Mn(III,IV) oxide mineral formation by bacterial oxidation of dissolved Mn(II) is an important process in aquatic and soil environments and is a key pathway of the global Mn cycle. Putative Mn(II)-oxidizing multicopper oxidase (MCO) enzymes have been identified in many bacteria, and the enzyme from Bacillus sp. PL-12, MnxG, has recently been expressed and purified. MCO enzymes use redox-active copper cofactors to couple the oxidation of a metal or organic substrate to the reduction of dioxygen to water. Unique among MCOs, MnxG is tightly bound to small accessory proteins, MnxE and MnxF, and supports not one, but two, successive one-electron oxidation steps, [Mn(II/III) and Mn(III/IV)], producing nanoparticulate Mn(IV) oxide biominerals. No other class of MCOs has a biomineral as a final product. The uniqueness of the Mnx manganese oxidase complex comes from the necessity to catalyze two energetically distinct oxidation reactions, where substrate, intermediate, and product require different ligand coordination. Using various spectroscopic methods, we showed that MnxG is a low-potential multicopper oxidase that exploits manganese polynuclear chemistry to (1) lower the Mn(III/II) reduction potential and enable electron transfer, (2) facilitate further oxidation of Mn(III) to Mn(IV), and (3) produce the oxide lattice of biomineral MnO2. The immediate enzyme product is likely a dimer, Mn(IV)(μ-O)2Mn(IV), or an oligomer, from which MnO2 nanoparticles nucleate and grow in a classical manner. Using a variety of synthetic MnO2 preparations, we have begun characterizing the Mnx-produced MnO2 nanoparticles, comparing them with the synthetic analogs. The initial detectable MnO2 products appear as small as 1 nm in diameter, and continue to grow to 50-80 nm nanoparticles. The accessory proteins, MnxE and MnxF, are not involved in the oxidation reaction, but possibly assist in nucleating and stabilizing MnO2 mineral products. Once formed, the biogenic MnO2, with a structure similar to birnessite, can undergo structural and redox transformation to other mineral phases. Microbial oxidation of Mn2+ is the likely origin of most MnO2 in the environment. The study of molecular mechanism of its formation, enabled by the purified manganese oxidase complex, provides intricate details on the process of how manganese biomineralization is accomplished, and advises us on how the properties of MnO2 biominerals can be controlled for environmental and technological applications.

Manganese(IV) oxide formation by a bacterial manganese oxidase

255th National Meeting (2018)

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