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

Abstract

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 Ca ²⁺ signalling is involved in diatom osmotic sensing. However, mechanistic insight of the role of osmotic Ca ²⁺ signalling is limited. Here, we show that Phaeodactylum Ca ²⁺ elevations are essential for surviving hypo-osmotic shock. Moreover, employing novel single-cell imaging techniques we have characterised real-time Ca ²⁺ signalling responses in single diatom cells to environmental osmotic perturbations. We observe that intracellular spatiotemporal patterns of osmotic-induced Ca ²⁺ elevations encode vital information regarding the nature of the osmotic stimulus. Localised Ca ²⁺ 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 Ca ²⁺-independent and dependent mechanisms for osmoregulation. We find that efflux of organic osmolytes occurs in a Ca ²⁺-independent manner, but this response is insufficient to mitigate cell damage during hypo-osmotic shock. By comparison, Ca ²⁺-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.

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