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Methylmercury (MeHg) is a hazardous neurotoxin, predominantly formed by microbial transformation of inorganic mercury in oxygen-depleted aquatic and terrestrial ecosystems. The ongoing deoxygenation of aquatic ecosystems due to global warming is likely to expand microbial niches for MeHg production. Although mercury methylators have also been reported to thrive in oxyge-deficients conditions in a few marine and freshwater ecosystems, there is a lack of comprehensive understanding of how they are distributed in freshwater systems. In this study, we retrieved hgcA genes, genomic marker for mercury methylation potential, from 586 metagenomes from the water column of 186 freshwater systems. Overall, hgcA genes were detected in the water column of 30 lakes, with the highest richness and abundance being detected in anoxic (0 mg O2L^-1) and hypoxic (>0–2 mg O2L^-1) compared to oxic conditions (>2 mg O2L^-1). Although Desulfobacterota had the highest hgcA gene richness across most freshwater systems, certain systems were dominated by hgcA genes from Bacteroidales and Kiritimatiellales, implying metabolic and ecological versatility of mercury methylators as a group. Our findings suggest that projected expanding deoxygenation may lead to new niches for mercury methylators in inland waters.