Dissolved organic matter fosters core mercury-methylating microbiome for methylmercury production in paddy soils

Abstract. Methylmercury (MeHg), accumulated in rice grain, is highly toxic for human. Its production is largely driven by microbial methylation in paddy soils; however, dissolved organic matter (DOM) represents a hotspot for soil biogeochemistry, resulting in MeHg production, remain poorly understood. Here, we conducted hgcA gene sequencing and genome-resolved metagenomic analysis to identify core Hg-methylating microbiome and investigate the effect of DOM on core Hg-methylating microbiome in paddy soils across a Hg contamination gradient. In general, the Hg-methylating microbial communities varied largely with the degree of Hg contamination in soils. Surprisingly, a core Hg-methylating microbiome was identified exclusively associated with MeHg concentration. The partial Mantel test revealed strong linkages among core Hg-methylating microbiome composition, DOM and MeHg concentration. Structural equation model further indicated that core Hg-methylating microbiome composition significantly impacted soil MeHg concentration (accounting for 89 %); while DOM was crucial in determining core Hg-methylating microbiome composition (65 %). These results suggested that DOM regulates MeHg production by altering the composition of core Hg-methylating microbiome. The presence of various genes associated with carbon metabolism in the metagenome-assembled genome of core Hg-methylating microorganisms suggests that different DOMs stimulate the activity of core Hg-methylating microorganisms to methylate Hg, which was confirmed by pure incubation experiment with Geobacter sulfurreducens PCA (core Hg-methylating microorganism) amended with natural DOM solution extracted from investigated soils. Overall, DOM simultaneously changes core Hg-methylating microbiome composition and functional activity and thus enhances MeHg production in paddy soils.