Understanding the Development and Stabilization of Mn(III) Intermediates during Microbial Manganese Reduction

Abstract:

The dominant products of Mn(II) oxidation are manganese(IV)-oxide phases, which act as important environmental oxidants and sorbents in soils, freshwater, and marine sediments. Mn(IV) oxides also provide favorable electron acceptors for metal-reducing microbes, but the intermediates and final products formed are highly dependent on environmental conditions, and challenging to predict thermodynamically. We engineered a flow-through reactor system to study the Mn phases during microbial Mn(IV) reduction by Shewanella oneidensis MR-1 in real time, using synchrotron X-ray absorption spectroscopy (XAS) to monitor redox and mineralogical changes. These 10-20 hour experiments capture Mn XAS spectra every 20 minutes and thus we can observe both transient phases and stable products under different experimental conditions. We also record the pH, collect solution and filtered solid samples throughout the experiments for later solute measurements, and confirm mineral identifications with synchrotron x-ray diffraction measurements. With excess organic carbon and high (mM) phosphate (like in a soil), Mn(IV) oxides are reduced to Mn(II) and immediately form Mn(II) phosphate in a clearly binary system. This experiment demonstrates that while there may be two successive single-electron transfer reactions from outer membrane cytochromes (Lin et al, 2012), the microbial reduction of Mn(IV) oxides is effectively a two-electron process. However, with minimal phosphate, a transient Mn(III) oxyhydroxide forms before all manganese is reduced to Mn(II) in solution and precipitates a final Mn(II)-carbonate product. We propose this Mn(III) intermediate phase forms due to reaction of Mn²⁺ in solution with Mn(IV)-oxide surfaces to form Mn(III)OOH, similar to experimental results from this abiotic comproportionation reaction (Elzinga, 2011). Recently, we stabilized this Mn(III) intermediate by limiting the organic carbon available to S. oneidensis, producing Mn(III)OOH and Mn(II) phases—an enigmatic but common assemblage in Mn-rich sedimentary rocks deposited on Earth after the rise of oxygen. Understanding how the reductive arm of the manganese cycle functions under a variety of environmental conditions will allow us to better predict the fate of Mn phases in a range of both modern and ancient environments.