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

Significance Phytoplankton transforms large amounts of inorganic to organic carbon, a critical step in the uptake of atmospheric CO2 in the ocean. Although iron is essential for this process, its bioavailability is often low. Phytoplankton has evolved strategies to cope with low environmental iron concentrations. We discovered that the iron storage protein ferritin is strongly regulated by the day/night cycle in the coastal California upwelling region dominated by the picophytoplanktonic genus Ostreococcus. Using genetic approaches, we showed that ferritin is used for short-term recycling of iron over diurnal cycles rather than for long-term iron storage. This work revealing the importance of ferritin in diurnal and circadian regulations of iron homeostasis should have implications for understanding carbon uptake by the ocean. 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 iron-binding 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.