Interactions of thallium with marine phytoplankton

Abstract

Thallium (Tl) is the most toxic metal for mammals, likely due to its chemical similarity to the bioessential potassium (K). The biogeochemical cycle of Tl is susceptible to perturbation from a number of anthropogenic activities. Tl accumulation in the food chain may cause chronic Tl poisoning from dietary intake for human beings. However, Tl accumulation in the marine biosphere has largely been overlooked because high concentrations of K are thought to inhibit any uptake of Tl by organisms. Here, for the first time, high accumulation of Tl in the cytosol by the ubiquitous and abundant marine phytoplankton Emiliania huxleyi was found, making it readily transferable to higher trophic levels. Dose-response and physiological data were presented from a range of 9 species of phytoplankton under a wide range of Tl concentrations (1 ng L−1 to 1 mg L−1), spanning modern open ocean concentrations of 10–20 ng L−1, and higher concentrations in the coastal and fresh waters. Of all phytoplankton studied here, the cyanobacteria Synechococcus and the haptophytes Isochrysis galbana and Pavlova granifera have the largest tolerance to Tl toxicity, while the chlorophyte Micromonas pusilla has the least tolerance to elevated Tl. Haptophytes, especially isochrysidales, accumulated significantly more Tl intracellularly (up to 300-fold higher) than chlorophytes, making them good candidates for Tl bioremediation studies. Potassium transporters from E. huxleyi are found to be different from all other phytoplankton in this study based on analyses of the proteome. Since Tl is well known to be taken into cells by mistake through potassium channels, the difference of K channels in E. huxleyi may be responsible for its highest accumulation of Tl. As one of the most widely distributed phytoplankton in the ocean, the bioaccumulation of Tl in E. huxleyi may transfer and concentrate through the marine food chain and have significant impacts on the Tl biogeochemical cycle in the modern ocean.