Ligand-Enhanced Abiotic Iron Oxidation and the Effects of Chemical versus Biological Iron Cycling in Anoxic Environments

Abstract

This study introduces a newly isolated, genetically tractable bacterium (Pseudogulbenkiania sp. strain MAI-1) and explores the extent to which its nitrate-dependent iron-oxidation activity is directly biologically catalyzed. Specifically, we focused on the role of iron chelating ligands in promoting chemical oxidation of Fe(II) by nitrite under anoxic conditions. Strong organic ligands such as nitrilotriacetate and citrate can substantially enhance chemical oxidation of Fe(II) by nitrite at circumneutral pH. We show that strain MAI-1 exhibits unambiguous biological Fe(II) oxidation despite a significant contribution (∼30–35%) from ligand-enhanced chemical oxidation. Our work with the model denitrifying strain Paracoccus denitrificans further shows that ligand-enhanced chemical oxidation of Fe(II) by microbially produced nitrite can be an important general side effect of biological denitrification. Our assessment of reaction rates derived from literature reports of anaerobic Fe(II) oxidation, both chemical and biological, highlights the potential competition and likely co-occurrence of chemical Fe(II) oxidation (mediated by microbial production of nitrite) and truly biological Fe(II) oxidation.

Potential Role of Nitrite for Abiotic Fe(II) Oxidation and Cell Encrustation during Nitrate Reduction by Denitrifying Bacteria

“…When nitrite diffuses through this EPS layer, green rust and goethite minerals form on the outside of the EPS layer, catalyzing Fe(II) oxidation and Fe(III) mineral formation (31,46,69). This mechanism would also explain the observations of (i) Fe(III) mineral formation without direct contact with the cells despite the low solubility of Fe(III) (14), (ii) oxidation of Fe(II) by sterile-filtered supernatants (67), and (iii) formation of an Fe(III) mineral coating on Shewanella putrefaciens cells incubated with Fe 2ϩ and NO 2 Ϫ (69). Is cell encrustation deleterious?…”

Fe(II) Oxidation Is an Innate Capability of Nitrate-Reducing Bacteria That Involves Abiotic and Biotic Reactions

“…A more extensive treatment of the accelerating effect that metal ligands have on the rate of microbial Fe(II) oxidation was recently published (53), and the authors demonstrated that NO 2 Ϫ reacts more rapidly with Fe(II)-NTA than with unchelated Fe(II), suggesting another possible explanation for the high rate of Fe(II)-NTA oxidation by A. ebreus (Fig. 3b) (53). However, Fe(II)-NTA-agarose beads, which cannot penetrate the outer membrane, showed no oxidation by A. ebreus cell suspensions (Fig.…”

“…Some NDFO organisms, such as Pseudogulbenkiania ferrooxidans (67) or Pseudogulbenkiania sp. strain MAI-1 (53), release higher concentrations of extracellular NO 2 Ϫ during organotrophic nitrate reduction, which can react with extracellular Fe(II), especially in the presence of catalytic mineral phases, such as green rusts (21,48,49), or chelating ligands (53). However, NO should also be considered.…”

“…Also, metal efflux pumps may function to keep Fe(II) out of the periplasm (Fig. 2) reduction may be directly catalyzed by Nar, Nir, and Nor (54) or other periplasmic components or through abiotic reactions that can be accelerated by ligands (53). If the rate of Fe(II) oxidation and Fe(III) mineral precipitation is faster than the rate of efflux, precipitation of Fe(II) minerals on periplasmic proteins will lead to their inhibition and NO 2 Ϫ , NO, and N 2 O accumulation (see Fig.…”

Sedimentology of the ∼3.3 Ga upper Mendon Formation, Barberton Greenstone Belt, South Africa

“…Although the coatings occur on some silica grains, they are most common and best-developed on volcanic grains. Previous studies have identified anaerobic nitrate-dependent Fe(II)-oxidizing organisms capable of utilizing Fe(II) in mineral phases, including goethite, siderite, pyrite, neosilicates, and phyllosilicates (Chaudhuri et al, 2001;Weber et al, 2001;Shelobolina et al, 2003), although other studies have highlighted that Fe(II) oxidation can also occur abiotically by reacting with nitrite, a metabolic intermediate of denitrification (Cooper et al, 2003;Coby and Picardal, 2005;Pantke et al, 2011;Carlson et al, 2012;Picardal, 2012;Kopf et al, 2013).…”