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.trace metals | carbohydrates | organic matter | exopolymeric substances | plankton

Dissolved organic matter (DOM) release by phytoplankton in the contemporary and future ocean

“…Exopolymers released by microorganisms may act to trap exoenzymes in the proximity of the cell, thereby ensuring that the cell that released the enzymes benefits most from the resources created by the enzyme activity (Decho, 1990). Extracellular saccharides enhance the bioavailability of iron to eukaryotic phytoplankton in the Southern Ocean (Hassler et al, 2011). This may be a significant finding, given that iron is the primary limiting nutrient over a significant area of the world ocean and carbohydrates are a major component of the DOM released by phytoplankton.…”

Southern Ocean phytoplankton physiology in a changing climate

“…Additionally, Fe is involved in other key cellular processes such as respiration, macronutrient assimilation and detoxification of reactive oxygen species (Sunda, 1989;Morel et al, 1991;Sunda and Huntsman, 1995). Due to their high demand for Fe, primary producers have developed specialised mechanisms to satisfy their needs; resulting in a decoupling between intracellular and dissolved Fe stoichiometry (Morel and Price, 2003;Moore et al, 2013), as well as complex interactions and feedbacks between Fe biology and its chemistry (Hassler et al, 2011a).…”

“…Fe-binding organic ligands are critical for Fe biogeochemistry, improving its solubility and affecting its reactivity to support phytoplankton growth Hassler et al, 2011aHassler et al, , 2012. The distribution of Fe-binding organic ligands in the open ocean is compatible with multiple biological sources associated with Fe-stress and its recycling/remineralisation (Hunter and Boyd, 2007).…”

“…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).…”

Effect of melting Antarctic sea ice on the fate of microbial communities studied in microcosms

“…Several factors can increase the efficiency of the fertilization of the Antarctic surface waters: (1) the thinning of the mixed layer when freshwater is added also reduces the cellular Fe demand of pelagic algae required in light harvesting processes (Raven 1990); (2) Fe is released into seawater together with organic ligands, which increase the residence time of Fe in surface waters and therefore its bioavailability (van der Merwe et al 2009;Hassler et al 2011). The production of exopolysaccharides (EPS) by sea ice algae, however, stimulates the formation of aggregates and therefore lead to rapid sedimentation of ice-derived Fe (Riebesell et al 1991;Meiners et al 2004); and (3) heterotrophic activity in seawater favours the remineralization of Fe associated with ice-derived organic matter.…”