Kinetic constraints for the formation of microniches for microaerophilic Fe(II) oxidation

Samenvatting

Oxidation of Fe(II) by oxygen (O₂) at circumneutral pH occurs abiotically or is mediated by microaerophilic Fe(II)-oxidizing bacteria. Abiotic Fe(II) oxidation(s) compete with microbial processes and the relative contribution of abiotic reactions depend on the chemical conditions, e.g. P_O2, pH and the presence and identity of ferric (oxyhydr)oxide mineral surfaces, catalyzing the heterogeneous reaction. At circumneutral pH, abiotic Fe(II) oxidation proceeds rapidly, which raises the question how and to which extent neutrophilic microaerophilic Fe(II)-oxidizing bacteria can compete with chemical reactions and gain metabolic energy from microbial Fe(II) oxidation. In this study, we have investigated the environmental constraints for microaerophilic Fe(II) oxidation in a film layer characterized by diffusive supply of both atmospheric O₂ (from the top) and dissolved Fe(II) (from the bottom) by use of a numerical model. A coupled diffusion–reaction model was tested at different chemical (pH and alkalinity gradients) and physical (film layer thickness) parameters to investigate their effects on the relative contributions of different reactions (abiotic homogeneous, heterogeneous and biological Fe(II) oxidation) to the overall (net) Fe(II) oxidation. A first order rate constant for biological oxidation was derived from experimental data from simplifcation of a Monod rate law to be 0.06 h⁻¹. The simulations demonstrate distinct spatial oxidation rate patterns for all of the considered reactions. Microaerophilic Fe(II) oxidation is predominant at a uniform pH 6 and a film thickness z of 1 mm with minor importance at pH 7. Maximum biological rates were on the order of 7∙10^-10 mol L⁻¹ s⁻¹ and are in the range of experimentally observed values. Minimum rates were close to the thermodynamic limit. In the presence of a pH gradient and z ≤ 1 mm, two distinct zones were observed: an upper zone dominated by abiotic Fe(II) oxidation (pH ∼ 7) and a lower zone dominated by microaerophilic Fe(II) oxidation (pH < 6.3), while the position and extent of the zones depend on the alkalinity. Such separation is strongly amplified for thinner films (z = 0.2 mm). The importance of heterogenous oxidation depends both on the pH and the amount of ferric (oxyhydr)oxides formed which increases with decreasing diffusive O₂ supply at z > 1 mm. In combination with high resolution imaging of pH values in a biofilm, our simulations underpin the importance of pH gradients in allowing for the formation of microniches. The conditions suitable for microaerophilic Fe(II) oxidation can be predicted based on reaction time scales and three factors were identified to be especially important: i) a pH low enough (<6.3) to outcompete abiotic processes; ii) sufficiently fast diffusive supply of Fe(II) (e.g. by Fe(III)-reducing bacteria or chemical processes) with O₂ concentrations below 150 μmol L⁻¹; iii) sufficient energy gain from Fe(II) oxidation reaction considering the thermodynamic factor F_T. We end by discussing strategies that Fe(II)-oxidizing microorganisms can employ to enhance their competitiveness against abiotic reactions.