The influence of extracellular superoxide on iron redox chemistry and bioavailability to aquatic microorganisms

Abstract

Superoxide, the one-electron reduced form of dioxygen, is produced in the extracellular milieu of aquatic microbes through a range of abiotic chemical processes and also by microbes themselves. Due to its ability to promote both oxidative and reductive reactions, superoxide may have a profound impact on the redox state of iron, potentially influencing iron solubility, complex speciation, and bioavailability. The interplay between iron, superoxide, and oxygen may also produce a cascade of other highly reactive transients in oxygenated natural waters. For microbes, the overall effect of reactions between superoxide and iron may be deleterious or beneficial, depending on the organism and its chemical environment. Here I critically discuss recent advances in understanding: (i) sources of extracellular superoxide in natural waters, with a particular emphasis on microbial generation; (ii) the chemistry of reactions between superoxide and iron; and (iii) the influence of these processes on iron bioavailability and microbial iron nutrition.

Keywords: bioavailability; iron; superoxide.

Figure 1

Major sources of ${\text{O}}_{\text{2}}^{-*}$ in natural waters. (A) Abiotic, photochemical oxidation of natural organic matter (NOM) with concomitant reduction of O₂. (B) Biological reduction of O₂ in the extracellular milieu via cell surface enzymes. (C) Biological reduction of oxidized labile redox-active compounds (LRAC_ox) in the extracellular milieu to form reduced labile redox-active compounds (LRAC_red) that subsequently reduce O₂ to ${\text{O}}_2^{-*}.$ (D) Biological release of LRAC_red into the extracellular milieu that subsequently reduce O₂ to ${\text{O}}_2^{-*}.$ (E) Diffusion of LRAC_red produced under suboxic conditions into more oxygenated waters. (F) The ${\text{O}}_2/{\text{O}}_2^{-*}$ couple readily exchanges electrons with a range of other labile redox-active compounds in the extracellular milieu. Decay pathways for ${\text{O}}_2^{-*}$ are not shown.

Figure 2

Transformations between various pools of Fe as mediated by ${\text{O}}_2^{-*}$. (A) Polynuclear complexes, which contain multiple Fe atoms and may also contain other inorganic and organic ligands. (B) Mononuclear inorganic complexes. (C) Mononuclear organic complexes. Fe(III) in all pools may be reduced by the ${\text{O}}_2^{-}$ anion to Fe(II), while Fe(II) in all pools may be oxidized to Fe(III) primarily by $\text{HO}{\text{O}}^{\bullet },$ but also indirectly by ${\text{O}}_2^{-}.$ The dotted arrows denote the dissociative reduction (DR) pathway, while the dashed arrows denote the non-dissociative reduction (NDR) pathway for Fe(III) reduction by ${\text{O}}_2^{-*}.$

Figure 3

Simplified steady-state model for Fe chemistry in a spatially homogeneous system containing ${\text{O}}_{\text{2}}^{-*}$ and a single ligand (L) that forms a 1:1 complex with Fe, showing relevant rate constants.

Figure 4

Effect of ${\text{O}}_{\text{2}}^{-*}$ on Fe bioavailability in a system containing a single Fe complexing ligand. (A) Steady-state $\left[{\text{O}}_2^{-*}\right]=0$ (B) Steady-state $\left[{\text{O}}_2^{-*}\right]=100\text{\hspace{0.17em}pM}$ (C) Steady-state $\left[{\text{O}}_2^{-*}\right]=100\text{\hspace{0.17em}pM}$ (D) Steady-state $\left[{\text{O}}_2^{-*}\right]=1\text{\hspace{0.17em}nM}$. Panels show the resulting pFe′ [= −log[Fe′] _T = −log([Fe(II)′] + [Fe(III)′]) at steady-state. The contours shown in each panel represent constant pFe′ values, as indicated by the numbers marked on the contour lines. The region to the bottom right of the dashed lines in each panel approximately indicates conditions where the strength of the Fe(II) complex relative to that of the Fe(III) complex is sufficiently high that the presence of ${\text{O}}_2^{-*}$ decreases Fe bioavailability.