Evolution of selenium utilization traits

Abstract

Background: The essential trace element selenium is used in a wide variety of biological processes. Selenocysteine (Sec), the 21st amino acid, is co-translationally incorporated into a restricted set of proteins. It is encoded by an UGA codon with the help of tRNASec (SelC), Sec-specific elongation factor (SelB) and a cis-acting mRNA structure (SECIS element). In addition, Sec synthase (SelA) and selenophosphate synthetase (SelD) are involved in the biosynthesis of Sec on the tRNASec. Selenium is also found in the form of 2-selenouridine, a modified base present in the wobble position of certain tRNAs, whose synthesis is catalyzed by YbbB using selenophosphate as a precursor.

Results: We analyzed completely sequenced genomes for occurrence of the selA, B, C, D and ybbB genes. We found that selB and selC are gene signatures for the Sec-decoding trait. However, selD is also present in organisms that do not utilize Sec, and shows association with either selA, B, C and/or ybbB. Thus, selD defines the overall selenium utilization. A global species map of Sec-decoding and 2-selenouridine synthesis traits is provided based on the presence/absence pattern of selenium-utilization genes. The phylogenies of these genes were inferred and compared to organismal phylogenies, which identified horizontal gene transfer (HGT) events involving both traits.

Conclusion: These results provide evidence for the ancient origin of these traits, their independent maintenance, and a highly dynamic evolutionary process that can be explained as the result of speciation, differential gene loss and HGT. The latter demonstrated that the loss of these traits is not irreversible as previously thought.

Figure 1

Distribution of selenium-utilization traits. The figure depicts the species tree for all organisms completely sequenced so far, based on the phylogenetic reconstruction using the small subunit rRNA sequences and is in good agreement with other consensus phylogenetic trees. Species able to decode Sec are those possessing selA (yellow) (excluding Archaea), selB (blue), selC (green) and selD (red). The presence of ybbB (gray) and selD indicates the ability to synthesize 2-selenouridine.

Figure 2

Phylograms of selA, selB, selC, selD and ybbB. Phylograms were inferred using phyML2.4 from curated T-Coffee alignments. The values above and below each branch indicate boostrap values (>70) of maximum likelihood analysis and posterior probabilities (>0.90) of Bayesian analysis respectively. In all trees γ-proteobacteria are highlighted in red, β-proteobacteria in blue and Sinorhizobium meliloti (α-proteobacteria) in green. Red circles denote putative horizontal gene transfer events.

Figure 3

Genome location of selA, selB, selC, selD and ybbB. Each bar represents one replicon of a species. On the vertical axis the species name, phylum, and domain are specified. The horizontal axis corresponds to the replicon size. Location of selA (yellow), selB (blue), selC (green), selD (red) and ybbB (black) is indicated; arrows denote direction of transcription.