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

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

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.

Ca signalling, Phaeodactylum, R-GECO1, algae, diatoms, environmental sensing, osmotic stress, signalling
0028-646X
155-170
Helliwell, Katherine E.
514f8174-da3f-46c8-be0d-3bcd92ee8189
Kleiner, Friedrich H.
30a39ba3-e75c-4b03-9d4d-6c1725ea35e2
Hardstaff, Hayley
ae2f3737-2676-4ed0-b23d-e35944db9ba4
Chrachri, Abdul
4c8a3ca0-7e80-42f4-a3be-dd2dae8583ba
Gaikwad, Trupti
edb10052-ae5f-4b18-8567-09f7df2da744
Salmon, Deborah
88ac927c-7845-4211-a0b9-fdc87976cbb5
Smirnoff, Nicholas
309c0af9-df61-46fa-ab08-01a8b8d85937
Wheeler, Glen L.
80ee477b-ceb3-4051-923c-399098bb746a
Brownlee, Colin
2af37c1c-b2bf-4832-8370-d9c35e7b3385
Helliwell, Katherine E.
514f8174-da3f-46c8-be0d-3bcd92ee8189
Kleiner, Friedrich H.
30a39ba3-e75c-4b03-9d4d-6c1725ea35e2
Hardstaff, Hayley
ae2f3737-2676-4ed0-b23d-e35944db9ba4
Chrachri, Abdul
4c8a3ca0-7e80-42f4-a3be-dd2dae8583ba
Gaikwad, Trupti
edb10052-ae5f-4b18-8567-09f7df2da744
Salmon, Deborah
88ac927c-7845-4211-a0b9-fdc87976cbb5
Smirnoff, Nicholas
309c0af9-df61-46fa-ab08-01a8b8d85937
Wheeler, Glen L.
80ee477b-ceb3-4051-923c-399098bb746a
Brownlee, Colin
2af37c1c-b2bf-4832-8370-d9c35e7b3385

Helliwell, Katherine E., Kleiner, Friedrich H., Hardstaff, Hayley, Chrachri, Abdul, Gaikwad, Trupti, Salmon, Deborah, Smirnoff, Nicholas, Wheeler, Glen L. and Brownlee, Colin (2021) Spatiotemporal patterns of intracellular Ca2+ signalling govern hypo‐osmotic stress resilience in marine diatoms. New Phytologist, 230 (1), 155-170. (doi:10.1111/nph.17162).

Record type: Article

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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nph.17162 - Version of Record
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Accepted/In Press date: 11 December 2020
e-pub ahead of print date: 24 January 2021
Published date: 2 March 2021
Keywords: Ca signalling, Phaeodactylum, R-GECO1, algae, diatoms, environmental sensing, osmotic stress, signalling

Identifiers

Local EPrints ID: 447196
URI: http://eprints.soton.ac.uk/id/eprint/447196
ISSN: 0028-646X
PURE UUID: 41818b02-68ce-440d-977a-964310f013cb

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Date deposited: 04 Mar 2021 17:43
Last modified: 25 Nov 2021 21:40

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Contributors

Author: Katherine E. Helliwell
Author: Friedrich H. Kleiner
Author: Hayley Hardstaff
Author: Abdul Chrachri
Author: Trupti Gaikwad
Author: Deborah Salmon
Author: Nicholas Smirnoff
Author: Glen L. Wheeler
Author: Colin Brownlee

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