Hypometabolism to survive the long polar night in the diatomFragilariopsis cylindrus

Abstract

Diatoms, the major eukaryotic phytoplankton in polar regions, are essential to sustain Arctic and Antarctic ecosystems. As such, it is fundamental to understand the physiological mechanisms and associated molecular basis of their resilience to the long polar night. Here, we report an integrative approach revealing that in prolonged darkness, diatom cells enter a state of quiescence associated 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. Our results further indicate that immediately following a return to light, diatom cells are able to use photoprotective mechanisms and rapidly resume photosynthesis. Cell division resumed rates similar to those before darkness. Our study demonstrates the remarkable robustness of polar diatoms to prolonged darkness at low temperatures.

Resting cells of Skeletonema marinoi assimilate organic compounds and respire by dissimilatory nitrate reduction to ammonium in dark, anoxic conditions

“…Surviving decades of dormancy implies the need for active cell maintenance such as DNA repairs to maintain cell viability, prevent microbial degradation and allow future regermination. The requirement of active cell maintenance has previously been suggested to be essential due to cell deterioration during dormancy (Joli et al, 2023; Sciandra et al, 2022). Previous studies of gene expression performed on resting spores of the diatom Chaetoceros socialis have suggested that cellular activities during dormancy is mostly dependent on internal recycling of substrates (Pelusi et al, 2023).…”

Hydrostatic pressure induces transformations in the organic matter and microbial community composition of marine snow particles

“…Possibly, S. marinoi survives dark, cold, and highpressure conditions and degrades its own photopigments to meet dissimilatory and/or assimilatory demands. External stress factors are known to induce autophagy of cellular components in diatoms 48,49 . Even at highest pressure levels, however, the cellular contents of photopigments remained substantial, which makes them suitable biomarkers even in the deep ocean.…”

“…Instead, a more likely explanation is lipid metabolism by the diatoms themselves, assuming that they survive the pressure treatment. Stressed diatoms are known to sacrifice membrane lipids for TAG production to feed minimal dark respiration activity under prolonged darkness 49 . TAGs are then shuttled as lipid droplets into the vacuole where they will be degraded 48 .…”

Antarctic benthic diatoms after 10 months of dark exposure: consequences for photosynthesis and cellular integrity

“…As confirmed by nile red staining, the cellular lipid pool is depleted after 10 months of dark inception, where only <1% of the cellular volume remained occupied by lipid droplets in all 5 strains. Drawing energy from the lipid pool via autophagy or lipophagy during darkness was also suggested for the polar diatom Fragilariopsis cylindrus (Joli et al, 2023). Another source for energy in benthic diatoms can be anaerobic respiration using intercellular storage pools of NO 3 to reduce them to NH 4 (Kamp et al, 2011).…”