Identifying Euglena Gracilis Metabolic and Transcriptomic Adaptations in Response to Mercury Stress

Abstract

Mercury contamination in aquatic systems poses a serious environmental stress to phototrophic plankton. We used Euglena gracilis to gain an understanding of the physiochemical changes resulting from mercury stress across the transcriptome and metabolome. Using a combination of Fourier Transform Ion Cyclotron Resonance Mass Spectrometry (FT-ICR-MS) and RNA-sequencing, we identified metabolomic and transcriptomic changes both within and outside cellular space after mercury exposure. Metabolic profiles of E. gracilis were less diverse after mercury exposure, highlighting an overall refinement of metabolites produced. Significant fold changes in cysteine, glutathione, and amino acid-based metabolites were significantly higher (p < 0.05) within the mercury exposed cells and in extracellular space than in untreated cultures. Using integrated omics analyses, a significant upregulation of transcripts and metabolites involved in amino acid synthesis, cellular responses to chemical stress, reactive oxygen species detoxification, and electron transport were identified. Together the enrichment of these pathways highlights mechanisms that E. gracilis harness to mitigate oxidative stress at sublethal concentrations of mercury exposure and give rise to new biomarkers of environmental stress in the widely distributed E. gracilis.

Role of phytoplankton in aquatic mercury speciation and transformations

“…Phytoplankton species could control intracellular Hg speciation and thus affect the intracellular transformations by cytosolic ligands. It has been shown that the quantity and the quality of the intracellular metabolites, which could interact with Hg species, are altered by iHg exposure (Mangal et al 2022). Glutathione (GSH) content, which is the most prevalent thiol in algae, was found to increase in algae exposed to iHg (Howe and Merchant 1992, Devars et al 2000, Morelli et al 2009.…”

“…The development of the Hg stable isotope fractionation approach opens up the possibility to decipher the contribution of interconnected abiotic and biotic transformation (Kritee et al 2013) and to track further the processes controlling origin and cycling of Hg before its incorporation in the foodweb (Bouchet et al 2022). Since the biotic transformations are considered prevailing, the development of the novel -omics approaches would provide key information on the interactions between Hg and phytoplankton species (Beauvais-Flück et al 2016, Beauvais-Flück et al 2018, Mangal et al 2022. These approaches can be used to design the strategies to understand the mechanisms of Hg-induced metabolic perturbations and to explore their Identifying specific organelles and cellular compartments where Hg species accumulate and can be transformed could be also of added value, given the importance of cellular speciation and distribution in the toxicity, detoxification and trophic transfer of mercury (Wu and Wang 2011).…”

The impact of elevated sulfur and nitrogen levels on cadmium tolerance in Euglena species

“…Exposing E. gracilis to low concentrations of HgCl 2 for at least 60 generations resulted in metabolic adaptations that enhanced its ability to accumulate CdCl 2 [10]. Recent metabolomic analysis identi ed metal-binding compounds produced by E. gracilis that are enriched in S and N [13,14]. These results lead to the hypothesis that a pre-treatment of both E. gracilis and E. mutabilis with elevated levels of S or N would increase Euglena's tolerance to Cd.…”

Influence of Carbon Sources on the Phenolic Compound Production by Euglena gracilis Using an Untargeted Metabolomic Approach

“…Euglena gracilis also shows high adaptation capacities for a broad range of environmental conditions [ 10 ] through the plasticity of its atypical and unique metabolism [ 6 , 11 ], including its ability to tolerate high concentrations of metals (ppm range) [ 12 ] via the production of chelating ligands [ 13 ]. These studies focused mainly on primary metabolites production, but little is known in terms of secondary metabolites [ 14 ]. Secondary metabolites are specialized compounds produced in response to environmental changes [ 15 ].…”

“…They play a key role in the defense mechanism against abiotic and biotic stress via their anti-allergenic, anti-microbial, anti-inflammatory and antioxidant properties [ 16 , 17 ]. For example, oxidative stress led to the formation of oxidative compounds and free radicals, and the breakdown of photosynthetic and metabolic enzymes [ 14 , 18 ].…”