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.

Keywords: iron; iron uptake; micro-algae; ocean; phytoplankton.

FIGURE 1

Model of reductive iron uptake in yeast. Ferric chelates (Fe³⁺-L) are dissociated by reduction at the cell surface, and free ferrous ions are taken up by the high-affinity Fet3-Ftr1 complex or by the divalent metal transporter Fet4.

FIGURE 2

Iron uptake in P. tricornutum. Unchelated ferric ions can be transported by endocytosis after binding to the phytotransferrin ISIP2a, or ferric chelates can be dissociated by reduction (FRE) and the resulting ferrous ions can be taken up by divalent metal transporters (ZIP). Hydroxamate siderophores are taken up by endocytosis after binding to the FBP1 protein, and iron is released by reduction (FRE2) possibly in endocytosis vesicles.

FIGURE 3

Structure of the siderophores schizokinen and synechobactin A.

FIGURE 4

Model of reductive iron uptake and uptake of inorganic ferric species. 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 free 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.

FIGURE 5

Iron sources available to marine phytoplankton and employed uptake pathways. Particulate iron from sources including atmospheric dust, glaciers, coastal sediments, hydrothermal vents is dissolved by the photochemical reactions, complexation and the microbial ferrous wheel (Kirchman, 1996). The enormous complexity of the mechanisms and species behind the biological iron recycling is only recently being fully acknowledged, involving organisms as diverse as viruses, both heterotrophic and photosynthetic bacteria and protists, mesozooplankton (Boyd and Ellwood, 2010). Different species of iron are available to phytoplankton based on marine chemistry, i.e., ferric and ferrous ions; in inorganic form or chelated to organic ligands. It appears that the main strategy of cyanobacterial iron acquisition is the reductive iron uptake that can be combined with siderophore-mediated pathway. The common iron uptake mechanism employed by eukaryotic phytoplankton is mediated by phytotransferrin, while some species additionally use reductive iron uptake and (at least) some diatoms are able to acquire xenosiderophores. Phycosphere represents a unique environment in the close proximity to algal cell surface, where iron availability may be significantly increased due to bacterial iron metabolism.