On the 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.

Keywords: hgc gene; LUCA; antimicrobial; evolution; gene loss; horizontal gene transfer; mercury; methylmercury.

Fig. 1.

Phylogenetic tree of the protein family PF03599. (A) Unrooted tree of the protein family PF03599. The tree was inferred by using the ML method under LG + C50 + F + R model. This analysis involved 478 amino acid sequences with a total of 2,922 positions in the alignments. Different taxonomies are represented by different colors. Ultrafast bootstrap support values were calculated with 1,000 replications, and ultrafast bootstrap values > 90% are shown by black dots at the nodes. (B) PF03599 tree rooted by the midpoint. Clades whose average branch length distance to their leaves are below 1.5 are collapsed with iTOL for better visualization.

Fig. 2.

Phylogenetic tree of HgcA proteins. The tree was inferred by using the ML method under LG + C60 + F + G model. This analysis involved alignment of 169 amino acid sequences with a total of 493 positions. Different taxonomies are represented by different colors. Ultrabootstrap support values were calculated with 1,000 replications, and ultrabootstrap values > 90% are shown by black dots at the nodes. Experimentally validated functional and nonfunctional HgcA sequences are labeled by solid and hollow stars. Fused-HgcAB sequences are indicated by a gray background.

Fig. 3.

Cophylogenetic tree of HgcA and HgcB. The phylogeny of HgcA shown on the left is the same as figure 2. The phylogeny of HgcB shown on the right was inferred by using the ML method under LG + C60 + F + G model. Lines between the two trees connect HgcA (left) and HgcB (right) proteins from the same proteome, illustrating the degree of congruency in their respective phylogenetic associations. This analysis involved alignment of 169 amino acid sequences with a total of 322 positions. Taxonomies of the HgcB sequences are represented in the same colors as shown in the HgcA phylogeny. Ultrabootstrap support values were calculated with 1,000 replications, and ultrabootstrap values > 90% are shown by black dots at the nodes. Gray-shaded blocks describe fused-HgcAB and “HgcB tail” genes in the two trees, respectively. The green dots at the tip of the HgcA tree represent the corresponding hgcA without downstream hgcB, and the red triangle represents the corresponding fused-hgcAB with another hgcB downstream.

Fig. 4.

Phylogenetic tree of MerB proteins. The tree was inferred by using the ML method under LG + C40 + F + G model. This analysis involved alignment of 223 amino acid sequences with a total of 1,448 positions. Different taxonomies are represented by different colors. Ultrabootstrap support values were calculated with 1,000 replications, and ultrabootstrap values > 90% are shown by black dots at the nodes.

Fig. 5.

Species tree of hgcA+ and merB+ genomes in the RP35 data set. The tree was inferred from a concatenate of 27 marker genes derived from Moody et al. (2022) by using the ML method under LG + F + R10 model. This analysis involved alignment of 251 amino acid sequences with a total of 8,024 positions. Different taxonomies are represented by different colors. The presence of genes hgcA/fused-hgcAB/hgcB/merB in the genomes was represented by different symbols and colors in the outer circle. Ultrabootstrap support values were calculated with 1,000 replications, and ultrabootstrap values > 90% are shown by black dots at the nodes.