Iron Uptake Mechanisms in Marine Phytoplankton

Abstract

Oceanic phytoplankton species have highly efficient mechanisms of iron acquisition, as they can take up iron from environments in which it is present at subnanomolar concentrations. In eukaryotes, three main models were proposed for iron transport into the cells by first studying the kinetics of iron uptake in different algal species and then, more recently, by using modern biological techniques on the model diatom Phaeodactylum tricornutum. In the first model, the rate of uptake is dependent on the concentration of unchelated Fe species, and is thus limited thermodynamically. Iron is transported by endocytosis after carbonate-dependent binding of Fe(III)' (inorganic soluble ferric species) to phytotransferrin at the cell surface. In this strategy the cells are able to take up iron from very low iron concentration. In an alternative model, kinetically limited for iron acquisition, the extracellular reduction of all iron species (including Fe') is a prerequisite for iron acquisition. This strategy allows the cells to take up iron from a great variety of ferric species. In a third model, hydroxamate siderophores can be transported by endocytosis (dependent on ISIP1) after binding to the FBP1 protein, and iron is released from the siderophores by FRE2-dependent reduction. In prokaryotes, one mechanism of iron uptake is based on the use of siderophores excreted by the cells. Iron-loaded siderophores are transported across the cell outer membrane via a TonB-dependent transporter (TBDT), and are then transported into the cells by an ABC transporter. Open ocean cyanobacteria do not excrete siderophores but can probably use siderophores produced by other organisms. In an alternative model, inorganic ferric species are transported through the outer membrane by TBDT or by porins, and are taken up by the ABC transporter system FutABC. Alternatively, ferric iron of the periplasmic space can be reduced by the alternative respiratory terminal oxidase (ARTO) and the ferrous ions can be transported by divalent metal transporters (FeoB or ZIP). After reoxidation, iron can be taken up by the high-affinity permease Ftr1.

Flow cytometry-based study of model marine microalgal consortia revealed an ecological advantage of siderophore utilization by the dinoflagellate Amphidinium carterae

“…Notably, the iron enrichment-induced downregulation of these recently discovered major players in iron uptake was also detected in all species of our coculture model. Both phytotransferrin-mediated and siderophore-bound iron uptake mechanisms are most likely based on elaborate machinery involving endocytosis [35] ; thus, this adaptation to life under iron-limited conditions requires complex fine-tuning.…”

Community Interaction Co-limitation: Nutrient Limitation in a Marine Microbial Community Context

“…The nutrient limiting the growth of siderophore producers could then possibly limit bioavailable iron delivery to the whole community, contributing to CIC. The details matter here though, as this siderophore-bound iron is not available to all community members equally ( Hutchins et al, 1999 ; Sanchez et al, 2018 ; Sutak et al, 2020 ). Identifying microbial groups that rely on interactions to obtain BPNs will be important for investigations of additional mechanisms of CIC.…”

Concentration, Spatial-Temporal Distribution, and Bioavailability of Dissolved Reactive Iron in Northern Coastal China Seawater

“…Combining these two iron uptake models and DrFe content in Sishili Bay, the relative stability of DrFe may be due to the following reason: weak chelated iron and unchelated inorganic iron could be first consumed, and complexed iron might be converted into DrFe by photoreduction and/or cell surface reduction in time to maintain the normal growth of phytoplankton [44]. Phytoplankton indeed can access Fe from strong organic ligands, such as siderophores excreted by the cells or produced by other bacterial or fungal species, through direct metal exchange accomplished by the ternary complex formed by iron chelator and acceptor [62]; but as long as DrFe concentrations are high enough, which is the case in this study as confirmed in Section 4.6 below, the consumption of Fe from strong ligands will be negligible [63]. Even so, the Fe(II)s model is the dominant but not the only iron uptake mechanism in this study, as several studies have strongly suggested that no one model can account for all iron uptake, with several different iron uptake mechanisms coexisting in a single species [62,64].…”

“…Phytoplankton indeed can access Fe from strong organic ligands, such as siderophores excreted by the cells or produced by other bacterial or fungal species, through direct metal exchange accomplished by the ternary complex formed by iron chelator and acceptor [62]; but as long as DrFe concentrations are high enough, which is the case in this study as confirmed in Section 4.6 below, the consumption of Fe from strong ligands will be negligible [63]. Even so, the Fe(II)s model is the dominant but not the only iron uptake mechanism in this study, as several studies have strongly suggested that no one model can account for all iron uptake, with several different iron uptake mechanisms coexisting in a single species [62,64].…”