Genome sequence and characterisation of a freshwater photoarsenotroph, Cereibacter azotoformans strain ORIO, isolated from sediments capable of cyclic light-dark arsenic oxidation and reduction

Abstract

A freshwater photosynthetic arsenite-oxidizing bacterium, Cereibacter azotoformans strain ORIO, was isolated from Owens River, CA, USA. The waters from Owens River are elevated in arsenic and serve as the headwaters to the Los Angeles Aqueduct. The complete genome sequence of strain ORIO is 4.8 Mb genome (68% G + C content) and comprises two chromosomes and six plasmids. Taxonomic analysis placed ORIO within the Cereibacter genus (formerly Rhodobacter). The ORIO genome contains arxB₂ AB₁ CD (encoding an arsenite oxidase), arxXSR (regulators) and several ars arsenic resistance genes all co-localised on a 136 kb plasmid, named pORIO3. Phylogenetic analysis of ArxA, the molybdenum-containing arsenite oxidase catalytic subunit, demonstrated photoarsenotrophy is likely to occur within members of the Alphaproteobacteria. ORIO is a mixotroph, oxidises arsenite to arsenate (As(V)) photoheterotrophically, and expresses arxA in cultures grown with arsenite. Further ecophysiology studies with Owens River sediment demonstrated the interconversion of arsenite and As(V) was dependent on light-dark cycling. arxA and arrA (As(V) respiratory reductase) genes were detected in the light-dark cycled sediment metagenomes suggesting syntrophic interactions among arsenotrophs. This work establishes C. azotoformans str. ORIO as a new model organism for studying photoarsenotrophy and light-dark arsenic biogeochemical cycling.