ArxA From Azoarcus sp. CIB, an Anaerobic Arsenite Oxidase From an Obligate Heterotrophic and Mesophilic Bacterium

Abstract

Arsenic is a toxic element widely distributed in nature, but numerous bacteria are able to resist its toxicity mainly through the <i>ars</i> genes encoding an arsenate reductase and an arsenite efflux pump. Some "arsenotrophic" bacteria are also able to use arsenite as energy supplier during autotrophic growth by coupling anaerobic arsenite oxidation <i>via</i> the <i>arx</i> gene products to nitrate respiration or photosynthesis. Here, we have demonstrated that <i>Azoarcus</i> sp. CIB, a facultative anaerobic β-proteobacterium, is able to resist arsenic oxyanions both under aerobic and anaerobic conditions. Genome mining, gene expression, and mutagenesis studies revealed the presence of a genomic island that harbors the <i>ars</i> and <i>arx</i> clusters involved in arsenic resistance in strain CIB. Orthologous <i>ars</i> clusters are widely distributed in the genomes of sequenced <i>Azoarcus</i> strains. Interestingly, genetic and metabolic approaches showed that the <i>arx</i> cluster of the CIB strain encodes an anaerobic arsenite oxidase also involved in the use of arsenite as energy source. Hence, <i>Azoarcus</i> sp. CIB represents the prototype of an obligate heterotrophic bacterium able to use arsenite as an extra-energy source for anaerobic cell growth. The arsenic island of strain CIB supports the notion that metabolic and energetic skills can be gained by genetic mobile elements.