Saccharides enhance iron bioavailability to Southern Ocean phytoplankton

Abstract

Iron limits primary productivity in vast regions of the ocean. Given that marine phytoplankton contribute up to 40% of global biological carbon fixation, it is important to understand what parameters control the availability of iron (iron bioavailability) to these organisms. Most studies on iron bioavailability have focused on the role of siderophores; however, eukaryotic phytoplankton do not produce or release siderophores. Here, we report on the pivotal role of saccharides--which may act like an organic ligand--in enhancing iron bioavailability to a Southern Ocean cultured diatom, a prymnesiophyte, as well as to natural populations of eukaryotic phytoplankton. Addition of a monosaccharide (>2 nM of glucuronic acid, GLU) to natural planktonic assemblages from both the polar front and subantarctic zones resulted in an increase in iron bioavailability for eukaryotic phytoplankton, relative to bacterioplankton. The enhanced iron bioavailability observed for several groups of eukaryotic phytoplankton (i.e., cultured and natural populations) using three saccharides, suggests it is a common phenomenon. Increased iron bioavailability resulted from the combination of saccharides forming highly bioavailable organic associations with iron and increasing iron solubility, mainly as colloidal iron. As saccharides are ubiquitous, present at nanomolar to micromolar concentrations, and produced by biota in surface waters, they also satisfy the prerequisites to be important constituents of the poorly defined "ligand soup," known to weakly bind iron. Our findings point to an additional type of organic ligand, controlling iron bioavailability to eukaryotic phytoplankton--a key unknown in iron biogeochemistry.

Fig. 1.

Iron uptake by natural bacterioplankton and eukaryotic phytoplankton in presence of organic ligands. Effect of increased concentrations of (A and C) siderophore (DFB) and (B and D) monosaccharide (glucuronic acid, GLU) on intracellular iron uptake ([Fe]_int) by natural eukaryotic phytoplankton and bacterioplankton collected (A and B) south of the polar front (54.0 °S 145.9 °E) and (C and D) in the subantarctic zone (46.0 °S 153.2 °E). ⁵⁵Iron addition represents less than 5% of the natural dissolved iron background. Error bars represent half interval (n = 2).

Fig. 2.

Iron uptake by Antarctic isolates in presence of organic ligands. Effect of organic ligands on iron uptake rate by eukaryotic phytoplankton (Chaetoceros sp. and Phaeocystis sp.) incubated in either (A) filtered (<0.2 μm) Antarctic seawater (68 °S, 55 °W; ref. 38) or (B) in synthetic seawater. Iron uptake rates in the presence of iron (1 nM) and organic ligands (15 nM) are represented. Organic ligands were siderophore (DFB), small (GLU), and large (DEX) saccharides. Error bars represent half interval (n = 2).

Fig. 3.

Chemical speciation of iron in the presence of organic ligands. Iron measured by competitive ligand exchange–adsorptive stripping voltammetry following iron standard addition in synthetic seawater in the absence of organic ligand (solid circle, dotted line). Effect of the presence of synthetic (A) and natural (B) organic ligands on iron chemical speciation in artificial seawater. Organic ligands were siderophore (DFB, 5 nM), small saccharides (GLU, 5 nM), and an exopolysaccharide (EPS) (1 nM) purified from bacteria isolated from the pelagic Southern Ocean. The dashed line shows a 1:1 relationship. Error bars represent SD (n = 3).