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Iron Uptake Mechanisms in Marine Phytoplankton Robert Sutak, Jean-Michel Camadro, Emmanuel Lesuisse

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Iron Uptake Mechanisms in Marine Phytoplankton Robert Sutak, Jean-Michel Camadro, Emmanuel Lesuisse Iron Uptake Mechanisms in Marine Phytoplankton Robert Sutak, Jean-Michel Camadro, Emmanuel Lesuisse To cite this version: Robert Sutak, Jean-Michel Camadro, Emmanuel Lesuisse. Iron Uptake Mechanisms in Marine Phy- toplankton. Frontiers in Microbiology, Frontiers Media, 2020, 11, 10.3389/fmicb.2020.566691. hal- 02995222 HAL Id: hal-02995222 https://hal.archives-ouvertes.fr/hal-02995222 Submitted on 9 Nov 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. fmicb-11-566691 October 31, 2020 Time: 15:37 # 1 REVIEW published: 05 November 2020 doi: 10.3389/fmicb.2020.566691 Iron Uptake Mechanisms in Marine Phytoplankton Robert Sutak1, Jean-Michel Camadro2 and Emmanuel Lesuisse2* 1 Department of Parasitology, Faculty of Science, Charles University, BIOCEV, Vestec, Czechia, 2 CNRS, Institut Jacques Monod, Université de Paris, Paris, France 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 Edited by: Martin G. Klotz, a great variety of ferric species. In a third model, hydroxamate siderophores can be Washington State University, transported by endocytosis (dependent on ISIP1) after binding to the FBP1 protein, and United States iron is released from the siderophores by FRE2-dependent reduction. In prokaryotes, Reviewed by: Katherine Barbeau, one mechanism of iron uptake is based on the use of siderophores excreted by the University of California, San Diego, cells. Iron-loaded siderophores are transported across the cell outer membrane via a United States TonB-dependent transporter (TBDT), and are then transported into the cells by an ABC Yeala Shaked, Hebrew University of Jerusalem, Israel transporter. Open ocean cyanobacteria do not excrete siderophores but can probably Kosman Daniel, use siderophores produced by other organisms. In an alternative model, inorganic University at Buffalo, United States ferric species are transported through the outer membrane by TBDT or by porins, *Correspondence: Emmanuel Lesuisse and are taken up by the ABC transporter system FutABC. Alternatively, ferric iron of [email protected] 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 Specialty section: This article was submitted to ZIP). After reoxidation, iron can be taken up by the high-affinity permease Ftr1. Aquatic Microbiology, Keywords: iron, phytoplankton, iron uptake, micro-algae, ocean a section of the journal Frontiers in Microbiology Received: 28 May 2020 Accepted: 19 October 2020 INTRODUCTION Published: 05 November 2020 Iron is vital for almost all forms of life, with aerobic organisms having particularly large Citation: requirements for this element. Iron is abundant in the respiratory and photosynthetic electron Sutak R, Camadro J-M and Lesuisse E (2020) Iron Uptake transport chains, in the form of heme and iron-sulfur prosthetic groups, and it is also present in Mechanisms in Marine Phytoplankton. the iron-rich nitrogenase protein complex of diazotrophs (Buren et al., 2020). Iron was abundant Front. Microbiol. 11:566691. doi: 10.3389/fmicb.2020.566691 Abbreviations: FOB, ferrioxamine B; FOE, ferrioxamine E; FOG, ferrioxamine G; FCH, ferrichrome. Frontiers in Microbiology| www.frontiersin.org 1 November 2020| Volume 11| Article 566691 fmicb-11-566691 October 31, 2020 Time: 15:37 # 2 Sutak et al. Iron Uptake Mechanisms in Phytoplankton in its reduced form, Fe2C, in the Proterozoic ocean (Falkowski, no ferric reductase activity and do not excrete siderophores 2006). However, the levels of bioavailable iron have decreased (Sutak et al., 2012). These organisms have to cope with considerably over time, with the increase in oxygen levels in the extremely low, subnanomolar concentrations of iron. The affinity environment, because the solubility of the oxidized form, Fe3C, is constants of the known terrestrial iron uptake systems are in extremely low in neutral and basic conditions. Marine organisms the micromolar