Genome-resolved metatranscriptomic analysis of arsenic demethylation and detoxification in a methanogenic rice paddy soil

Abstract

Microbial methylation and demethylation of arsenic in rice paddy soils influence the speciation and toxicity of arsenic in rice, with implications for human health and rice yields. Here, we combine genome-resolved metatranscriptomics with arsenic speciation analysis in methanogenic paddy soil incubations to elucidate microbial pathways regulating As demethylation, with emphasis on: (i) evaluating links between methyltransferase gene transcription by methylotrophic methanogens and arsenic demethylation; and (ii) assessing how toxicity-induced microbial responses regulate As demethylation and the resulting distribution of As species. Experiments with dimethylarsinic (DMAs) and 2-bromoethanesulfonate as a methanogenesis inhibitor confirm an important role of methanogens in anaerobic arsenic demethylation. Amendment of the methylotrophic substrate trimethylamine accelerated arsenic demethylation and induced an association between arsenic demethylation rates and the transcription of diverse methylotrophic methyltransferases. Six Methanosarcina metagenome assembled genomes dominated methyltransferase transcription and concurrently transcribed genes involved in multiple (methyl)arsenic oxidation and efflux pathways, illustrating a link between putative demethylation and arsenic detoxification at the genome level. Paddy soil incubations also demonstrated toxicity-driven feedbacks between DMAs concentrations and demethylation rates, wherein higher DMAs concentrations inhibited methanogenesis and decreased pseudo first-order demethylation rate constants. These findings provide new insights into links between methylotrophic methanogenesis and arsenic demethylation in anaerobic conditions, with implications for biogeochemical control of arsenic speciation in rice paddy soils.