Mercury methylation by metabolically versatile and cosmopolitan marine bacteria

Microbes transform aqueous mercury (Hg) into methylmercury (MeHg), a potent neurotoxin that accumulates in terrestrial and marine food webs, with potential impacts on human health. This process requires the gene pair hgcAB, which encodes for proteins that actuate Hg methylation, and has been well described for anoxic environments. However, recent studies report potential MeHg formation in suboxic seawater, although the microorganisms involved remain poorly understood. In this study, we conducted large-scale multi-omic analyses to search for putative microbial Hg methylators along defined redox gradients in Saanich Inlet, British Columbia, a model natural ecosystem with previously measured Hg and MeHg concentration profiles. Analysis of gene expression profiles along the redoxcline identified several putative Hg methylating microbial groups, including Calditrichaeota, SAR324 and Marinimicrobia, with the last the most active based on hgc transcription levels. Marinimicrobia hgc genes were identified from multiple publicly available marine metagenomes, consistent with a potential key role in marine Hg methylation. Computational homology modelling predicts that Marinimicrobia HgcAB proteins contain the highly conserved amino acid sites and folding structures required for functional Hg methylation. Furthermore, a number of terminal oxidases from aerobic respiratory chains were associated with several putative novel Hg methylators. Our findings thus reveal potential novel marine Hg-methylating microorganisms with a greater oxygen tolerance and broader habitat range than previously recognized.

Automated summary

This study identified potential novel marine Hg-methylating microorganisms with greater oxygen tolerance and broader habitat range than previously recognized, by conducting large-scale multi-omic analyses in a natural ecosystem and analyzing gene expression profiles along defined redox gradients. The findings highlighted the presence of putative microbial Hg methylators, such as Calditrichaeota, SAR324, and Marinimicrobia, with the latter showing the highest activity levels based on hgc transcription. Computational modeling predicted the functionality of HgcAB proteins from Marinimicrobia in Hg methylation, suggesting a key role in marine Hg methylation for this microbial group. Additionally, the study also associated several putative novel Hg methylators with terminal oxidases from aerobic respiratory chains.