Integrated cellular and molecular responses to uranium chemotoxicity in the metal-tolerant microalga Coelastrella sp. PCV
Camille Beaulier, Fabienne Devime, Adrien Galeone, Grégory Si LarbiiD, Abir IsraeliD, Pierre‐Henri JouneauiD, Jonathan Przybyla‐ToscanoiD, Claude AlbaniD, Stéphane RavaneliD
Abstract
Understanding the toxicity of hazardous metals in microalgae is critical for environmental risk assessment and sustainable phycoremediation. Metal-tolerant organisms provide powerful models for dissecting the mechanisms that mitigate metal toxicity. Here, we investigated the cellular and molecular responses to uranium (U) chemotoxicity in the metal-tolerant microalga Coelastrella sp. PCV. We used an integrated multi-omics and high-resolution imaging approach, combined with physiological analyses, to elucidate the mechanisms underlying U tolerance in Coelastrella. Using TEM-EDX, U was localized to the cell wall, polyphosphate bodies within acidocalcisomes, and vacuoles. Three-dimensional cell reconstruction and morphometric analysis using FIB-SEM showed that U-challenged cells displayed increased vacuolization, reflecting sequestration of uranyl ions and autophagy-mediated detoxification. Transcriptome responses were rapid and extensive, characterized by repression of cell division and photosynthesis, and pronounced imbalance in protein turnover and trafficking. Uranium also disrupted the homeostasis of essential elements, with marked rewiring of gene networks governing molybdenum, manganese, phosphate, iron and calcium homeostasis, notably affecting transporters and metal-binding proteins. Coelastrella sp. PCV efficiently sequestered U in acidocalcisomes and vacuoles, while rapidly excluding U from the cell. These coordinated detoxification responses are likely mediated by calcium, iron, ABC, and MATE transporters among the strongly deregulated genes under U stress.
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