The importance of siderophores in iron nutrition of heterotrophic marine bacteria

Abstract

Recent studies demonstrate that dissolved iron in seawater is bound to strong organic complexes that have stability constants comparable to those of microbial iron chelates. We examined iron acquisition by seven strains of heterotrophic marine bacteria from a number of siderophore-iron complexes, including desferrioxamine B (DFB) and marine siderophores partially purified from iron-limited cultures. Hydroxamate siderophores were detected in the supernatants of four strains, one of which also produced a catechol. All strains transported iron bound to siderophores regardless of whether or not they produced their own, and the majority took up iron bound to DFB. Uptake rates of Fe siderophores were similar among iron-limited strains and among ligands. Transport of FeDFB by strain Neptune was enhanced 20 times by iron limitation, whereas uptake of unchelated iron (FeЈ) did not saturate at the highest concentration tested and was not regulated by the iron nutritional status of the cells. The half-saturation constant for uptake of FeDFB by Neptune was 15 nM, the lowest reported for an Fe siderophore in any microorganism. Iron uptake by the catechol-producing strain, LMG1, differed markedly in two respects from the other strains: LMG1 could not take up iron bound to DFB; furthermore, transport of FeЈ by iron-limited LMG1 was 10 times faster than the other strains and was upregulated 46 times compared to Fe-sufficient cells. Experimental evidence suggests that iron transport by LMG1 may be mediated by surface-associated catechol siderophores that scavenge inorganic ferric species as well as iron bound to weaker complexes, such as EDTA (ethylenediaminetetraacetic acid). The combined results of the study highlight the importance of siderophores in iron transport by heterotrophic marine bacteria and suggest, by inference, that bacteria may rely on siderophores to acquire iron in situ.

Microbial iron uptake in the naturally fertilized waters in the vicinity of the Kerguelen Islands: phytoplankton–bacteria interactions

“…Iron uptake rates, Fe cellular contents and Fe : C ratios have been determined in various environments (Tortell et al, 1996;Maldonado et al, 2001;Sarthou et al, 2008). Culture experiments (Granger and Price, 1999;Fourquez et al, 2014) have elucidated some of the metabolic pathways affected by Fe limitation which may explain the changes observed in Fe-limited heterotrophic cells or communities. Additionally, the obligate requirement of Fe for heterotrophic bacteria and phytoplankton suggests that both organisms are competing for Fe acquisition.…”

Enhancement of the reactive iron pool by marine diatoms

“…marine bacteria to scavenge and transport Fe (Granger and Price, 1999;Trick, 1989;Wilhelm and Trick, 1994), that are photo-reactive (Barbeau, 2006;Barbeau et al, 2001). Photoredox reactions of Fe-ligand complexes occur via a ligand to metal charge transfer (LMCT) reaction resulting in the production of Fe(II) and an irreversible decomposed organic ligand (Waite and Morel, 1984).…”

Saharan dust nutrients promote Vibrio bloom formation in marine surface waters

“…Dissolved Fe (dFe) is believed to be the most biologically available fraction of Fe, but is present in vanishingly low amounts in marine systems around the world, especially due to the low solubility of Fe(III) in seawater (17). Heterotrophic bacteria, including Vibrio, play a key role in Fe cycling (14,15,18,19), in part by modulating Fe solubility through secretion of high-affinity Fe-chelating siderophores (20,21). Fe-siderophore complexes allow active uptake into the bacterial cell (20) and provide a usable exogenous source of Fe for phytoplankton (22,23).…”

“…Heterotrophic bacteria, including Vibrio, play a key role in Fe cycling (14,15,18,19), in part by modulating Fe solubility through secretion of high-affinity Fe-chelating siderophores (20,21). Fe-siderophore complexes allow active uptake into the bacterial cell (20) and provide a usable exogenous source of Fe for phytoplankton (22,23). Although most studies of Fe enrichment in marine systems have focused on autotrophs (24,25), heterotrophic bacteria have been shown to have a higher Fe per biomass quota than many phytoplankton (18), accounting for up to 80% of the total planktonic uptake in some systems (26).…”