Biological oxidation of As(III) and Sb(III) by a novel bacterium with Sb(III) oxidase rather than As(III) oxidase under anaerobic and aerobic conditions

Abstract

Sb and As are chemically similar, but the sequences and structures of Sb(III) and As(III) oxidase are totally distinct. It is thus interesting to explore whether Sb(III) oxidase oxidizes As(III), and if so, how microbial oxidations of Sb(III) and As(III) influence one another. Previous investigations have yielded ambiguous or even erroneous conclusions. This study aimed to clarify this issue. Firstly, we prepared a consortium of Sb(III)-oxidizing prokaryotes (SOPs) by enrichment cultivation. Metagenomic analysis reveals that SOPs with the Sb(III) oxidase gene, but lacking the As(III) oxidase gene are predominant in the SOP community. Despite this, SOPs exhibit comparable Sb(III) and As(III)-oxidizing activities in both aerobic and anaerobic conditions, indicating that at the microbial community level, Sb(III) oxidase can oxidize As(III). Secondly, we isolated a representative cultivable SOP, Ralstonia sp. SbOX with Sb(III) oxidase gene but without As(III) oxidase gene. Genomic analysis of SbOX reveals that this SOP strain has a complete Sb(III) oxidase (AnoA) gene, but lacks As(III) oxidase (AioAB or ArxAB) gene. It is interesting to discover that, besides its Sb(III) oxidation activities, SbOX also exhibits significant capabilities in oxidizing As(III) under both aerobic and anaerobic conditions. Moreover, under aerobic conditions and in the presence of both Sb(III) and As(III), SbOX exhibited a preference for oxidizing Sb(III). Only after the near complete oxidation of Sb(III) did SbOX initiate rapid oxidation of As(III). In contrast, under anaerobic conditions and in the presence of both Sb(III) and As(III), Sb(III) oxidation notably inhibited the As(III) oxidation pathway in SbOX, while As(III) exhibited minimal effects on the Sb(III) oxidation. These findings suggest that SOPs can oxidize As(III) under both aerobic and anaerobic conditions, exhibiting a strong preference for Sb(III) over As(III) oxidation in the presence of both. This study unveils a novel mechanism of interaction within the Sb and As biogeochemical cycles.