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NMR-based metabolomics and LC-MS/MS quantification reveal metal-specific tolerance and redox homeostasis in Chlorella vulgaris.

Live green algae are promising candidates for phytoremediation, but a suitable algal species which bio-accumulates high concentrations of heavy metals, and survives well in industrial water is yet to be identified. Potential metabolic engineering may be applied to improve algal phytoremediation performance, but the metal tolerance and bioaccumulation mechanisms in green algae have to be first fully understood. In this study, NMR-based metabolomics was used to study the effect of different metal species (copper, cadmium and lead) and metal concentrations in green microalgae, Chlorella vulgaris. High Cu concentrations influenced substantial decrease in organic osmolytes (betaine and glycerophosphocholine), which indicated Cu-induced redox imbalance. Accompanying redox imbalance, growth inhibition and photosynthesis impairments in Cu-spiked C. vulgaris revealed a clear relationship between Cu toxicity and redox homeostasis. As these metabolic changes were less prominent in Cd and Pb-spiked cultures, we inferred metal-specific toxicity in C. vulgaris, where redox active Cu(2+) is more potent than non-redox active Cd(2+) and Pb(2+) in causing redox imbalance. Subsequently, ICP-MS and LC-MS/MS quantification shed light on the metal-specific bioaccumulation and detoxification mechanisms. The metal bioconcentration factor (BCF) correlated well with the phytochelatin (PC) content in Cu and Cd-spiked C. vulgaris biomass. High BCF and PC levels with increasing Cu and Cd exposure concentrations indicated that PCs played a significant role in Cu and Cd bioaccumulation and detoxification. In contrast, the undetectable PC levels in Pb-spiked cultures despite high Pb BCF suggest an alternative detoxification mechanism for Pb: either by passive absorption to the algal cell wall or interaction with glutathione (GSH).