Inter-relationships of MnO2 precipitation, siderophore Mn(III) complex formation, siderophore degradation, and iron limitation in Mn(II)-oxidizing bacterial cultures

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To examine the pathways that form Mn(III) and Mn(IV) in the Mn(II)-oxidizing bacterial strains Pseudomonas putida GB-1 and MnB1, and to test whether the siderophore pyoverdine (PVD) inhibits Mn(IV)O2 formation, cultures were subjected to various protocols at known concentrations of iron and PVD. Depending on growth conditions, P. putida produced one of two oxidized Mn species either soluble PVD Mn(III) complex or insoluble Mn(IV)O2 minerals but not both simultaneously. PVD Mn(III) was present, and MnO2 precipitation was inhibited, both in iron-limited cultures that had synthesized 26 50 μM PVD and in iron-replete (non-PVD-producing) cultures that were supplemented with 10 550 μM purified PVD. PVD Mn(III) arose by predominantly ligand-mediated air oxidation of Mn(II) in the presence of PVD, based on the following evidence: (a) yields and rates of this reaction were similar in sterile media and in cultures, and (b) GB-1 mutants deficient in enzymatic Mn oxidation produced PVD Mn(III) as efficiently as wild type. Only wild type, however, could degrade PVD Mn(III), a process linked to the production of both MnO2 and an altered PVD with absorbance and fluorescence spectra markedly different from those of either PVD or PVD Mn(III). Two conditions, the presence of bioavailable iron and the absence of PVD at concentrations exceeding those of Mn, both had to be satisfied for MnO2 to appear. These results suggest that P. putida cultures produce soluble Mn(III) or MnO2 by different and mutually inhibitory pathways: enzymatic catalysis yielding MnO2 under iron sufficiency or PVD-promoted oxidation yielding PVD Mn(III) under iron limitation. Since PVD-producing Pseudomonas species are environmentally prevalent Mn oxidizers, these data predict influences of iron (via PVD Mn(III) versus MnO2) on the global oxidation/reduction cycling of various pollutants, recalcitrant organic matter, and elements such as C, S, N, Cr, U, and Mn.

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