Hypometabolism to survive the long polar night and subsequent successful return to light in the diatom Fragilariopsis cylindrus.

Diatoms, the main eukaryotic phytoplankton of the polar marine regions, are essential for the maintenance of food chains specific to Arctic and Antarctic ecosystems, and are experiencing major disturbances under current climate change. As such, it is fundamental to understand the physiological mechanisms and associated molecular basis of their endurance during the long polar night. Here, using the polar diatom Fragilariopsis cylindrus, we report an integrative analysis combining transcriptomic, microscopic and biochemical approaches to shed light on the strategies used to survive the polar night. We reveal that in prolonged darkness, diatom cells enter a state of quiescence with reduced metabolic and transcriptional activity, during which no cell division occurs. We propose that minimal energy is provided by respiration and degradation of protein, carbohydrate and lipid stores and that homeostasis is maintained by autophagy in prolonged darkness. We also report internal structural changes that manifest the morphological acclimation of cells to darkness, including the appearance of a large vacuole. Our results further show that immediately following a return to light, diatom cells are able to use photoprotective mechanisms and rapidly resume photosynthesis, demonstrating the remarkable robustness of polar diatoms to prolonged darkness at low temperature.

Potential for the Production of Carotenoids of Interest in the Polar Diatom Fragilariopsis cylindrus.

Carotenoid xanthophyll pigments are receiving growing interest in various industrial fields due to their broad and diverse bioactive and health beneficial properties. Fucoxanthin (Fx) and the inter-convertible couple diadinoxanthin-diatoxanthin (Ddx+Dtx) are acknowledged as some of the most promising xanthophylls; they are mainly synthesized by diatoms (Bacillariophyta). While temperate strains of diatoms have been widely investigated, recent years showed a growing interest in using polar strains, which are better adapted to the natural growth conditions of Nordic countries. The aim of the present study was to explore the potential of the polar diatom Fragilariopsis cylindrus in producing Fx and Ddx+Dtx by means of the manipulation of the growth light climate (daylength, light intensity and spectrum) and temperature. We further compared its best capacity to the strongest xanthophyll production levels reported for temperate counterparts grown under comparable conditions. In our hands, the best growing conditions for F. cylindrus were a semi-continuous growth at 7 °C and under a 12 h light:12 h dark photoperiod of monochromatic blue light (445 nm) at a PUR of 11.7 µmol photons m-2 s-1. This allowed the highest Fx productivity of 43.80 µg L-1 day-1 and the highest Fx yield of 7.53 µg Wh-1, more than two times higher than under 'white' light. For Ddx+Dtx, the highest productivity (4.55 µg L-1 day-1) was reached under the same conditions of 'white light' and at 0 °C. Our results show that F. cylindrus, and potentially other polar diatom strains, are very well suited for Fx and Ddx+Dtx production under conditions of low temperature and light intensity, reaching similar productivity levels as model temperate counterparts such as Phaeodactylum tricornutum. The present work supports the possibility of using polar diatoms as an efficient cold and low light-adapted bioresource for xanthophyll pigments, especially usable in Nordic countries.

Genome-Scale Metabolic Reconstruction and in Silico Perturbation Analysis of the Polar Diatom Fragilariopsis cylindrus Predicts High Metabolic Robustness.

Diatoms are major primary producers in polar environments where they can actively grow under extremely variable conditions. Integrative modeling using a genome-scale model (GSM) is a powerful approach to decipher the complex interactions between components of diatom metabolism and can provide insights into metabolic mechanisms underlying their evolutionary success in polar ecosystems. We developed the first GSM for a polar diatom, Fragilariopsis cylindrus, which enabled us to study its metabolic robustness using sensitivity analysis. We find that the predicted growth rate was robust to changes in all model parameters (i.e., cell biochemical composition) except the carbon uptake rate. Constraints on total cellular carbon buffer the effect of changes in the input parameters on reaction fluxes and growth rate. We also show that single reaction deletion of 20% to 32% of active (nonzero flux) reactions and single gene deletion of 44% to 55% of genes associated with active reactions affected the growth rate, as well as the production fluxes of total protein, lipid, carbohydrate, DNA, RNA, and pigments by less than 1%, which was due to the activation of compensatory reactions (e.g., analogous enzymes and alternative pathways) with more highly connected metabolites involved in the reactions that were robust to deletion. Interestingly, including highly divergent alleles unique for F. cylindrus increased its metabolic robustness to cellular perturbations even more. Overall, our results underscore the high robustness of metabolism in F. cylindrus, a feature that likely helps to maintain cell homeostasis under polar conditions.