Microaerophilia enhances heavy metal biosorption and internal binding by polyphosphates in photosynthetic Euglena gracilis

Euglena gracilis is a photosynthetic protist with proved ability to resist and remove toxic single heavy metals under different laboratory conditions. To assess these abilities under more realistic conditions, cells subjected to combinations of heavy metals in a defined culture medium as well as in field polluted enriched medium were analyzed. Cells were cultured in the presence of Cd2+plus Cu2+ or Cr(VI) plus Fe3+ under aerobiosis or microaerophilia. Under aerobic growth, Cd2+plus Cu2+ (50 + 80 μM) and Cr(VI) plus Fe3+ (2 + 1 mM) strongly inhibited cell growth by inducing severe oxidative stress. In contrast, under microaerophilia, higher resistance and heavy metal removal were attained. This was indicated by (i) substantial biomass production; (ii) greater activities of glutathione reductase, glutathione peroxidase and ascorbate peroxidase as well as greater amounts of intracellular glutathione and ascorbate; (iii) increased metal removal by biosorption (i.e. greater than 80% for Cd, Cr, and Fe) due to an enhanced biofilm synthesis. The fraction of intracellularly heavy metal accumulated was bound mostly by polyphosphates (polyP). Cells cultured under microaerophilia in heavy metal polluted wastewater and sediments media were also able to grow and remove Fe, Cr, Cu and Cd. It is concluded that microaerophilia favors, the resistance of photosynthetic Euglena gracilis to heavy metal toxicity, and its ability to remove such metals from polluted water and solid samples. This work provides the biochemical basis for designing genetically engineered microorganisms with enhanced efficiency in metal removal. Moreover, it brings forward the combination of physicochemical and biological techniques to profit recovery. [Display omitted] •Euglena was cultured under microaerophilia in presence of heavy metal mixtures.•Microaerophilia but not aerobiosis allowed cell duplication despite metal toxicity.•Biofilm trapped more than 80% of Cd2+, Fe3+ and Cr(VI).•Microaerophilia enhanced 2 times the antioxidant system activity versus aerophilia.•Microaerophilic cells showed metal removal from polluted water and solid samples.