Bioaccumulation of gadolinium in Tetrahymena: Phagocytotic uptake leads to the formation of gadolinium phosphate–organic composite particles

Abstract

The mechanisms of bioaccumulation in eukaryotic cells, along with the understanding of pathways and metal binding, are fundamental to advances in both basic and applied research. The ciliate Tetrahymena pyriformis bioaccumulates the rare earth element gadolinium (Gd) into food vacuoles and subsequently excretes Gd-containing particles. We investigated the uptake mechanism of Gd in detail and characterised the properties of the resulting biogenic particles. Our results demonstrate that T. pyriformis accumulates Gd³⁺ ions via phagocytosis, with components of the organic cell culture medium playing a central role in mediating the uptake of Gd³⁺ ions. Bioaccumulation occurred in cells cultivated in Gd³⁺-containing environmental water samples and in standard cell culture medium containing proteose peptone, but was absent when Gd³⁺ ions were applied in complexed form, such as gadolinium-based contrast agents. The bioaccumulated and excreted microparticles are amorphous, display magnetic properties, and can be isolated. They consist of about 70 wt% amorphous gadolinium phosphate, 25–27 wt% organic material, and 3 wt% combined Ca, K, Mg, and Na. The individual components can be fractionated based on their solubility. These insights into microbial bioaccumulation of metal elements enhance our understanding of environmental elemental cycles and could provide new strategies for element recovery.