On the origin and evolution of microbial mercury methylation

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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 thehgcoperon, and explain the distribution ofhgcin 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 bymerB) reduced a selective advantage for mercury methylators and resulted in widespread loss ofhgcin Bacteria and Archaea.

Significance

Neurotoxic methylmercury (MeHg+(aq)) is synthesized from HgII(aq)in the environment by microorganisms possessing the gene pairhgcAB. Our phylogenetic analyses elucidate the origin and evolution of thehgcoperon, 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 thathgchas been primarily vertically inherited in Bacteria and Archaea, with extensive parallel loss, and note that few taxa possessinghgcalso possess the gene encoding for MeHg+demethylation,merB. Our findings support the interpretation thatmerBevolved as a defense mechanism against the evolution of microbial HgII(aq)methylation.

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