Arsenic oxidation by root endophytes mediates arsenic speciation within rice (Oryza sativa)

Arsenic (As) uptake through rice consumption is a major exposure pathway that severely threatens the health of over 140 million people. Since flooded cultivation makes rice specifically vulnerable to As contamination, dry rice cultivation has been proposed to reduce As accumulation. While microorganisms play important roles in As biogeochemical cycles, the impact of the root-associated microbiome, especially endophytes, on As uptake and metabolism in rice growing under different water regimes remains elusive. In this study, different water regimes significantly altered As speciation in the rhizosphere but less impacted those in roots, in which As(V) dominated. While the endosphere community was significantly altered, microbial As transformation potentials were less impacted by different water treatments. Within rice roots, As(III) oxidase gene (aioA) abundance was consistently higher than that of the genes for As reduction (As(V) respiratory reductase arrA and As(V) detoxification reductase arsC) under both treatments, indicating that As(III) oxidation might be the major As transformation pathway in planta. Activity measurements of the endosphere microbial community demonstrated that As(III) oxidation was significantly faster compared to reduction processes. The major endosphere microbial communities harboring aioA genes were affiliated with Rhodocyclaceae, Xanthobacteraceae, and Burkholderiaceae under dry conditions, while members of Rhodocyclaceae dominated under flooded conditions. These results suggest that dominant microbial As(III) oxidation in rice roots may contribute to maintaining a higher As(V) proportion in planta and potentially reduce As translocation to edible grains.