Anoxygenic phototrophic arsenite oxidation by a Rhodobacter strain

Abstract

Microbially mediated arsenic redox transformations are key for arsenic speciation and mobility in rice paddies. Whereas anaerobic anoxygenic photosynthesis coupled to arsenite (As(III)) oxidation has been widely examined in arsenic-replete ecosystems, it remains unknown whether this light-dependent process exists in paddy soils. Here, we isolated a phototrophic purple bacteria, Rhodobacter strain CZR27, from an arsenic-contaminated paddy soil and demonstrated its capacity to oxidize As(III) to arsenate (As(V)) using malate as a carbon source photosynthetically. Genome sequencing revealed an As(III)-oxidizing gene cluster (aioXSRBA) encoding an As(III) oxidase. Functional analyses showed that As(III) oxidation under anoxic phototrophic conditions correlated with transcription of the large subunit of the As(III) oxidase aioA gene. Furthermore, the non-As(III) oxidizer Rhodobacter capsulatus SB1003 heterologously expressing aioBA from strain CZR27 was able to oxidize As(III), indicating that aioBA was responsible for the observed As(III) oxidation in strain CZR27. Our study provides evidence for the presence of anaerobic photosynthesis-coupled As(III) oxidation in paddy soils, highlighting the importance of light-dependent, microbe-mediated arsenic redox changes in paddy arsenic biogeochemistry.