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Hypometabolism to survive the long polar night in the diatom Fragilariopsis cylindrus

ABSTRACT: Diatoms, the major eukaryotic phytoplankton in polar regions, are essential to sustain food webs. As such, it is fundamental to understand the physiological mechanisms and associated molecular basis of resilience to polar night of diatoms. Here, we report an integrative approach that reveals that in prolonged darkness, the cell enters a state of hypometabolism associated with reduced transcriptional activity during which no cell division occurs. Minimal energy is provided by respiration via alternative oxidase and progressive degradation of protein, carbohydrate and lipid stores. We also report internal structural changes that manifest the morphological acclimation of cells to darkness. Our results further indicate that immediately after returning to light, the majority of cells were able to use photoprotective mechanisms and resume photosynthesis. Divisions of surviving cells resumed at rates similar to those before darkness. Our study demonstrates the robustness of this species to prolonged darkness at low temperatures.

ORGANISM(S): Fragilariopsis cylindrus

PROVIDER: GSE218215 | GEO | 2023/02/14

REPOSITORIES: GEO

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Project description:Diatoms, albeit being only distantly related with higher plants, harbour a plant-like cryptochrome (CryP) that was proposed to act as a photoreceptor required for the regulation of photosynthetic proteins. Importantly, plant cryptochromes are assumed to be involved in the regulation of developmental processes that are only needed in multicellular organisms; their role in the unicellular diatoms to date is mostly enigmatic. To elucidate the function of this plant-like cryptochrome in a unicellular species, we examined the role of CryP in the regulation of transcription in the diatom Phaeodactylum tricornutum by comparative RNA-seq of wild type and CryP knock-down mutants, under prolonged darkness and one hour after onset of blue light. In total, mRNAs of 12,298 genes were identified and more than 70% of the genes could be sorted into functional bins. We here show that CryP influences gene expression in three different ways: some genes are regulated by CryP under blue light only, others independent of the light condition and surprisingly some are regulated by CryP only in darkness. Changes under blue light included only around 4% of total genes, and genes regulated in any condition were distributed over almost all functional categories. Expression of photosynthesis genes was lowered by CryP under BL, in contrast to the overall enhancement in wild-type cells under the same conditions. Interestingly, CryP also exerted an influence on two other photoreceptors: the genes for phytochrome (Pt-DPH) and CPF1, another cryptochrome of Phaeodactylum tricornutum, were down-regulated by CryP independent of the light condition. However, the regulatory effects of the different photoreceptors on transcriptional output were independent. The influence of CryP on the expression of other photoreceptors hints to the existence of a regulatory signalling network in diatoms that includes several cryptochromes and phytochrome, whereby CryP acts as a regulator of transcript abundance under light as well as in darkness.

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Hypometabolism to survive the long polar night in the diatom Fragilariopsis cylindrus

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