Oxygen Dependency of Neutrophilic Fe(II) Oxidation by Leptothrix Differs from Abiotic Reaction

Abstract

Neutrophilic Fe(II) oxidizing microorganisms are found in many natural environments. It has been hypothesized that, at low oxygen concentrations, microbial iron oxidation is favored over abiotic oxidation. Here, we compare the kinetics of abiotic Fe(II) oxidation to oxidation in the presence of the bacterium Leptothrix cholodnii Appels isolated from a wetland sediment. Rates of Fe(II) oxidation were determined in batch experiments at 20°C, pH 7 and oxygen concentrations between 3 and 120 μmol/l. The reaction progress in experiments with and without cells exhibited two distinct phases. During the initial phase, the oxygen dependency of microbial Fe(II) oxidation followed a Michaelis-Menten rate expression (K_M = 24.5 ± 10 μmol O₂/l, v_max = 1.8 ± 0.2 μmol Fe(II)/(l min) for 10⁸ cells/ml). In contrast, abiotic rates increased linearly with increasing oxygen concentrations. At similar oxygen concentrations, initial Fe(II) oxidation rates were faster in the experiments with bacteria. During the second phase, the accumulated iron oxides catalyzed further oxidative iron precipitation in both abiotic and microbial reaction systems. That is, abiotic oxidation also dominated the reaction progress in the presence of bacteria. In fact, in some experiments with bacteria, iron oxidation during the second phase proceeded slower than in the absence of bacteria, possibly due to an inhibitory effect of extracellular polymeric substances on the growth of Fe(III) oxides. Thus, our results suggest that the competitive advantage of microbial iron oxidation in low oxygen environments may be limited by the autocatalytic nature of abiotic Fe(III) oxide precipitation, unless the accumulation of Fe(III) oxides is prevented, for example, through a close coupling of Fe(II) oxidation and Fe(III) reduction.

Keywords:

• neutrophilic Fe(II) oxidation
• Leptothrix cholodnii
• oxygen dependency
• Michaelis-Menten kinetics

Acknowledgments

We thank Juanjuan Wang for the 16S RNA analysis of the isolated Leptothrix cholodnii Appels strain. Funding was provided by Utrecht University and the Darwin Center for Biogeosciences project 1030: The role of microbial activity in iron-deposition in wetland ecosystems. This is publication number DW-2012-1002 of the Darwin Center for Biogeosciences.