Organoarsenical Biotransformations by Shewanella putrefaciens

Abstract

Microbes play a critical role in the global arsenic biogeocycle. Most studies have focused on redox cycling of inorganic arsenic in bacteria and archaea. The parallel cycles of organoarsenical biotransformations are less well characterized. Here we describe organoarsenical biotransformations in the environmental microbe Shewanella putrefaciens. Under aerobic growth conditions, S. putrefaciens reduced the herbicide MSMA (methylarsenate or MAs(V)) to methylarsenite (MAs(III)). Even though it does not contain an arsI gene, which encodes the ArsI C–As lyase, S. putrefaciens demethylated MAs(III) to As(III). It cleaved the C–As bond in aromatic arsenicals such as the trivalent forms of the antimicrobial agents roxarsone (Rox(III)), nitarsone (Nit(III)) and phenylarsenite (PhAs-(III)), which have been used as growth promoters for poultry and swine. S. putrefaciens thiolated methylated arsenicals, converting MAs(V) into the more toxic metabolite monomethyl monothioarsenate (MMMTAs(V)), and transformed dimethylarsenate (DMAs(V)) into dimethylmonothioarsenate (DMMTAs(V)). It also reduced the nitro groups of Nit(V), forming p-aminophenyl arsenate (p-arsanilic acid or p-AsA(V)), and Rox(III), forming 3-amino-4-hydroxybenzylarsonate (3A4HBzAs(V)). Elucidation of organoarsenical biotransformations by S. putrefaciens provides a holistic appreciation of how these environmental pollutants are degraded.

The antibiotic action of methylarsenite is an emergent property of microbial communities

“…Four different species of bacteria, Pseudomonas putida KT2440 (Yoshinaga et al , ), Burkholderia sp. MR1 (Yoshinaga et al , ), Shewanella putrefaciens 200 (Chen and Rosen, ) and Sinorhizobium meliloti RM1021 are capable of reducing MAs(V), demonstrating that multiple soil bacteria have the ability to reductively generate MAs(III). Neither E. coli ArsC (Oden et al , ) nor yeast Acr2p (Mukhopadhyay et al , ) reduce MAs(V) (unpublished results), and the pathway/genes/enzymes involved in MAs(V) reduction are as yet unknown.…”

“…Several bacterial strains have been identified that are capable of reducing MAs(V), including the environmental isolate Burkholderia sp. MR1 (Yoshinaga et al , ), as well as S. putrefaciens 200 (Chen and Rosen, ), P. putida KT2440 (Yoshinaga et al , ), and S. meliloti RM1021. To date, no specific genes/enzymes involved in MAs(V) reduction have been identified.…”

A novel MAs(III)‐selective ArsR transcriptional repressor

“…In S. putrefaciens 200, the arsenic ars cluster consists of 19 genes, which are regulated by three different arsR genes (Chen and Rosen, ). One, termed SparsR (accession number: ADV53698), is novel in its gene product has a two‐cysteine arsenic binding motif and lacks a third ligand for binding of inorganic As(III) compared to characterized ArsRs such as R773 ArsR, CgArsR and AfArsR.…”

The Arsenic Methylation Cycle: How Microbial Communities Adapted Methylarsenicals for Use as Weapons in the Continuing War for Dominance

“…This suggests that formation of thioarsenicals is non-enzymatic but does not eliminate the possibility of enzymatic pathways of synthesis. Environmental microbes such as Shewanella putrefaciens also thiolate methylated arsenicals, producing MMMTAs(V) and DMMTAs(V) (Rubin et al, 2014;Chen and Rosen, 2016). However, its mechanism is similarly, poorly understood.…”