Enhanced ferrihydrite dissolution by a unicellular, planktonic cyanobacterium: a biological contribution to particulate iron bioavailability

Abstract

Iron (Fe) bioavailability, as determined by its sources, sinks, solubility and speciation, places severe environmental constraints on microorganisms in aquatic environments. Cyanobacteria are a widespread group of aquatic, photosynthetic microorganisms with especially high iron requirements. While iron exists predominantly in particulate form, little is known about its bioavailability to cyanobacteria. Some cyanobacteria secrete iron solubilizing ligands called siderophores, yet many environmentally relevant strains do not have this ability. This work explores the bioavailability of amorphous synthetic Fe-oxides (ferrihydrite) to the non-siderophore producing, unicellular cyanobacterium, Synechocystis sp PCC 6803. Iron uptake assays with ferrihydrite established dissolution as a critical prerequisite for iron transport. Dissolution assays with the iron binding ligand, desferrioxamine B, demonstrated that Synechocystis 6803 enhances ferrihydrite dissolution, exerting siderophore-independent biological influence on ferrihydrite bioavailability. Dissolution mechanisms were studied using a range of experimental conditions; both cell-particle physical proximity and cellular electron flow were shown to be important determinants of bio-dissolution by Synechocystis 6803. Finally, the effects of ferrihydrite stability on bio-dissolution rates and cell physiology were measured, integrating biological and chemical aspects of ferrihydrite bioavailability. Collectively, these findings demonstrate that Synechocystis 6803 actively dissolves ferrihydrite, highlighting a significant biological component to mineral phase iron bioavailability in aquatic environments.

Iron Uptake Mechanisms in Marine Phytoplankton

“…The preferred collection of iron-rich particles and rejection of iron-free particles suggest the ability to sense iron and selectively utilize ironrich dust particles (Kessler et al, 2020). The ability of a cyanobacterium to solubilize ferrihydrite particles has been shown in Synechocystis PCC 6803 (Kranzler et al, 2016). The main mechanisms for dissolving mineral iron from dust include reductive dissolution and siderophore-mediated dissolution, both being thought to be involved in Trichodesmium dust utilization (Basu et al, 2019;Eichner et al, 2019).…”

Mineral iron utilization by natural and cultured Trichodesmium and associated bacteria

“…Mineral Fe uptake assays 55 Ferrrihydrite: Synthesis and solubility 55 Ferrihydrite (amorphous Fe oxyhydroxide) was synthesized as described earlier (Rubin et al 2011;Kranzler et al 2016). Briefly, the mineral was formed by gradual titration of an acidic solution of 55 FeCl 3 (0.5M HCl, specific activity 10.18 mCi mg 21 , Perkin Elmer) with 0.1 N NaOH to pH 8.…”

“…Solid Fe is not directly available to most phytoplankton, which can internalize only soluble Fe (Rich and Morel ). The utilization of particulate Fe by phytoplankton is hence restricted by the low solubility of many of the solid Fe forms as well as rapid sinking loss of particulate Fe from the euphotic column (Shaked and Lis ; Kranzler et al ).…”

Why microbes secrete molecules to modify their environment: the case of iron-chelating siderophores

“…Furthermore, inorganic ferric iron can be acquired directly using ATP-binding cassette transporters that are frequently detected in marine bacterial genomes [31,32]. In addition, surface-associated reductases allow uptake from particulate iron [33][34][35], outer membrane receptors mediate uptake of iron bound to exogenous chelators like heme or transferrin [36], and ferric citrate can be taken up via transporters or porins [37].…”