Methylation of arsenic differs with substrates in Arcticibacter tournemirensis R1 from an As-contaminated paddy soil

Abstract

Arsenic can be methylated by arsenite (As(III)) S-adenosylmethionine methyltransferases (ArsMs) among various kingdoms of life. The intermediate product methylarsenite (MAs(III)) is highly toxic and can be utilized as an antibiotic by some microbes. ArsM gene is widely distributed in the members of every kingdom from bacteria to humans and displays a high diversity of sequence. Based on arsenic methylating capacity, ArsM proteins can be divided into two phylogenetically distinct clades (Groups 1 and 2). In this study, we show that Arcticibacter tournemirensis R1 isolated from arsenic contaminated paddy soil is resistant to both As(III) and MAs(III), but exhibits different methylation activities for As(III) and MAs(III). The A. tournemirensis R1 shows low As(III) methylation activity and produces an unknown arsenic compound. In contrast, it shows high methylation activity with MAs(III), with the main product of dimethylarsenate (DMAs(V)). An AtarsM gene is found in ars operon of A. tournemirensis R1 genome and is regulated by an atypical transcriptional repressor ArsR. Expressed in Escherichia coli AtArsM confers resistance to As(III) and MAs(III). Both in vivo and in vitro assays show that AtArsM methylates As(III) and MAs(III) to dimethyl- and trimethyl‑arsenicals. AtArsM has four conserved cysteine residues, which are present in most ArsMs and can be classified into phylogenetic group 2 family, producing trimethylated arsenic metabolites. The high arsenic methylation and volatilization activity of AtArsM provides a potential strategy for arsenic bioremediation. The methylation activity differs with As(III) and MAs(III) in A. tournemirensis R1 indicates that there may have different detoxification mechanisms for As(III) and MAs(III), which are worth investigating in the future.