Microbial Arsenic Methylation and Microbial Reduction of Dimethylarsenate Contribute to the Production of Highly Toxic Dimethylarsenite in Paddy Soil

Dimethylarsenic (DMAs) is a causal agent of rice straighthead disease, a physiological disorder resulting in severe yield losses. Both pentavalent [DMAs(V)] and trivalent [DMAs(III)] forms of DMAs have been detected in anoxic paddy soils. However, the extent of DMAs(III) toxicity to rice plants and the pathways and mechanisms underlying its generation in paddy soils remain poorly understood. In the present study, we showed that DMAs(III) was more toxic to rice plants and induced more severe straighthead disease than DMAs(V) in hydroponic experiments. Incubation of 11 paddy soils under flooded conditions confirmed the prevalence of DMAs(III) in the soil solution. We used pure cultures of bacteria isolated from paddy soils and in vitro enzyme assays to reveal two pathways of DMAs(III) generation. In the first pathway, DMAs(III) was produced via arsenic methylation by Paraclostridium benzoelyticum TC8 and in vitro by the recombinant arsenite S-adenosylmethionine methyltransferase (ArsM). In the second pathway, DMAs(III) was generated through anaerobic microbial reduction of DMAs(V). Using gene deletion and heterologous expression, we showed that glutathione or cysteine plays an important role in DMAs(V) reduction in Enterobacter CZ-1. These findings advance our understanding of the arsenic biogeochemistry in paddy soil regarding the production of highly toxic DMAs(III).