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Silver Accumulation in the Green Microalga Coccomyxa actinabiotis: Toxicity, in Situ Speciation, and Localization Investigated Using Synchrotron XAS, XRD, and TEM

Leonardo, T.; Farhi, E.; Pouget, S.; Motellier, S.; Boisson, A. M.; Banerjee, D.; Rebeille, F.; Den Auwer, C.; Rivasseau, C.

Abstract

Microalgae are good candidates for toxic metal remediation biotechnologies.
This study explores the cellular processes implemented by the green microalga Coccomyxa actinabiotis to take up and cope with silver over the concentration range of 10−7 to 10−2 M Ag+. Understanding these processes enables us to assess the potential of this microalga for applications for bioremediation. Silver in situ speciation and localization were investigated using X-ray absorption spectroscopy, X-ray diffraction, and transmission electron microscopy. Silver toxicity was evaluated by monitoring microalgal growth and photochemical parameters. Different accumulation mechanisms were brought out depending on silver concentration. At low micromolar concentration, microalgae fixed all silver initially present in solution, trapping it inside the cells into the cytosol, mainly as unreduced Ag(I) bound with molecules containing sulfur. Silver was efficiently detoxified. When concentration increased, silver spread throughout the cell and particularly entered the chloroplast, where it damaged the photosystem. Most silver was reduced to Ag(0) and aggregated to form crystalline silver nanoparticles of face-centered cubic structure with a mean size of 10 nm. An additional minor interaction of silver with molecules containing sulfur indicated the concomitant existence of the mechanism observed at low concentration or nanoparticle capping. Nanoparticles were observed in chloroplasts, in mitochondria, on the plasma membrane, on cytosolic membrane structures, and in vacuoles. Above 10−4MAg+, damages were irreversible, and photosynthesis and growth were definitely inhibited. However, high silver amounts remained confined inside microalgae, showing their potential for the bioremediation of contaminated water.

Keywords: Algae; Ag; Coccomyxa actinabiotis; EXAFS

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