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Spatiotemporal patterns of intracellular Ca 2+ signalling govern hypo‐osmotic stress resilience in marine diatoms
Author(s) -
Helliwell Katherine E.,
Kleiner Friedrich H.,
Hardstaff Hayley,
Chrachri Abdul,
Gaikwad Trupti,
Salmon Deborah,
Smirnoff Nicholas,
Wheeler Glen L.,
Brownlee Colin
Publication year - 2021
Publication title -
new phytologist
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 3.742
H-Index - 244
eISSN - 1469-8137
pISSN - 0028-646X
DOI - 10.1111/nph.17162
Subject(s) - osmotic shock , osmolyte , osmoregulation , intracellular , biology , osmotic pressure , microbiology and biotechnology , osmotic concentration , biophysics , signalling , ecology , biochemistry , salinity , gene
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 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.