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

Abstract. Methylmercury (MeHg), accumulated in rice grains, is highly toxic for humans. Its production is largely driven by microbial methylation in paddy soils; however, dissolved organic matter (DOM) is a critical component of the soil biogeochemistry process, yet its interactions with microorganisms involved in MeHg production remain poorly understood. Here, we conducted hgcA gene sequencing and a genome-resolved metagenomic analysis to identify core Hg-methylating microbiomes and investigate the effect of DOM on core Hg-methylating microbiomes 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 that was exclusively associated with MeHg concentration. The partial Mantel test revealed strong linkages among core Hg-methylating microbiome composition, DOM, and MeHg concentration. Structural equation models further indicated that core Hg-methylating microbiome composition significantly impacted soil MeHg concentration, contributing 89 % of the observed variation, while DOM plays a crucial role in determining core Hg-methylating microbiome composition, accounting for 65 %. These results suggested that DOM regulates MeHg production by altering the composition of core Hg-methylating microbiomes. The presence of various genes associated with carbon metabolism in the metagenome-assembled genome of core Hg-methylating microorganisms suggests that different DOM stimulates the activity of core Hg-methylating microorganisms to methylate Hg, which was confirmed by a pure incubation experiment with Geobacter sulfurreducens PCA (a core Hg-methylating microorganism) amended with a 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.