Marine and freshwater micropearls: biomineralization producing strontium-rich amorphous calcium carbonate inclusions is widespread in the genus Tetraselmis (Chlorophyta)

Unicellular algae play important roles in the biogeochemical cycles of numerous elements, particularly through the biomineralization capacity of certain species (e.g., coccolithophores greatly contributing to the "organic carbon pump" of the oceans), and unidentified actors of these cycles are still being discovered. This is the case of the unicellular alga Tetraselmis cordiformis (Chlorophyta) that was recently discovered to form intracellular mineral inclusions, called micropearls, which had been previously overlooked. These intracellular inclusions of hydrated amorphous calcium carbonates (ACCs) were first described in Lake Geneva (Switzerland) and are the result of a novel biomineralization process. The genus Tetraselmis includes more than 30 species that have been widely studied since the description of the type species in 1878. The present study shows that many other Tetraselmis species share this biomineralization capacity: 10 species out of the 12 tested contained micropearls, including T. chui, T. convolutae, T. levis, T. subcordiformis, T. suecica and T. tetrathele. Our results indicate that micropearls are not randomly distributed inside the Tetraselmis cells but are located preferentially under the plasma membrane and seem to form a definite pattern, which differs among species. In Tetraselmis cells, the biomineralization process seems to systematically start with a rod-shaped nucleus and results in an enrichment of the micropearls in Sr over Ca (the Sr/Ca ratio is more than 200 times higher in the micropearls than in the surrounding water or growth medium). This concentrating capacity varies among species and may be of interest for possible bioremediation techniques regarding radioactive Sr-90 water pollution. The Tetraselmis species forming micropearls live in various habitats, indicating that this novel biomineralization process takes place in different environments (marine, brackish and freshwater) and is therefore a widespread phenomenon.