Mechanisms of Ca2+ Signalling in Diatoms

Abstract

Diatoms are unicellular algae characterised by their two intercalating cell walls made of silica. Diatoms are among the most abundant phytoplankton in the oceans and are key players in the oceanic and global ecosystem, providing a significant contribution to global photosynthetic productivity and oceanic nutrient cycling. Despite their importance and ecological success, little is known on how individual diatom cells monitor abiotic changes in their environment - a crucial undertaking to ensure cell survival. This study presents novel insight into how Ca2+ signalling, a highly versatile and strongly conserved signalling system based on the Ca2+ ion as cellular messenger and initiator of cell responses, helps diatoms to quickly respond and adapt to abiotic changes in their environment. In this study,the centric diatom Thalassiosira pseudonana and the green alga Chlamydomonasreinhardtii were transformed to express fluorescent Ca2+ biosensors. This succeeded for T.pseudonana and the R-GECO1 biosensor, which complemented the existing R-GECO1reporter strain in the pennate diatom Phaeodactylum tricornutum. Using both strains, this study shows that diatom cells exhibit complex spatio-temporal cytosolic Ca2+ elevations in response to hypo-osmotic and cold shocks. P. tricornutum was examined in more detail,which exhibits strongly graded Ca2+ elevations depending on the magnitude and change rate of the decrease in osmolarity and temperature, including localised apical Ca2+elevations and propagating Ca2+ waves. For hypo-osmotic shock, these Ca2+ elevations are vital for cell survival, and also differ between genetically identical yet physiologically different pelagic fusiform and benthic oval morphotype of P. tricornutum. The role of the graded cold shock-induced Ca2+ elevations is not yet resolved, but bear many similarities to cold-shock induced Ca2+ elevations in plants, known to facilitate acclimation to low temperatures. An investigation of diatom ion channels revealed a novel class of two-pore channel (TPCL) that localised to the vacuole membrane. TPCL was only found in diatomgenomes and differs significantly from other TPC channels, including an atypical ionselective motif with negatively charged amino-acid substitutions, suggesting a specialised but yet unknown function in diatoms. Although they are unicellular organisms, diatoms therefore likely exhibit complex signal perception, transduction and deduction pathways rivaling those of more complex multicellular organisms.

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