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Camille Beaulier

Deciphering the molecular mechanisms underlying the tolerance and accumulation of uranium in a metal-hypertolerant green microalga of the Coelastrella genus

Published on 1 December 2023
Thesis presented December 01, 2023

Abstract:
Uranium (U) pollution of terrestrial and aquatic ecosystems poses a significant threat to the environment and human health because this radionuclide is chemotoxic. Characterization of organisms that tolerate and accumulate U is critical to decipher the mechanisms evolved to cope with the radionuclide and to propose new effective strategies for bioremediation of U-contaminated environments.
In this project, we isolated a unicellular green microalga of the genus Coelastrella from U-contaminated wastewater. We showed that Coelastrella sp. PCV is much more tolerant to U than Chlamydomonas reinhardtii and Chlorella vulgaris. Coelastrella is able to accumulate U very rapidly and, then, progressively release it into the medium, probably to limit the toxic effects of U. The ability of Coelastrella to accumulate U is remarkably high, with up to 600 mg U sorbed per g dry biomass. Coelastrella is able to grow and maintain high photosynthesis in natural metal-contaminated waters from a wetland near a reclaimed U mine. In a single one-week growth cycle, Coelastrella was able to capture 25-55% of U from contaminated waters and demonstrated lipid droplet accumulation. Coelastrella sp. PCV is a very promising microalga for the remediation of polluted waters with valorization of algal biomass that accumulates lipids.​
Transcriptomic, metabolomic and ionomic analyses have also been performed to identify the molecular actors involved in the tolerance and the accumulation of U in Coelastrella sp. PCV. The ontology of genes whose expression is regulated by U stress provides for the first time a global view of the main processes affected by the radionuclide in a green microalga. Genes involved in the cell cycle, translation, photosynthesis and the biosynthesis of amino acids and nucleotides are down regulated during the stress, confirming physiological and metabolomic data (decrease in the pools of proteins, amino acids and nucleotides). The functional categories that are up regulated by U relate to stress response, catabolism, lipid metabolism and transport. For example, many genes encoding proteins involved in the transport of calcium, phosphate and iron are dysregulated during U stress. Some of these genes may play a role in the accumulation and/or in the efflux of U in Coelastrella.
Finally, to better understand the mechanisms of U accumulation in Coelastrella and its consequences on ion homeostasis, different cellular imaging approaches are currently being used. FIB-SEM and STEM-EDX analyses enable us to study the dynamics of cellular compartments during U stress and to identify potential accumulation sites of the radionuclide.

Keywords:
Microalga, uranium, tolerance, accumulation, molecular mechanisms, bioremediation