A general kinetic model for iron acquisition by eukaryotic phytoplankton

Abstract

The conventional model of iron uptake in marine eukaryotic phytoplankton-the FeЈ model-suggests a dependency of uptake rate on the concentration of unchelated iron species (FeЈ), and not the concentration of total iron or iron chelated with organic ligands. However, iron in seawater is bound by strong organic ligands that buffer such low FeЈ concentrations that they should not support phytoplankton growth. Studies that show uptake and extracellular reduction of siderophore-bound iron by diatoms and provide indications that the iron uptake system of phytoplankton may be similar to that of yeast in which extracellular reduction is a prerequisite for uptake, call for revisions of the FeЈ model. In this paper we propose a new model for iron uptake by diatoms in which extracellular reduction of all Fe species is a necessary step for iron acquisition. Experiments verifying the predictions of the model are presented. In particular we show data supporting the fact that Fe(II) is formed as an intermediate during Fe uptake from all experimental media, including those buffered by Fe(III)EDTA. This model reconciles the standing FeЈ model with new data and concepts on reduction of iron chelates and provides a convenient framework for designing and interpreting iron uptake experiments in a variety of natural and artificial media.A major role for iron in marine phytoplankton physiology, ecosystem structure, and the ocean carbon cycle is emerging from numerous oceanographic studies (e.g., Wells et al. 1994;Maldonado et al. 2001). Trace metal clean procedures and many innovative analytical techniques have provided accurate measurements of oceanic iron concentrations and are beginning to reveal the speciation and cycling of iron in the ocean (e.g., Johnson et al. 1997;Rue and Bruland 1997). In order to understand the import of these findings for phytoplankton physiology and ecology, we must understand the relationship between uptake mechanisms of phytoplankton and the concentration and speciation of iron in seawater. The conventional model of iron uptake by marine eukaryotic phytoplankton-the FeЈ model-suggests a dependency of uptake rate on the concentration of unchelated

Ocean acidification slows nitrogen fixation and growth in the dominant diazotroph Trichodesmium under low-iron conditions

“…Our data show a similar effect of pH on Fe uptake in the cyanobacterium Trichodesmium. Although the mechanism of Fe uptake by Trichodesmium remains to be fully elucidated, it has been shown that the uptake process can involve a bio-reduction step, as has been demonstrated in some model diatom species (26)(27)(28). Trichodesmium apparently is capable of accessing Fe from Fe oxide, aerial dust, and siderophores (29,30) in which Fe bioavailability should be less sensitive to pH than in our EDTA-buffered medium (4).…”

Southern Ocean phytoplankton physiology in a changing climate

“…Remineralisation of particulate Fe at depth mediated by heterotrophic bacteria can also release Fe and ligands , thus potentially affecting Fe bioavailability to primary producers. Moreover, microorganisms can affect Fe redox chemistry, either by direct reduction of an Fe organic complex (often resulting in Fe (II) complexes easier to dissociate; e.g., Shaked et al, 2005) or by the excretion of compounds such as superoxide (Kutska et al, 2005). Despite numerous studies, the parameters controlling the bioavailability of Fe to SO primary producers remains poorly understood (Boyd and Ellwood, 2010;Hassler et al, 2011a).…”

Enhancement of the reactive iron pool by marine diatoms

“…The Fe(II) concentration at the end of the dark period in experiment C was higher than the Fe(II) concentration during irradiance on the previous day. These high Fe(II) concentrations in the dark may be ascribed to two different conceivable mechanisms: reduction of Fe(III) in the dark by either superoxide produced by C. brevis as was shown by Kustka et al (2005) for the diatoms Thallassiosira weissflogii and Thallassiosira pseudonana or by extra-cellular enzymes (Maldonado and Price, 2000;Salmon et al, 2006;Shaked et al, 2005).…”

“…Specifically, the Fe redox cycle, as initiated by photochemical processes, is believed to be an important mechanism that converts (colloidal) Fe into more reactive species (defined by the research method applied) resulting in a higher bioavailability for phytoplankton (Finden et al, 1984;Miller and Kester, 1994;. Note, that Fe(II) is suggested to be more bioavailable than Fe(III) (Anderson and Morel, 1980;Anderson and Morel, 1982;Maldonado and Price, 2001;Salmon et al, 2006;Shaked et al, 2005).…”