Abstract
Massive amounts of methyl [e.g., methylarsenate, MAs(V)] and aromatic arsenicals [e.g., roxarsone (4-hydroxy-3-nitrophenylarsonate, Rox(V)] have been utilized as herbicides for weed control and growth promotors for poultry and swine, respectively. The majority of these organoarsenicals degrade into more toxic inorganic species. Here, we demonstrate that the legume symbiont Sinorhizobium meliloti both reduces MAs(V) to MAs(III) and catalyzes sequential two-step reduction of nitro and arsenate groups in Rox(V), producing the highly toxic trivalent amino aromatic derivative 4-hydroxy-3-aminophenylarsenite (HAPA(III)). The existence of this process suggests that S. meliloti possesses the ability to transform pentavalent methyl and aromatic arsenicals into antibiotics to provide a competitive advantage over other microbes, which would be a critical process for the synthetic aromatic arsenicals to function as antimicrobial growth promoters. The activated trivalent aromatic arsenicals are degraded into less-toxic inorganic species by an MAs(III)-demethylating aerobe, suggesting that environmental aromatic arsenicals also undergo a multiple-step degradation pathway, in analogy with the previously reported demethylation pathway of the methylarsenate herbicide. We further show that an FAD-NADPH-dependent nitroreductase encoded by mdaB gene catalyzes nitroreduction of roxarsone both in vivo and in vitro. Our results demonstrate that environmental organoarsenicals trigger competition between members of microbial communities, resulting in gradual degradation of organoarsenicals and contamination by inorganic arsenic.
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