Spatiotemporal patterns of intracellular Ca²⁺ signalling govern hypo‐osmotic stress resilience in marine diatoms

Abstract

Summary Diatoms are globally important phytoplankton that dominate coastal and polar‐ice assemblages. These environments exhibit substantial changes in salinity over dynamic spatiotemporal regimes. Rapid sensory systems are vital to mitigate the harmful consequences of osmotic stress. Population‐based analyses have suggested that Ca2+ signalling is involved in diatom osmotic sensing. However, mechanistic insight of the role of osmotic Ca2+ signalling is limited. Here, we show that Phaeodactylum Ca2+ elevations are essential for surviving hypo‐osmotic shock. Moreover, employing novel single‐cell imaging techniques we have characterised real‐time Ca2+ signalling responses in single diatom cells to environmental osmotic perturbations. We observe that intracellular spatiotemporal patterns of osmotic‐induced Ca2+ elevations encode vital information regarding the nature of the osmotic stimulus. Localised Ca2+ signals evoked by mild or gradual hypo‐osmotic shocks are propagated globally from the apical cell tips, enabling fine‐tuned cell volume regulation across the whole cell. Finally, we demonstrate that diatoms adopt Ca2+‐independent and dependent mechanisms for osmoregulation. We find that efflux of organic osmolytes occurs in a Ca2+‐independent manner, but this response is insufficient to mitigate cell damage during hypo‐osmotic shock. By comparison, Ca2+‐dependent signalling is necessary to prevent cell bursting via precise coordination of K+ transport, and therefore is likely to underpin survival in dynamic osmotic environments.

Strain-specific transcriptional responses overshadow salinity effects in a marine diatom sampled along the Baltic Sea salinity cline

“…Altogether, these data highlight intraspecific differences in how salinity stress affects cell functioning, including cell-signaling pathways. For example, Ca 2+ -signaling is involved in osmotic sensing in diatoms [ 88 ], suggesting strains differ in how they respond to osmotic stress.…”

Genome analysis of Parmales, a sister group of diatoms, reveals the evolutionary specialization of diatoms from phago-mixotrophs to photoautotrophs

“…Diatoms also exhibit action potential signalling to modulate their cellular motility 22,23 . Furthermore, parmaleans encode a strikingly greater number of calcium-binding proteins (up to 300) that could act as messenger molecules 24 (Fig. 2b).…”

Genotype-specific transcriptional responses overshadow salinity effects in a marine diatom sampled along the Baltic Sea salinity cline

“…11), highlighting intraspecific differences in how salinity stress affects protein function and cell-signalling pathways. For example, Ca 2+ -signalling is involved in osmotic sensing in diatoms [72], suggesting S. marinoi genotypes differ in how they perceive and respond to osmotic stress.…”