Ancient origin and evolution of microbial mercury methylation

Abstract

The origin of microbial mercury methylation has long been a mystery. Here we employed genome-resolved phylogenetic analyses to decipher the evolution of the mercury methylating gene, hgcAB, constrain the ancestral origin of the hgc operon, and explain the distribution of hgc in Bacteria and Archaea. We infer the extent to which vertical inheritance and horizontal gene transfer have influenced the evolution of mercury methylators and hypothesize that evolution of this trait bestowed the ability to produce an antimicrobial compound (MeHg+) on a potentially resource-limited early Earth. We speculate that, in response, the evolution of MeHg+-detoxifying alkylmercury lyase (encoded by merB) reduced a selective advantage for mercury methylators and resulted in widespread loss of hgc in Bacteria and Archaea. SignificanceNeurotoxic methylmercury (MeHg+(aq)) is synthesized from HgII(aq) in the environment by microorganisms possessing the gene pair hgcAB. Our phylogenetic analyses elucidate the origin and evolution of the hgc operon, and support a hypothesis that mercury methylation evolved as an antimicrobial production mechanism, possibly from competition for limited resources on the early Earth. We infer from our analyses that hgc has been primarily vertically inherited in Bacteria and Archaea, with extensive parallel loss, and note that few taxa possessing hgc also possess the gene encoding for MeHg+ demethylation, merB. Our findings support the interpretation that merB evolved as a defense mechanism against the evolution of microbial HgII(aq) methylation.