Central role for ferritin in the day/night regulation of iron homeostasis in marine phytoplankton

Abstract

In large regions of the open ocean, iron is a limiting resource for phytoplankton. The reduction of iron quota and the recycling of internal iron pools are among the diverse strategies that phytoplankton have evolved to allow them to grow under chronically low ambient iron levels. Phytoplankton species also have evolved strategies to cope with sporadic iron supply such as long-term storage of iron in ferritin. In the picophytoplanktonic species Ostreococcus we report evidence from observations both in the field and in laboratory cultures that ferritin and the main ironbinding proteins involved in photosynthesis and nitrate assimilation pathways show opposite diurnal expression patterns, with ferritin being maximally expressed during the night. Biochemical and physiological experiments using a ferritin knock-out line subsequently revealed that this protein plays a central role in the diel regulation of iron uptake and recycling and that this regulation of iron homeostasis is essential for cell survival under iron limitation.

Diatom Transcriptional and Physiological Responses to Changes in Iron Bioavailability across Ocean Provinces

“…Ferritin (FTN) gene expression patterns furthermore diverged between the two taxa at the coastal sites C4 (Line-P) and C2 (CUZ). This supports laboratory findings suggesting FTN may exhibit different expression patterns among diverse phytoplankton Botebol et al, 2015), even between taxa residing in the same location. Lastly, ABC.FEV.S, encoding a membrane Fe transport system protein, displayed divergent expression patterns between the examined genera with only Pseudo-nitzschia increasing ABC.FEV.S expression after Fe addition in all incubations exhibiting signs of iron limitation (C3, C4, and O5).…”

Transcriptional Orchestration of the Global Cellular Response of a Model Pennate Diatom to Diel Light Cycling under Iron Limitation

“…For example, the marine diazotroph Crocosphaera watsonii recycles intracellular Fe reserves for synthesis of day or night specific metalloenzymes (“hotbunking”) as a strategy to reduce its overall Fe requirement, [47]. Also, Ostreococcus tauri expresses ferritin nocturnally in order to store intracellular Fe recovered from damaged/oxidized iron-binding proteins [18]. Ferritin is used for iron storage in some bloom-forming diatoms [48] and may be similarly nocturnally expressed in these species, though no diel pattern was detected for ferritin in our experiments with P .…”

“…Additionally, diatoms appear to induce reductive [14–16] and potentially non-reductive [17] high-affinity transport systems to acquire Fe. Some Fe-acquisition and homeostasis mechanisms have been shown to be dependent on the light:dark cycle in phytoplankton [18]. Fe stress also seems to impose a strain on overall proteome health that cells counteract by induction of proteolysis, chaperone expression and various reactive oxygen species (ROS) defense mechanisms [19–23].…”

Acclimation of a low iron adapted Ostreococcus strain to iron limitation through cell biomass lowering

“…The iron cell content was determined by scintillation counting after bleaching photosynthetic pigments with sodium hypochlorite, as previously described 17, 29 .…”