Rhizosphere microbiota drives biogeochemical arsenic transformations in rice paddies amended with sulfate

Submerged rice paddies are affected by arsenic release into the pore-water from iron (oxy)hydroxides dissolution, with subsequent uptake by the plant and translocation to the grains and specific limits for inorganic arsenic content in rice grains have been established by the European Union. These regulations do not take into account thiolated inorganic and organic arsenics, recognized to be toxic and that have been recently demonstrated to be transported to rice plants. The mechanisms and contribution of biotic and abiotic factors are still poorly characterized. In this study, the role of the rhizosphere microbiota on arsenic concentration and speciation in rice paddies and grains was assessed. Open air mesocosms were set up with rice plants cultivated in soils with different carbon content and sulfate fertilization. Rhizosphere soil and pore-water microbiomes were characterized by monitoring the main physic-chemical parameters and by 16S rRNA genes Illumina sequencing over rice growing season. Phylogenetic and functional genes related to arsenic, sulfur and iron metabolisms were quantified by real-time quantitative PCR. According to Illumina libraries, in all mesocosms, microbiotas in rhizosphere soil and in pore-water differed greatly in terms of both phylogenetic composition and relative abundances. Within the same compartment, soil type mainly drove bacterial and archaeal diversity whereas sulfate amendment did not. However, within the rare biosphere, sulfate fertilization promoted sulfate-reducing, sulfur-oxidizing, arsenate-reducing and arsenite-methylating microorganisms. These results related to a proportional increase of methylated arsenic species in the pore-water and in rice grains, and total arsenic decrease in the medium-carbon soil. These findings indicate a strong link between sulfur- and arsenic-cycling mediated by rice rhizosphere microbiota, with essential implications on revision of possible strategies to deal with arsenic contamination in rice.