Mercury-Pollution Induction of Intracellular Lipid Accumulation and Lysosomal Compartment Amplification in the Benthic Foraminifer Ammonia parkinsoniana

Abstract

Heavy metals such as mercury (Hg) pose a significant health hazard through bioaccumulation and biomagnification. By penetrating cell membranes, heavy metal ions may lead to pathological conditions. Here we examined the responses of Ammonia parkinsoniana, a benthic foraminiferan, to different concentrations of Hg in the artificial sea water. Confocal images of untreated and treated specimens using fluorescent probes (Nile Red and Acridine Orange) provided an opportunity for visualizing the intracellular lipid accumulation and acidic compartment regulation. With increased Hg over time, we observed an increased number of lipid droplets, which may have acted as a detoxifying organelle where Hg is sequestered and biologically inactivated. Further, Hg seems to promote the proliferation of lysosomes both in terms of number and dimension that, at the highest level of Hg, resulted in cell death. We report, for the first time, the presence of Hg within the foraminiferal cell: at the basal part of pores, in the organic linings of the foramen/septa, and as cytoplasmic accumulations.

Foraminiferal Ultrastructure: A perspective From Fluorescent and Fluorogenic Probes

“…The LD were labeled in yellow, whereas polar lipids are recognized as red spheres (Figure d). A significant increase in LDs in Hg‐treated samples was described, though there was not found a significant difference in their size except for one specimen from the highest Hg concentration (Full results in Frontalini et al, ). These results are in accordance with findings described for other taxa exposed to adverse conditions, such as lichens facing dust pollution (Paoli et al, ) or grey mullet ( Mugil cephalus ) hepatocytes facing heavy metal pollution (Vasanthi et al, ).…”

“…Some of the Hg‐dosed specimens also exhibited diffuse red fluorescence in their chambers, suggesting cytoplasmic acidification. After prolonged incubation, mercury‐exposed specimens appeared to show an acidic compartment decrease as marked by reduction of red vacuoles suggesting a loss of lysosomal activity, a possible signal of recent or imminent death (Frontalini et al, ). Similar results were described in cells of other organisms, such as insects ( Aedes albopictus ; Marigómez et al, ), gastropod mollusk ( Arion ater ; Braeckman & Raes, ), or even foraminifera (Le Cadre & Debenay, ).…”

“…Previously, NR was used on A . parkinsoniana to detect membranous vesicles and to compare the lipidic distributions of specimens with or without exposure to Hg (Frontalini et al, ).…”

“…These LDs appear in a variety of shapes, and they are randomly distributed through all the space in foraminiferal chambers, in agreement with previous studies (LeKieffre et al, 2018). Ammonia parkinsoniana specimens were treated with NR to label and distinguish neutral lipids from polar lipids (e.g., lipidic membranes) on Hg-treated and nontreated samples (Frontalini et al, 2016). The LD were labeled in yellow, whereas polar lipids are recognized as red spheres (Figure 4d).…”

Changes in ultrastructural features of the foraminifera Ammonia spp. in response to anoxic conditions: Field and laboratory observations

“…Occurrence of increased intracellular lipid has been described as a classic symptom of hypoxic cell injury in cellular pathology (e.g., Gordon et al, 1977 and references therein). Other environmental stressors, such as heavy metal toxicity, have been linked to increases in the lipid contents of both marine dinoflagellates (Prévot and Soyer, 1978) and benthic foraminifera (Le Cadre and Debenay, 2006;Frontalini et al, 2016;Frontalini et al, 2017). In mammals, lipid droplet formation has been shown to be a cellular response to detrimental environmental conditions, with cells switching from oxidative phosphorylation to glycolysis and fatty acid synthesis in response to mitochondrial dysfunction, and sequestering resources in lipid droplets (Lee et al, 2013).…”