Overlooked role of soil microbial-derived carbon in promoting neurotoxic methylmercury production

The bioaccumulation of neurotoxic methylmercury (MeHg) in rice has raised global concerns due to its potential threat to human health. Organic carbon is a crucial factor influencing MeHg production in soils, as it regulates mercury bioavailability and microbial activity. However, the role of microbial-derived carbon, a critical source of soil organic matter, in regulating MeHg production remains unclear. Here, we compared the effect of microbial necromass (i.e., Gram-negative bacteria, Gram-positive bacteria, and fungi) and plant residues on microbial mercury methylation during incubation of paddy soil. Results showed that the addition of all four types of organic matter consistently resulted in higher MeHg concentrations, with Gram-negative bacterial necromass exhibiting the most significant enhancement (2.07-5.73 folds). By combining analyses of DNA-stable isotope probing and long-read sequencing of mercury methylation genes (i.e., hgcAB), we found that the promoting effect was associated with the increased proportions of methylators with high mercury methylation potential, such as Geobacter, in the treatment of Gram-negative bacterial necromass. Meanwhile, Fourier transform ion cyclotron resonance mass spectrometry analyses revealed that the decomposition of microbial necromass and plant residues released more sulfur-containing compounds compared with the control, and this increased mercury bioavailability by forming complexes with mercury in the soil. These findings highlight the critical role of soil microbial-derived carbon in enhancing Hg methylation and emphasize the importance of the source of organic matter when predicting MeHg production in environments.