Alternative Mechanisms for Fast Na+/Ca2+ Signaling in Eukaryotes via a Novel Class of Single-Domain Voltage-Gated Channels

Helliwell, Katherine E.; Chrachri, Abdesslam; Koester, Julie A.; Wharam, Susan D.; Verret, Frédéric; Taylor, Alison R.; Wheeler, Glen; Brownlee, Colin

doi:10.1016/j.cub.2019.03.041

Cited by 51 publications

(70 citation statements)

References 68 publications

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“…To investigate the role of Ca 2+ signalling in nutrient sensing in diatoms, we used a transgenic Phaeodactylum tricornutum line (PtR1), encoding the genetically-encoded fluorescent Ca 2+ biosensor, R-GECO1 (Helliwell et al, 2019; Zhao et al, 2011). PtR1 cells were grown in f/2 medium (Guillard and Ryther, 1962) made up in natural seawater (NSW), but with reduced concentrations of phosphate, nitrate or f/2 trace metals (Materials and Methods).…”

Section: Resultsmentioning

confidence: 99%

“…This work raises important questions about the role of Ca 2+ signalling in nutrient sensing in eukaryotes more broadly. Certainly, diatoms use Ca 2+ signalling for perception of several abiotic and biotic stimuli (Falciatore et al, 2000; Helliwell et al, 2019; Vardi et al, 2006). Moreover, our recent identification of a novel class of voltage-gated channels in diatoms (EukCatAs), demonstrates that they have evolved unique mechanisms for environmental perception in the oceans (Helliwell et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

“…Certainly, diatoms use Ca 2+ signalling for perception of several abiotic and biotic stimuli (Falciatore et al, 2000; Helliwell et al, 2019; Vardi et al, 2006). Moreover, our recent identification of a novel class of voltage-gated channels in diatoms (EukCatAs), demonstrates that they have evolved unique mechanisms for environmental perception in the oceans (Helliwell et al, 2019). Here, we report the discovery of a phosphorus-Ca 2+ -signalling pathway that is essential for phosphorus sensing and acclimation in Phaeodactylum tricornutum , and likely provides a competitive advantage to diatoms in regions of pulsed or intermittent phosphorus supply.…”

Section: Introductionmentioning

confidence: 99%

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A novel Ca²⁺signalling pathway co-ordinates environmental phosphorus sensing and nitrogen metabolism in marine diatoms

Helliwell

Harrison

Christie-Oleza

et al. 2020

Preprint

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20Diatoms are a diverse and globally important phytoplankton group, responsible for an 21 estimated 20% of carbon fixation on Earth. They frequently form spatially extensive 22 phytoplankton blooms, responding rapidly to increased availability of nutrients including 23 phosphorus and nitrogen. Although it is well established that diatoms are common first-24 responders to nutrient influxes in aquatic ecosystems, little is known of the sensory 25 mechanisms that they employ for nutrient perception. Here we show that diatoms use a novel 26 and highly-sensitive Ca 2+ -dependent signalling pathway, not previously described in 27 eukaryotes, to sense and respond to the critical macronutrient phosphorus. We demonstrate that 28 phosphorus-Ca 2+ signalling is essential for regulating diatom recovery from phosphorus 29 limitation, by controlling rapid and substantial increases in nitrogen assimilation. Phosphorus-30 Ca 2+ signalling thus mediates fundamental cross-talk between the vital nutrients P and N to 31 maximise resource competition, and likely governs the success of diatoms as major bloom 32 formers in regions of pulsed nutrient supply. Importantly, our study demonstrates that distinct 33 mechanisms for nutrient sensing have evolved in photosynthetic eukaryotes. 34 35 36 37 38 39 Riveras et al., 2015), and Zn 2+ (Behera et al., 2017), but not phosphate (Matthus et al., 2019).87Nitrate resupply to nitrogen-limited Arabidopsis plants induces [Ca 2+ ]cyt elevations, which 88 triggers several nitrate-associated regulatory responses, orchestrated via Ca 2+ -dependent 89 5 protein kinases (Liu et al., 2017). This work raises important questions about the role of Ca 2+ 90 signalling in nutrient sensing in eukaryotes more broadly. Certainly, diatoms use Ca 2+ 91 signalling for perception of several abiotic and biotic stimuli (Falciatore et al., 2000; Helliwell 92 et al., 2019; Vardi et al., 2006). Moreover, our recent identification of a novel class of voltage-93 gated channels in diatoms (EukCatAs), demonstrates that they have evolved unique 94 mechanisms for environmental perception in the oceans (Helliwell et al., 2019). Here, we report 95 the discovery of a phosphorus-Ca 2+ -signalling pathway that is essential for phosphorus sensing 96 and acclimation in Phaeodactylum tricornutum, and likely provides a competitive advantage 97 to diatoms in regions of pulsed or intermittent phosphorus supply. 98 99 Results resupply 102 To investigate the role of Ca 2+ signalling in nutrient sensing in diatoms, we used a transgenic 103 Phaeodactylum tricornutum line (PtR1), encoding the genetically-encoded fluorescent Ca 2+ 104 biosensor, R-GECO1 (Helliwell et al., 2019; Zhao et al., 2011). PtR1 cells were grown in f/2 105 medium (Guillard and Ryther, 1962) made up in natural seawater (NSW), but with reduced 106 concentrations of phosphate, nitrate or f/2 trace metals (Materials and Methods). We then 107 monitored single-cell R-GECO1 fluorescence of nutrient deplete cells, following resupply with 108 each respective nutrient...

