Water-fertilizer regulation drives microorganisms to promote iron, nitrogen and manganese cycling: A solution for arsenic and cadmium pollution in paddy soils

Abstract

The co-contamination of arsenic (As) and cadmium (Cd) in rice fields presents a global imperative for resolution. However, understanding the complex microbially driven geochemical processes and network connectivity crucial for As and Cd bioavailability under the frequent redox transitions in rice fields remains limited. Here, we conducted a series of microcosm experiments, using flooding and drainage, alongside fertilization treatments to emulate different redox environment in paddy soils. Soil As significantly reduced in drained conditions following applications of biochar or calcium-magnesium-phosphate (CMP) fertilizers by 26.3 % and 31.2 %, respectively, with concurrent decreases in Cd levels. Utilizing geochemical models, we identified the primary redox cycles dynamically altering during flooding (Fe and S cycles) and drainage (Fe, Mn, and N cycles). PLS-SEM elucidated 76 % and 61 % of the variation in Cd and As through Mn and N cycles. Functional genes implicated in multi-element cycles were analyzed, revealing a significantly higher abundance of assimilatory N reduction genes (nasA, nirA/B, narB) in drained soil, whereas an increase in ammonia-oxidizing genes (amoA/B) and a decrease in nitrate reduction to ammonium genes were observed after CMP fertilizer application. Biochar application led to significant enrichment of the substrate-binding protein of the Mn transport gene (mntC). Moreover, Fe transport genes were enriched after biochar or CMP application compared to drained soils. Among 40 high-quality metagenome-assembled genomes (MAGs), microbial predictors associated with low Cd and As contents across different treatments were examined. Bradyrhizobacea harbored abundant Mn and Fe^III transport genes, while Nitrososphaeraceae carried nitrification-related genes. Two MAGs affiliated with Caulobacteraceae, carrying diverse Fe transport genes, were enriched in biochar-applied soils. Therefore, applying CMP fertilizer or biochar in aerobic rice fields can synergistically reduce the bioavailability of Cd and As by specifically enhancing the circulation of essential elements.

Keywords: Arsenic; Cadmium; Fertilizer regime; Microbial process; Water regime.