Ancient origin and evolution of microbial mercury methylation

The origin and evolution of microbial mercury methylation have long remained a mystery. Here we employed genome-resolved phylogenetic analyses to decipher the evolution of the mercury methylating genes hgcAB, to constrain the ancestral origin of the hgc operon, and to explain its current distribution across the bacterial and archaeal domains. We infer the extent to which vertical descent and horizontal gene transfer have influenced the evolution of this operon and hypothesize that the original function of methylmercury was as an antimicrobial compound on the early Earth. We speculate that subsequent evolution of the detoxifying agent alkylmercury lyase (merB) reduced the selective advantage of the mercury methylation activity, resulting in widespread loss of the hgcAB genes among archaea and bacteria. Significance Neurotoxic methylmercury (MeHg+) is synthesized from HgII in the environment by microorganisms, involving the gene pair hgcA and hgcB. However, the origin and evolution of these two genes are poorly understood. Our phylogenetic analyses revealed the evolutionary history of the hgc gene pair and uncovered a link between the evolution of Hg methylation and demethylation. We show that the hgc gene has undergone generally vertical evolution with extensive parallel gene loss, and we propose that mercury methylation evolved as an antimicrobial production mechanism during competition for limited energy resources on the early Earth.