| Abstract |
Manganese oxide minerals are strong oxidants capable of degrading recalcitrant carbon compounds and altering the speciation of trace metals. While the majority of Mn oxidation in the environment is believed to be biologically catalyzed, the mechanism(s) underlying the oxidation and mineral formation processes remain enigmatic. New evidence demonstrates that some microbes oxidize Mn(II) to Mn(III) through the production of extracellular superoxide, but that extracellular superoxide production does not necessarily confer the ability to precipitate Mn oxide minerals. We predict that the presence of additional exuded biomolecules is requisite for the formation of Mn oxide minerals following the initial oxidation step. Biomolecules may (a) stabilize the intermediate Mn(III) species against reduction so that the second electron transfer can occur and/or (b) provide a nucleation site or template for the Mn(IV) oxide mineral. To test this hypothesis, we explored the presence of Mn(III) ligands and examined mineral-organic associations in Mn oxides formed by two common marine Mn(II)-oxidizing bacteria. Solid-phase extraction of Mn-associated organic molecules during the course of oxidation from Mn(II) to Mn(III) followed by characterization with HPLC-ICP-MS indicates an array of relatively polar ligands. Bulk NEXAFS spectroscopy of rinsed Mn biooxides reveals a strong protein-mineral association. Protein extractions of rinsed minerals and cell-free filtrate contain a significant fraction of animal heme peroxidases, implicating this specific protein in Mn(III) oxidation and/or Mn oxide precipitation. This research suggests that Mn(III) complexation and MnOx templation are requisite components for the formation of Mn oxides following Mn(II) oxidation by superoxide. Microbes forming Mn oxides by the superoxide pathway must therefore exude a range of molecules to facilitate these steps. The results of this study guide future efforts to quantify the extent of Mn cycling in the environment by identifying molecular characteristics of biologically mediated Mn oxide formation. |
