Multicopper oxidase involvement in both Mn(II) and Mn(III) oxidation during bacterial formation of MnO(2) - PubMed (original) (raw)

Multicopper oxidase involvement in both Mn(II) and Mn(III) oxidation during bacterial formation of MnO(2)

Alexandra V Soldatova et al. J Biol Inorg Chem. 2012 Dec.

Abstract

Global cycling of environmental manganese requires catalysis by bacteria and fungi for MnO(2) formation, since abiotic Mn(II) oxidation is slow under ambient conditions. Genetic evidence from several bacteria indicates that multicopper oxidases (MCOs) are required for MnO(2) formation. However, MCOs catalyze one-electron oxidations, whereas the conversion of Mn(II) to MnO(2) is a two-electron process. Trapping experiments with pyrophosphate (PP), a Mn(III) chelator, have demonstrated that Mn(III) is an intermediate in Mn(II) oxidation when mediated by exosporium from the Mn-oxidizing bacterium Bacillus SG-1. The reaction of Mn(II) depends on O(2) and is inhibited by azide, consistent with MCO catalysis. We show that the subsequent conversion of Mn(III) to MnO(2) also depends on O(2) and is inhibited by azide. Thus, both oxidation steps appear to be MCO-mediated, likely by the same enzyme, which is indicated by genetic evidence to be the MnxG gene product. We propose a model of how the manganese oxidase active site may be organized to couple successive electron transfers to the formation of polynuclear Mn(IV) complexes as precursors to MnO(2) formation.

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Figures

Fig. 1

Fig. 1. TEM of MnO2-coated spores from Bacillus sp. SG-1 [9]

Fig. 2

Fig. 2

UV-vis absorption spectra of exosporium (50 μL in 1 mL of HEPES buffer) (black), Mn(III)-pyrophosphate complex (100 μM in HEPES buffer) (red), and MnO2 suspension in water (blue) used as basis spectra for a linear squares fit analysis of the UV-vis absorption spectra taken over 30 h experiments of Mn oxidation catalyzed by exosporium

Fig. 3

Fig. 3

Time-resolved UV-vis absorption spectral measurements of Mn(II) oxidation by exosporium at room temperature. (a) Selected UV-vis absorption spectra of the reaction mixture taken at the indicated time points during the course of Mn(II) oxidation. The growth of 265 nm band indicates formation of the Mn(III) intermediate trapped by pyrophosphate; the 400 nm band is due to formation of particulate Mn oxides. (b) Time courses followed by Mn(III)-pyrophosphate and MnO2 species during the 30 h UV-vis absorption experiment and obtained from the fit of the absorption spectrum at each time point to a linear combination of the component spectra depicted in Fig.2

Fig. 4

Fig. 4

Time-resolved UV-vis absorption spectral measurements of Mn(III) oxidation by exosporium at room temperature. (a) Selected UV-vis absorption spectra of the reaction mixture taken at the indicated time points during Mn(III) oxidation. The growth of the 400 nm band indicates formation of the particulate Mn oxides. (b) Time courses followed by Mn(III)-pyrophosphate and MnO2 species during the 30 h UV-vis absorption experiment and obtained from the fit of the absorption spectrum at each time point to a linear combination of the component spectra depicted in Fig. 2

Fig. 5

Fig. 5

UV-vis absorption spectra of the reaction mixture taken at the indicated time points during Mn(III) oxidation by exosporium (a) under anaerobic condition; (b) with 10 mM azide present. Both conditions, exclusion of oxygen and addition of azide, resulted in inhibition of Mn(III) oxidation

Fig. 6

Fig. 6

Possible pathways for bacterial MnO2 formation by MCO-catalyzed Mn(II) to Mn(III) oxidation followed by further oxidation (top) or by disproportionation (bottom) of complexed Mn(III)

Fig. 7

Fig. 7

Structure of human ceruloplasmin (pdb #:1KCW) showing mononuclear type 1 copper site, and “substrate” and “holding” cation-binding sites in domain 6. Arrow indicates a movement of sidechain E935 from the substrate site to the holding site upon iron translocation after oxidation. Adapted from ref. [28]

Fig. 8

Fig. 8. Proposed mechanism of Mn(II) oxidation and MnO2 formation catalyzed by manganese oxidase, MnxG (see text for details)

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