Anaerobic arsenic methylation as a microbial warfare strategy

Abstract

ABSTRACTMicrobial arsenic methylation is established as a detoxification process under aerobic conditions (converting arsenite to monomethylated arsenate) but proposed to be a microbial warfare strategy under anoxic conditions due to the toxicity of its main product monomethylarsonous acid (MMAs(III)). Here we leveraged a paddy soil-derived anaerobic arsenic methylator,Paraclostridium bifermentansstrain EML to gain insights into this process. Strain EML was inoculated into a series of media involving systematic dilutions of Reinforced Clostridial Broth (RCB) with 25 μM arsenite to assess the impact of growth substrate on arsenic methylation. Concentrations of MMAs(III) andarsMgene transcription were found to be positively correlated with the RCB dilution, suggesting that substrate limitation enhancesarsMgene expression and associated anaerobic arsenic methylation. Anaerobic co-cultures of strain EML with either wild-typeEscherichia coliK-12 MG1655 (WT) orE. coliexpressing the MMAs(III)-resistance gene (arsP), ArsPE. coli, evidenced increased MMAs(III) production in the presence ofE. colithan its absence and growth inhibition of WTE. colito a greater extent than ArsPE. coli, presumably due to MMAs(III) produced by strain EML. Our findings point to an ecological role for anaerobic arsenic methylation, providing support for a microbial warfare function for this process.SYNOPSISUnderstanding the controls on anaerobic microbial arsenic methylation is relevant for rice paddy soils and helps to ensure food security.Graphic abstract