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A novel Ca²⁺signalling pathway co-ordinates environmental phosphorus sensing and nitrogen metabolism in marine diatoms

Helliwell

Harrison

Christie-Oleza

et al. 2020

Preprint

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“…For instance, we found the single-domain voltage-gated channels (EukCatAs) and the red/far-red light sensing phytochrome (DPH) families expanded by dispersed and tandem gene duplicates, respectively. While the EukCatAs family has been shown to modulate gliding locomotion in raphid pennate diatoms through fast Na + /Ca 2+ signaling [19], the DPH family may be relevant for sensing the density and stress status of biofilms [20] (Supplementary Note S3).…”

Section: Tandem Duplication As a Driver Of Gene Family Expansions Formentioning

confidence: 99%

TheSeminavis robustagenome provides insights into the evolutionary adaptations of benthic diatoms

Osuna-Cruz

Bilcke

Vancaester

et al. 2020

Preprint

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Benthic diatoms are the main primary producers in shallow freshwater and coastal environments, fulfilling important ecological functions such as nutrient cycling and sediment stabilization. However, little is known about their evolutionary adaptations to these highly structured but heterogeneous environments. Here, we report a reference genome for the marine biofilm-forming diatom Seminavis robusta, showing that gene family expansions are responsible for a quarter of all 36,254 protein-coding genes. Tandem duplications play a key role in extending the repertoire of specific gene functions, including light and oxygen sensing, which are probably central for its adaptation to benthic habitats. Genes differentially expressed during interactions with bacteria are strongly conserved in other benthic diatoms while many species-specific genes are strongly upregulated during sexual reproduction. Combined with resequencing data from 48 strains, our results offer new insights on the genetic diversity and gene functions in benthic diatoms.

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“…Recently, an early eukaryote, diatom, was found to have another homo-tetrameric channel with no selectivity that has an important role in electrical signaling in this species (35). These findings suggest that the cation selectivity of the homo-tetrameric channel family can be flexibly tuned to realize the required roles specific to its original species.…”

Section: Cavs In Prokaryotes and The Species-specific Tuning Of Homo-mentioning

confidence: 99%

A native prokaryotic voltage-dependent calcium channel with a novel selectivity filter sequence

Shimomura

Yonekawa

Nagura

et al. 2019

Preprint

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Voltage-dependent Ca 2+ channels (Cavs) are indispensable for coupling action potentials with Ca 2+ signaling in living organisms. The structure of Cavs is similar to that of voltage-dependent Na + channels (Navs). It is known that prokaryotic Navs can obtain Ca 2+ selectivity by negative charge mutations of the selectivity filter, but native prokaryotic Cavs had not yet been identified.Here, we report the first identification of a native prokaryotic Cav, CavMr, and its relative, NavPp. Although CavMr contains a smaller number of negatively charged residues in the selectivity filter than artificial prokaryotic Cavs, CavMr exhibits high Ca 2+ selectivity. In contrast, NavPp, which has similar filter sequence to artificial Cavs, mainly allows Na + to permeate. Interestingly, a NavPp mutant whose selectivity filter was replaced with that of CavMr exhibits high Ca 2+ selectivity. Mutational analyses revealed that the glycine residue of the CavMr selectivity filter is a determinant for Ca 2+ selectivity. This glycine residue is well conserved among subdomains I and III of eukaryotic Cavs.These findings provide new insight into the Ca 2+ selectivity mechanism conserved from prokaryotes to eukaryotes. Significance StatementCavMr is the first identified native prokaryotic Cav. CavMr has a unique selectivity filter sequence different from that of artificial prokaryotic Cavs derived from canonical prokaryotic Navs. Unlike artificial Cavs, the glycine residue of the selectivity filter of CavMr is important for the selective permeation of Ca 2+ ions, indicating that there are two different mechanisms of Ca 2+ recognition. Interestingly, corresponding glycine residues are found in subdomains I and III of eukaryotic Cavs.These findings suggest that the small glycine residue in the Cav selectivity filter is an overlooked feature determining Ca 2+ selectivity. Therefore, further investigation of CavMr will contribute to our understanding of the principles underlying Ca 2+ selectivity.

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Alternative Mechanisms for Fast Na+/Ca2+ Signaling in Eukaryotes via a Novel Class of Single-Domain Voltage-Gated Channels

Cited by 51 publications

References 68 publications

A novel Ca²⁺signalling pathway co-ordinates environmental phosphorus sensing and nitrogen metabolism in marine diatoms

A novel Ca²⁺signalling pathway co-ordinates environmental phosphorus sensing and nitrogen metabolism in marine diatoms

TheSeminavis robustagenome provides insights into the evolutionary adaptations of benthic diatoms

A native prokaryotic voltage-dependent calcium channel with a novel selectivity filter sequence

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Alternative Mechanisms for Fast Na+/Ca2+ Signaling in Eukaryotes via a Novel Class of Single-Domain Voltage-Gated Channels

Cited by 51 publications

References 68 publications

A novel Ca2+signalling pathway co-ordinates environmental phosphorus sensing and nitrogen metabolism in marine diatoms

A novel Ca2+signalling pathway co-ordinates environmental phosphorus sensing and nitrogen metabolism in marine diatoms

TheSeminavis robustagenome provides insights into the evolutionary adaptations of benthic diatoms

A native prokaryotic voltage-dependent calcium channel with a novel selectivity filter sequence

Contact Info

Product

Resources

About

A novel Ca²⁺signalling pathway co-ordinates environmental phosphorus sensing and nitrogen metabolism in marine diatoms

A novel Ca²⁺signalling pathway co-ordinates environmental phosphorus sensing and nitrogen metabolism in marine diatoms