Effect of extracellular polymeric substances on arsenic accumulation in Chlorella pyrenoidosa

Abstract

Inorganic arsenic (iAs) in its dominant dissolved phase in the environment is known to pose major threats to ecological and human health. While the biological effects in many arsenic-bearing freshwaters have been extensively studied, the behavior and bioaccumulation of dissolved iAS in the presence of extracellular polymeric substances (EPS) still remains to be a critical knowledge gap. In this study, the uptakes and kinetic characteristics of iAs were studied using Chlorella pyrenoidosa (a typical freshwater green algae) by addressing the different effects of EPS on arsenite (AsШ) and arsenate (AsV). The arsenic uptake capacity increased as the exposure concentration increased from 0 to 300 µmol L−1, and the uptake rate constants (Ku) in the Bio-dynamic model were greater for AsV than AsШ (0.63–11.57 L g−1 h−1 vs. 0.44–5.43 L g−1 h−1). The toxic effects as mitigated by EPS were observed through the morphological changes of algal cells by TEM and SEM. When compared with the EPS-free algal cells (EPS-F), EPS-covered cells (EPS-C) had a higher arsenic adsorption capacity through EPS-enhanced surface adsorption and reduced intracellular uptake. The overall decrease (35% and 23.3% for AsШ and AsV, respectively) in the maximum uptake capacity in intact algae cells favors cell’s tolerance to the toxic effects of iAs. These observed discrepancies between AsШ and AsV and between EPS-C and EPS-F were further elucidated through morphological images (TEM and SEM) and molecular/atomic spectroscopic data that combine three-dimensional excitation-emission matrix fluorescence spectroscopy (3D-EEM), Fourier transform infrared spectroscopy (FTIR) and X-ray photoelectron spectroscopy (XPS). Altogether, the spectroscopic evidence revealed the interactions of iAs with C–O–C, C–O–H and –NH2 functional groups in EPS’ tyrosine- and tryptophan-like proteins as the binding sites. Overall, this study for the first time provides comprehensive evidence on the iAs-EPS interactions. Such insights will benefit our understanding of the biogeochemical processes of iAs and the strategic development of bioremediation techniques involving microalgae in the natural and engineered systems.