conditions 10 . This rate agrees with the criteria from the Afnor standard (XP T 90-722-3) for feeding rate measurement in the sentinel species G. fossarum 35 .…”

“…Gammarus fossarum were sampled in the Bourbre River (France) 33,34 , and acclimatized three weeks to laboratory conditions. Nine 1 cm-long males were fed during 7 days with E. nuttallii intracellular (I) or the cell wall (CW) compartments pre-exposed to 4 and 20 µg L -1 MeHg concentrations, thereafter referred as 'low' and 'high' MeHg treatments in line with their concentrations corresponding to lowly and highly contaminated environments, respectively 2,10,11,31 . To ensure exclusive exposure of gammarids through plant consumption, water renewal and daily removal of dead individuals was done to avoid exposure to Hg through water or cannibalism, respectively.…”

“…Similarly, chironomids fed with shopped macrophytes, to mimic incorporation in sediments of decaying tissues, revealed that MeHg was more transferable to sensitive subcellular targets and bioavailable fraction in primary consumers than IHg found in intracellular or cell wall compartments 11 . Data point that the composition of cell walls could affect the transfer rate of Hg to consumers 10,11,21 .…”

“…Moreover, studies on effect of trophic Hg exposure in primary consumers, i.e. invertebrates are rare 10,11,21 . At environmental concentrations, cell walls appeared as the main bioaccumulation compartment of Hg in macrophytes and because of their low degradability are expected to remain for long periods in the aquatic systems, likely serving as food source 25,26,27 .…”