Native-state imaging of calcifying and noncalcifying microalgae reveals similarities in their calcium storage organelles

Coccolithophores are abundant unicellular marine algae that produce calcified scales via a controlled intracellular process. Understanding the cellular controls over the calcification process is a pressing need to predict the influence of changing oceanic conditions on these major contributors to global marine calcification and carbon fluxes. Using several microalgae, and a combination of state-of-the-art cryoelectron and cryo soft X-ray microscopy, we demonstrate that the recently discovered calcium stores of coccolithophores are similar to the common calcium storage organelles of noncalcifying organisms. These results relate questions of environmental and evolutionary significance to a large body of physiological and molecular genetic findings of better-characterized organisms, and therefore provide fresh entry points for understanding calcification in coccolithophores.Calcium storage organelles are common to all eukaryotic organisms and play a pivotal role in calcium signaling and cellular calcium homeostasis. In most organelles, the intraorganellar calcium concentrations rarely exceed micromolar levels. Acidic organelles called acidocalcisomes, which concentrate calcium into dense phases together with polyphosphates, are an exception. These organelles have been identified in diverse organisms, but, to date, only in cells that do not form calcium biominerals. Recently, a compartment storing molar levels of calcium together with phosphorous was discovered in an intracellularly calcifying alga, the coccolithophore Emiliania huxleyi, raising a possible connection between calcium storage organelles and calcite biomineralization. Here we used cryoimaging and cryospectroscopy techniques to investigate the anatomy and chemical composition of calcium storage organelles in their native state and at nanometer-scale resolution. We show that the dense calcium phase inside the calcium storage compartment of the calcifying coccolithophore Pleurochrysis carterae and the calcium phase stored in acidocalcisomes of the noncalcifying alga Chlamydomonas reinhardtii have common features. Our observations suggest that this strategy for concentrating calcium is a widespread trait and has been adapted for coccolith formation. The link we describe between acidocalcisomal calcium storage and calcium storage in coccolithophores implies that our physiological and molecular genetic understanding of acidocalcisomes could have relevance to the calcium pathway underlying coccolithophore calcification, offering a fresh entry point for mechanistic investigations on the adaptability of this process to changing oceanic conditions