title: Surface Mn(II) oxidation actuated by a multicopper oxidase in a soil bacterium leads to the formation of manganese oxide minerals.
abstract: In this manuscript, we report that a bacterial multicopper oxidase (MCO266) catalyzes Mn(II) oxidation on the cell surface, resulting in the surface deposition of Mn(III) and Mn(IV) oxides and the gradual formation of bulky oxide aggregates. These aggregates serve as nucleation centers for the formation of Mn oxide micronodules and Mn-rich sediments. A soil-borne Escherichia coli with high Mn(II)-oxidizing activity formed Mn(III)/Mn(IV) oxide deposit layers and aggregates under laboratory culture conditions. We engineered MCO266 onto the cell surfaces of both an activity-negative recipient and wild-type strains. The results confirmed that MCO266 governs Mn(II) oxidation and initiates the formation of deposits and aggregates. By contrast, a cell-free substrate, heat-killed strains, and intracellularly expressed or purified MCO266 failed to catalyze Mn(II) oxidation. However, purified MCO266 exhibited Mn(II)-oxidizing activity when combined with cell outer membrane component (COMC) fractions in vitro. We demonstrated that Mn(II) oxidation and aggregate formation occurred through an oxygen-dependent biotic transformation process that requires a certain minimum Mn(II) concentration. We propose an approximate electron transfer pathway in which MCO266 transfers only one electron to convert Mn(II) to Mn(III) and then cooperates with other COMC electron transporters to transfer the other electron required to oxidize Mn(III) to Mn(IV).
authors.affiliation: 1] State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan 430070, China [2] Key Laboratory of Subtropical Agricultural Resource and Environment, Ministry of Agriculture, Huazhong Agricultural University, Wuhan 430070, China.
authors.forename: Zhen
authors.initials: Z
authors.lastname: Zhang
authors.affiliation: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan 430070, China.
authors.forename: Zhongming
authors.initials: Z
authors.lastname: Zhang
authors.affiliation: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan 430070, China.
authors.forename: Hong
authors.initials: H
authors.lastname: Chen
authors.affiliation: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan 430070, China.
authors.forename: Jin
authors.initials: J
authors.lastname: Liu
authors.affiliation: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan 430070, China.
authors.forename: Chang
authors.initials: C
authors.lastname: Liu
authors.affiliation: School of Life Science, Hubei University, Wuhan 430062, China.
authors.forename: Hong
authors.initials: H
authors.lastname: Ni
authors.affiliation: Key Laboratory of Subtropical Agricultural Resource and Environment, Ministry of Agriculture, Huazhong Agricultural University, Wuhan 430070, China.
authors.forename: Changsong
authors.initials: C
authors.lastname: Zhao
authors.affiliation: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan 430070, China.
authors.forename: Muhammad
authors.initials: M
authors.lastname: Ali
authors.affiliation: Key Laboratory of Subtropical Agricultural Resource and Environment, Ministry of Agriculture, Huazhong Agricultural University, Wuhan 430070, China.
authors.forename: Fan
authors.initials: F
authors.lastname: Liu
authors.affiliation: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan 430070, China.
authors.forename: Lin
authors.initials: L
authors.lastname: Li
mesh_terms: D001419:Bacteria / Q000378:metabolism*; D004926:Escherichia coli / Q000378:metabolism / Q000648:ultrastructure; D007700:Kinetics; D008345:Manganese / Q000378:metabolism*; D017895:Manganese Compounds / Q000378:metabolism*; D010084:Oxidation-Reduction; D010087:Oxides / Q000378:metabolism*; D010088:Oxidoreductases / Q000378:metabolism*; D012988:Soil Microbiology
chemical_list: D017895:Manganese Compounds; D010087:Oxides; D008345:Manganese; C027424:manganese oxide; D010088:Oxidoreductases; C024748:copper oxidase