Dataset Information

Phosphorus-Ca2+ signalling in marine diatoms

ABSTRACT: Phosphorus is a critical nutrient controlling phytoplankton growth. Availability of this limiting factor can vary significantly in space and time, particularly in dynamic aquatic ecosystems. Diatoms are important eukaryotic phytoplankton that thrive in regions of pulsed phosphate supply, yet little is known of the sensory mechanisms enabling them to detect and rapidly respond to phosphorus availability. Here we show that phosphorus-starved diatoms utilise a novel Ca2+-dependent signalling pathway to sense and regulate cellular recovery following phosphorus resupply. This pathway, which has not previously been described in eukaryotes, is sensitive to sub-micromolar concentrations of phosphate, alongside a range of environmentally relevant phosphorus forms. Using comparative proteomics, we have characterised early adaptations governing diatom cellular recovery from phosphorus limitation. Strikingly, the dominant response was substantial enhancement of nitrogen assimilation proteins. This led to 12-fold increases in absolute nitrate uptake rates, relative to phosphorus-starved cells. Moreover, we find that the novel phosphorus-Ca2+ signalling pathway controls this primary recovery response. Our findings highlight that fundamental cross-talk between the essential nutrients phosphorus and nitrogen drive diatom recovery from phosphorus limitation. Moreover, a novel Ca2+-dependent phosphorus signalling pathway governs such ecological acclimation responses, and is thus likely critical to the success of diatoms in regions of episodic nutrient supply.

INSTRUMENT(S): Orbitrap Fusion

ORGANISM(S): Phaeodactylum Tricornutum (strain Ccap 1055/1)

TISSUE(S): Cell Culture

SUBMITTER: Joseph Christie-Oleza

LAB HEAD: Joseph A. Christie-Oleza

PROVIDER: PXD022586 | Pride | 2021-02-22

REPOSITORIES: Pride

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Publications

A Novel Ca<sup>2+</sup> Signaling Pathway Coordinates Environmental Phosphorus Sensing and Nitrogen Metabolism in Marine Diatoms.

Helliwell Katherine E KE Harrison Ellen L EL Christie-Oleza Joseph A JA Rees Andrew P AP Kleiner Friedrich H FH Gaikwad Trupti T Downe Joshua J Aguilo-Ferretjans Maria M MM Al-Moosawi Lisa L Brownlee Colin C Wheeler Glen L GL

Current biology : CB 20201228 5

Diatoms are a diverse and globally important phytoplankton group, responsible for an estimated 20% of carbon fixation on Earth. They frequently form spatially extensive phytoplankton blooms, responding rapidly to increased availability of nutrients, including phosphorus (P) and nitrogen (N). Although it is well established that diatoms are common first responders to nutrient influxes in aquatic ecosystems, little is known of the sensory mechanisms that they employ for nutrient perception. Here, ...[more]

PMID: 33373640

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Project description:Phosphorus (P) is a critical driver of phytoplankton growth and ecosystem structure and function in the ocean. Diatoms are an abundant and widespread functional group of phytoplankton that are responsible for significant amounts of primary production in the ocean, however there has not been a comprehensive study of diatom physiological responses to P deficiency. Here, we coupled deep sequencing of transcript tags and quantitative proteomic analysis from the diatom Thalassiosira pseudonana grown under P-replete and P-deficient conditions. The reads (tags) were mapped to the T. pseudonana genome sequence, confirming expression of 91% of the modeled gene set. A total of 318 genes were differentially regulated with a false discovery rate of p<0.05. A total of 1264 proteins were detected, and of those 136 were differentially expressed with a false discovery rate of p<0.05. Significant changes in the abundance of transcripts and proteins were observed and these changes were coordinated for glycolysis, translation, and multiple biochemical responses to P deficiency. These data demonstrate that diatom P deficiency results in changes in cellular P allocation through polyphosphate production, increased P transport, a switch to utilization of dissolved organic P (DOP) through increased production of alkaline phosphatase metalloenzymes and a diesterase, and a remodeling of the cell surface through production of sulfolipids. Together, these findings reveal that T. pseudonana has evolved a sophisticated response to P deficiency involving multiple biochemical strategies that are likely critical to its ability to rapidly respond to variations in environmental P availability. T. pseudonana (Strain 1335 from the Provosoli-Guillard National Center for the Culture of Marine Phytoplankton (CCMP)) was grown in a modified f/2 medium made from Sargasso Sea water. Macronutrients and vitamin B12, biotin, and thiamine solutions were treated with prepared Chelex-100 resin to remove trace metal contaminants followed by trace-metal clean syringe sterilization to yield final nutrient concentrations of 882 μM NaNO3 and 106 μM Na2SiO3, and vitamin concentrations of 75 pM, 400 pM, and 60 nM, respectively. The Fe concentration was also modified from f/2 to 400 nM. All conditions were run in triplicate at 14 ºC, in constant light (120 µmol photons m-2 s-1). Cells were grown with f/2 phosphorus concentrations (P-replete; 36 µM PO4) and with low phosphorus concentrations (P-deficient; 0.4 µM PO4). Growth was monitored daily with cell counts. Duplicate P-replete treatments were pooled and harvested in mid log phase, and triplicate P-deficient treatments were pooled, and also quickly harvested onto 2 µm filters at the onset of P depletion. All RNA samples were snap frozen in liquid nitrogen. Replicate P-deficient cultures were refed to 36 µM phosphate at the onset of P depletion, and subsequently resumed growth. Additional growth studies were performed as described above substituting glycerolphosphate and adenosine monophosphate at 36 µM, for the phosphate in the medium.

Dataset Information

Phosphorus-Ca2+ signalling in marine diatoms

Publications

A Novel Ca<sup>2+</sup> Signaling Pathway Coordinates Environmental Phosphorus Sensing and Nitrogen Metabolism in Marine Diatoms.

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