Iron Isotope Fractionation during Fe(II) Oxidation Mediated by the Oxygen-Producing Marine Cyanobacterium Synechococcus PCC 7002

Abstract

In this study, we couple iron isotope analysis to microscopic and mineralogical investigation of iron speciation during circumneutral Fe(II) oxidation and Fe(III) precipitation with photosynthetically produced oxygen. In the presence of the cyanobacterium Synechococcus PCC 7002, aqueous Fe(II) (Fe(II)_aq) is oxidized and precipitated as amorphous Fe(III) oxyhydroxide minerals (iron precipitates, Fe_ppt), with distinct isotopic fractionation (ε⁵⁶Fe) values determined from fitting the δ⁵⁶Fe(II)_aq (1.79‰ and 2.15‰) and the δ⁵⁶Fe_ppt (2.44‰ and 2.98‰) data trends from two replicate experiments. Additional Fe(II) and Fe(III) phases were detected using microscopy and chemical extractions and likely represent Fe(II) and Fe(III) sorbed to minerals and cells. The iron desorbed with sodium acetate (Fe_NaAc) yielded heavier δ⁵⁶Fe compositions than Fe(II)_aq. Modeling of the fractionation during Fe(III) sorption to cells and Fe(II) sorption to Fe_ppt, combined with equilibration of sorbed iron and with Fe(II)_aq using published fractionation factors, is consistent with our resulting δ⁵⁶Fe_NaAc. The δ⁵⁶Fe_ppt data trend is inconsistent with complete equilibrium exchange with Fe(II)_aq. Because of this and our detection of microbially excreted organics (e.g., exopolysaccharides) coating Fe_ppt in our microscopic analysis, we suggest that electron and atom exchange is partially suppressed in this system by biologically produced organics. These results indicate that cyanobacteria influence the fate and composition of iron in sunlit environments via their role in Fe(II) oxidation through O₂ production, the capacity of their cell surfaces to sorb iron, and the interaction of secreted organics with Fe(III) minerals.

Figure 1

(a) Bottle 1 and (b) bottle 2 are biological replicates of the Fe(II) oxidation experiment with Synechococcus PCC 7002. Green circles are δ⁵⁶Fe(II)_aq data; orange squares are δ⁵⁶Fe_ppt data; blue diamonds are δ⁵⁶Fe_NaAc data. The solid green lines are the Rayleigh fits of the δ⁵⁶Fe(II)_aq data, with an ε⁵⁶Fe for Fe(II)_aq of 1.79‰ (a) to 2.15‰ (b). The solid orange lines are the Rayleigh fits of the δ⁵⁶Fe_ppt data, with ε⁵⁶Fe for δ⁵⁶Fe_ppt of 2.44‰ (a) and 2.98‰ (b). The linear fits are shown as dotted lines for reference.

Figure 2

(a) X-ray diffraction (XRD) pattern obtained from X-ray total scattering data of the Fe_ppt phase after complete Fe(II) oxidation, freeze-drying, and water washing. The indexed reflections for lepidocrocite (Lp) and goethite (Gt) are shown. (b) A 3-component linear combination fit of 58% ferrihydrite, 22% goethite, and 20% lepidocrocite (Supplementary Table 4).

Figure 3

CLSM images of Synechococcus PCC 7002 cultured anoxically with 4.5 mM Fe(II). (a) Autofluorescent cells, (b) stained with the lectin-binding dye SBA-488, (c) the reflection signal from Fe(III) minerals, and (d) an overlay of (a–c). Correlation plot of the fluorescence intensity in individual pixels from (e) autofluorescence (a) vs SBA-488 (b) and (f) SBA-488 (b) vs Fe(III) minerals (c). This analysis demonstrates that EPS, which is bound by SBA-488, is coating Fe(III) minerals but is not spatially associated with cells.

Figure 4

Controls on the overall iron isotope fractionation in the system are (1) Fe(II) oxidation and precipitation of Fe(III) as Fe_ppt; (2) sorption of Fe(III) to cells; (3) partial equilibrium atom and electron exchange after sorption of Fe(II)_aq to Fe_ppt. (1) generates Fe_ppt (solid orange line) that is 2–3‰ heavier than Fe(II)_aq (solid green line). (2) produces sorbed Fe(III) on cells with an estimated equilibrium Δ⁵⁶Fe_{FeNaAc-Fe(II)aq} of 1.84‰. (3) produces Fe(II) sorbed on goethite with an estimated Δ⁵⁶Fe_{FeNaAc-Fe(II)aq} of 0.8‰. The resulting δ⁵⁶Fe_NaAc predicted from (2) and (3) are denoted by the light blue diamonds.