Mining-impacted rice paddies select for Archaeal methylators and reveal a putative (Archaeal) regulator of mercury methylation

Methylmercury (MeHg) is a microbially produced neurotoxin derived from inorganic mercury (Hg), which accumulation in rice represents a major health concern to humans. However, the microbial control of MeHg dynamics in the environment remains elusive. Here, leveraging three rice paddy fields with distinct concentrations of Hg (Total Hg (THg): 0.21−513 mg kg−1 dry wt. soil; MeHg: 1.21−6.82 ng g−1 dry wt. soil), we resorted to metagenomics to determine the microbial determinants involved in MeHg production under contrasted contamination settings. We show that Hg methylating Archaea, along with methane-cycling genes, were enriched in severely contaminated paddy soils. Metagenome-resolved Genomes of novel putative Hg methylators belonging to Nitrospinota (UBA7883), with poorly resolved taxonomy despite high completeness, showed evidence of facultative anaerobic metabolism and adaptations to fluctuating redox potential. Furthermore, we found evidence of environmental filtering effects that influenced the phylogenies of not only hgcA genes under different THg concentrations, but also of two housekeeping genes, rpoB and glnA, highlighting the need for further experimental validation of whether THg drives the evolution of hgcAB. Finally, assessment of the genomic environment surrounding hgcAB suggests that this gene pair may be regulated by an archaeal toxin-antitoxin (TA) system, instead of the more frequently found arsR-like genes in bacterial methylators. This suggests the presence of distinct hgcAB regulation systems in bacteria and archaea. Our results support the emerging role of Archaea in MeHg cycling under mining-impacted environments and shed light on the differential control of the expression of genes involved in MeHg formation between Archaea and Bacteria.