A Comparative Study of Iron Uptake Mechanisms in Marine Microalgae: Iron Binding at the Cell Surface Is a Critical Step    

Abstract

We investigated iron uptake mechanisms in five marine microalgae from different ecologically important phyla: the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana, the prasinophyceae Ostreococcus tauri and Micromonas pusilla, and the coccolithophore Emiliania huxleyi. Among these species, only the two diatoms were clearly able to reduce iron, via an inducible (P. tricornutum) or constitutive (T. pseudonana) ferrireductase system displaying characteristics similar to the yeast (Saccharomyces cerevisiae) flavohemoproteins proteins. Iron uptake mechanisms probably involve very different components according to the species, but the species we studied shared common features. Regardless of the presence and/or induction of a ferrireductase system, all the species were able to take up both ferric and ferrous iron, and iron reduction was not a prerequisite for uptake. Iron uptake decreased with increasing the affinity constants of iron-ligand complexes and with increasing ligand-iron ratios. Therefore, at least one step of the iron uptake mechanism involves a thermodynamically controlled process. Another step escapes to simple thermodynamic rules and involves specific and strong binding of ferric as well as ferrous iron at the cell surface before uptake of iron. Binding was paradoxically increased in iron-rich conditions, whereas uptake per se was induced in all species only after prolonged iron deprivation. We sought cell proteins loaded with iron following iron uptake. One such protein in O. tauri may be ferritin, and in P. tricornutum, Isip1 may be involved. We conclude that the species we studied have uptake systems for both ferric and ferrous iron, both involving specific iron binding at the cell surface.

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

“…These two taxa were classified by the Tara Oceans circumnavigation expedition to be two of the eight most abundant diatom genera in the global ocean (Malviya et al, 2016). Given the large amount of genetic and physiological variation observed between major diatom groups (Bowler et al, 2008;Sutak et al, 2012;Alexander et al, 2015), differences in molecular responses to changing Fe availabilities across the NE Pacific Ocean and CUZ were anticipated.…”

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

“…In support of this hypothesis, it was reported that in a ferritin triple mutant of the plant Arabidopsis there is a massive accumulation of iron in the apoplastic space, suggesting that in the absence of iron buffering cells activate iron efflux and/or repress iron influx to limit the amount of free iron in the cell (36). Because O. tauri is unicellular, it is possible that in ΔFtn cells at dusk iron is exported outside the cell, where it would be bound either to the plasma membrane (34) or to exopolysaccharides (37,38), thus remaining bioavailable for later uptake before dawn and dusk. In the presence of DFOB, extracellular iron would be irreversibly chelated and therefore would be unavailable to the cells.…”

“…Different final concentrations of total iron were obtained by adding different amounts of Fe(III) EDTA complex. For all other experiments such as short-term Fe(III) uptake rate measurements and identification of iron-loaded proteins in onedimensional gels, we used an EDTA-free medium (Mf) (34) containing Fe(III) citrate (1:20) at a final concentration of 1 μM. The higher uptake rates of iron by cells in this medium, compared with AQUIL medium, allow enough radioactive 55 Fe to accumulate within the cells after short-term incubation to be detected by scintillation counting or autoradiography (Fig.…”

The regeneration of highly bioavailable iron by meso‐ and microzooplankton

“…An increase in the regeneration of ferrous over ferric Fe would lead to more rapid uptake of Fe. For example, Sutak et al (2012) showed that several phytoplankton species (including T. pseudonana) can use both ferrous and ferric species as an Fe source, although ferrous Fe was always taken up more rapidly. The suggestion that grazing may lead to the release of more Fe(II) relative to Fe(III) would be consistent with the observed faster uptake rates of regenerated iron in comparison to inorganic Fe(III) in some experiments.…”

“…Taxonomic differences in uptake of regenerated Fe were not addressed in this study, but previous work (Sato et al 2007;Dalbec and Twining 2009) suggests differences in uptake of naturally produced regenerated Fe among eukaryotic and prokaryotic phytoplankton. These differences in bioavailability are likely due to the fact that different phytoplankton phyla may access different Fe species using different cellular pathways that might include a prerequisite reduction step (Maldonado and Price 1999;Shaked et al 2005;Sutak et al 2012). Future Fe regeneration studies will provide detailed information about how digestive physiologies of different zooplankton affect organic and redox speciation of regenerated Fe.…”