Periphyton-Driven Arsenic Methylation in Paddy Soils: The Crucial Role of Trophic Interactions

Arsenic (As) methylation facilitated by periphyton in paddy soils is crucial for its biogeochemical cycling and thus its bioavailability. However, the key functional taxa and underlying interactive metabolisms remain unclear due to the high complexity of the periphytic microbiome. Here, we employ DNA-stable isotope probing with metagenomic binning analysis to uncover the critical role of intrinsic trophic interactions in stimulating As methylation within the periphyton in association with soil inorganic carbon. Abundance of As-methylating microorganisms in the periphyton increases by 2.1-fold after bicarbonate addition. Members of phototrophs are predominantly responsible for regulating the stability of the periphytic microbiome, of which photoautotrophs (e.g., Oscillatoriales) initiate carbon fixation and constitute a major portion of As-methylating populations. These phototrophs further offer requisite organic substrates such as polysaccharides for heterotrophic bacteria (e.g., Chitinophagales) that in return foster the growth of the periphytic community, while these taxa simultaneously detoxify As through biomethylation to secure their ecological niches in periphyton. Such a symbiotic metabolism between phototrophs and heterotrophs facilitates carbon sequestration and shapes the functional community, collaboratively determining methylated As production in paddy soils. These findings offer new insights into the influence of trophic interactions within the periphyton on As speciation with potential implications for element cycling and soil remediation in paddy soils.