Chronic Iron Limitation in the Chlorarachniophyte Bigelowiella natans

Iron limitation is a major factor controlling phytoplankton growth in oceans. Here, we focused on the response to and recovery from chronic iron limitation of the marine chlorarachniophyte alga Bigelowiella natans whose plastid was acquired secondarily via endosymbiosis with a green alga. We resupplied an iron-limited culture with 100 nM ferric citrate and performed detailed proteomic analysis during the first 24h after iron repletion, concomitantly with a combination of physiological methods. Fe deficiency led to a strong up-regulation of Fe-assimilating proteins and protein CREG1 responsible for controlling cell growth and differentiation. Fe resupply induced suppression of those proteins within the first 3h, and 24h later the level of protein expression was at the level of control cells. Chronic Fe deprivation also affected photosystem II (PS II) photochemistry. We observed a pronounced increase of effective PSII antennae cross-section (σPSII), a significant reduction of the maximum quantum yield of PSII (Fv/Fm) and an increase of photoprotective non-photochemical fluorescence quenching (NPQ) that corresponded with strong up-regulation in expression of the light stress-related LI818 protein. Fv/Fm and NPQ recovered within 24 hours upon iron resupply, while σPSII, as well as antenna decoupling regenerated much slower. Because of its high Fe content, photosystem I (PSI) is known to be a prime target of iron deficiency. In B. natans, the chronic iron deprivation caused a decrease in the PSI/PSII ratio, as well as severe down-regulation of ferredoxin along with the PS I subunit PsaE that resulted in substantially reduced rates of carbon fixation. These parameters recovered at a much slower rate than PSII parameters, the first signs of regeneration were detected only after 9 hours of iron repletion, and after 24 hours levels of protein expression associated to PSI and carbon fixation reached only half of those in control cultures grown under iron replete conditions. In summary, expression of proteins related to Fe-assimilation and cell differentiation responded very promptly to the resupply of iron. The subsequent recovery of photochemistry started from PSII quantum yield and NPQ, followed by configuration of PSII antennae, while recovery of parameters related to PSI electron transport was the slowest.