Intracellular Metal Compartmentalization in the Green Algal Model System Micrasterias Denticulata (Streptophyta) Measured by Transmission Electron Microscopy-Coupled Electron Energy Loss Spectroscopy1

Abstract

Entry of metals in form of aerosols into areas of high air humidity such as peat bogs represents a serious danger for inhabiting organisms such as the unicellular desmid Micrasterias denticulata Bréb. ex Ralfs (Desmidiaceae, Zynematophyceae, Streptophyta). To understand cellular detoxification and tolerance mechanisms, detailed intracellular localization of metal pollutants is required. This study localizes the metals aluminum (Al), zinc (Zn), copper (Cu), and cadmium (Cd) in the green algal model system Micrasterias after experimental exposure to sulfate solutions by highly sensitive TEM-coupled electron energy loss spectroscopy (EELS). Concentrations of the metals shown to induce inhibiting effects on cell development and cytomorphogenesis were chosen for these experiments. Long-term exposure to these metal concentrations led to a pronounced impact on cell physiology expressed by a general decrease in apparent photosynthesis. After long-term treatment, Zn, Al, and Cu were detected in the cell walls by EELS. Zn was additionally found in vacuoles and mucilage vesicles, and Cu in starch grains and also in mucilage vesicles. Elevated amounts of oxygen in areas where Zn, Al, and Cu were localized suggest sequestration of these metals as oxides. The study demonstrated that Micrasterias can cope differently with metal pollutants. In low doses and during a limited time period, the cells were able to compartmentalize Cu the best, followed by Zn and Al. Cu and Zn were taken up into intracellular compartments, whereas Al was only bound to the cell wall. Cd was not compartmentalized at all, which explains its strongest impact on growth, cell division rate, and photosynthesis in Micrasterias.

Sustainable Sources of Biomass for Bioremediation of Heavy Metals in Waste Water Derived from Coal-Fired Power Generation

“…The high concentrations achieved in our study may be the result of the live algae bioconcentrating within the cell vacuole as well as binding to the cell walls. This provides additional sites for elemental storage in live algae [14], indeed, metals can even be bound in free sugars e.g. arseno-sugars for arsenic [39].…”

“…However, biosorption approaches rely largely on specific binding of elements to active sites on cell walls [6] whereas bioconcentration may occur in numerous cellular structures or compartments, e.g. vacuolar accumulation of heavy metals [14] and can occur simultaneously for metals in different ionic states, cf. anionic or cationic arsenic: Ghimire et al [15].…”

Effects of chlorpyrifos on the growth and ultrastructure of green algae, Ankistrodesmus gracilis

“…Polyphosphate bodies not only store phosphorus and/or are an energy source in the cell, but also contain reserves of several important elements and can even accumulate toxic substances (Jensen, 1993). Compartmentalization of toxic substances, mainly heavy metals, in polyphosphate bodies has been well documented (Jensen and Rachlin, 1984;Volland et al, 2011;Wong et al, 1994); most of these authors agree that polyphosphate bodies function as a mechanism of detoxification or protection of the algae from toxicity.…”

Asymmetry and integration of cellular morphology in Micrasterias compereana

“…In organisms inhabiting water ecosystems, increased developmental instability resulting in asymmetric deviations in morphology of the symmetric body parts has been found to strongly correlate with higher concentrations of environmental stressors, such as organic and inorganic pollutants [64–66]. In Micrasterias species, such analysis could be particularly intriguing with regard to known toxic effects of certain heavy metals such as Cd, Cr, or Al on intracellular architecture, metabolism, and cytomorphogenesis [67–69]. In addition, these toxic ions are typically more soluble in the low pH conditions of the acidic wetlands, which constitute a typical desmid habitat [21, 60].…”