range and would, therefore be inefficient in a have, therefore, had to adapt, to maintain sufficiently high marine environment. The iron acquisition strategies of marine levels of this increasingly scarce resource. Low iron availability phytoplankton must have evolved to cope with iron scarcity nevertheless limits phytoplankton growth in about 30–50% of and the very particular conditions prevailing in the marine the ocean, in the vast HNLC (high-nutrient low-chlorophyll) environment, which has a transition metal composition very regions, in eastern boundary upwelling regions and at the deep different from that of terrestrial environments (Butler, 1998). chlorophyll maximum (Hogle et al., 2018). The existence of this Some progress has been made recently in our understanding of iron limitation has been demonstrated in experiments in which the mechanisms phytoplankton employs to cope with low iron the addition of iron to HNLC waters has been shown to boost the levels in the marine environment, and the mechanisms involved growth of phytoplankton considerably, generating spectacular often diverge from terrestrial models. blooms (Boyd et al., 2007). The bioavailability of iron (as Fe’ released from acidic ligands) to phytoplankton may decrease still further in the future, due to the acidification of the ocean as EUKARYOTES atmospheric CO2 levels increase, while the bioavailability of iron from oxy-hydroxide colloids should not change significantly (Shi Different Models of Iron Uptake et al., 2010), and the release of iron upon dust deposition may be Oceanic eukaryotic phytoplankton species have highly efficient enhanced (Li et al., 2017). mechanisms of iron acquisition, as they can take up iron Most of the iron in the ocean is complexed with organic from environments in which it is present at subnanomolar ligands, the nature of which remains unclear. Nevertheless, there concentrations. By comparing the rate of iron uptake from is growing evidence to suggest that iron is associated with both free inorganic soluble ferric species (Fe(III)’) in several iron- small, well-defined ligands including siderophores, and with limited phytoplankton species, Lis et al.(2015b) revealed diverse macromolecular complexes (Gledhill and Buck, 2012; a strong correlation of uptake rate constants (iron uptake Shaked et al., 2020). Unchelated iron is present in hydrolyzed rate/substrate concentration) between all the species tested, and .3−x/C forms, Fe(OH)x , the neutral tri-hydroxy species, Fe(OH)3, showed that these uptake rate constants were proportional having an extremely low solubility. It has been shown that to surface area, suggesting that they had reached a universal this pool of unchelated iron is the preferred source of iron upper limit (Lis et al., 2015b). Iron uptake may have been for marine micro-algae (Lis et al., 2015b). However, given the pushed up toward the maximum limits imposed by diffusion very particular nature of the ocean environment (low iron and ligand exchange kinetics (Sunda and Huntsman, 1995). concentration with episodic inputs, heterogeneous pool of iron Several authors have tried to identify the best iron sources complexes), it seems likely that highly novel mechanisms of iron for uptake in phytoplankton. The ocean contains a number of uptake await our discovery in phytoplanktonic algae and bacteria. different physicochemical fractions of dissolved iron, including Dark/light cycles may also be involved in regulating iron uptake Fe(II), colloidal and inorganic Fe, and organically complexed systems in phytoplankton species, because the photoreductive iron. It is widely thought that organic iron-binding ligands dissociation of natural ferric chelates or ferric colloids in seawater complex more than 99% of the dissolved iron in the ocean may increase the concentration of free iron (Fe3Caq) available for (Gledhill and Buck, 2012; Boiteau et al., 2016). These organic transport by more than two orders of magnitude (Sunda, 2001). ligands include siderophores, larger macromolecular complexes, Terrestrial microorganisms and plants have two main iron such as
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