Evolution of selenium utilization traits
© Romero et al.; licensee BioMed Central Ltd. 2005
Received: 20 April 2005
Accepted: 27 June 2005
Published: 27 July 2005
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.
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.
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.
Selenium (Se) is an essential trace element for numerous organisms that belong to the three domains of life. The most relevant biological form of selenium is the rare amino acid selenocysteine (Sec), the selenium analog of cysteine (Cys). Sec is co-translationally incorporated into protein [1–3]. In functionally characterized selenoproteins, Sec is the catalytic group in the active site and is directly involved in redox catalysis. It is thought that Sec confers a functional advantage over cysteine at these active sites, increasing the catalytic efficiency of the enzymes . Despite this selective advantage, the set of selenoproteins in any given organism is small [5, 6].
Sec is inserted into selenoproteins at in-frame UGA codons (usually termination codons) by tRNASec (SelC) [2, 7]. Interpretation of UGA as Sec requires translational reprogramming, which is provided by the Sec insertion sequence (SECIS) element, a cis-acting stem-loop structure present in the selenoprotein mRNA . The decoding of Sec in bacteria also involves a Sec-specific elongation factor (SelB) which binds GTP, the SECIS element and the tRNASec [8, 9]. In eukaryotes, this function is carried out by two proteins: EF-Sec and SECIS-binding protein (SBP2). EF-Sec is a Sec-specific elongation factor, distantly related to bacterial SelB, that binds GTP, tRNASec and SBP2; this latter protein, in turn, binds the SECIS element . Sec synthesis is the other part of the metabolic pathway required for biosynthesis of selenoproteins. It takes place on tRNASec, which is first aminoacylated with serine (by a canonical seryl-tRNA synthetase) and then modified to selenocysteinyl-tRNA, in the reaction that uses selenophosphate as the selenium donor . In the Bacteria, this reaction is catalyzed by Sec synthase (SelA). The functional equivalent of SelA in Archaea and Eukarya has not been described. A phosphoseryl-tRNASec kinase (PSTK) has been recently identified only in eukaryotic and archaeal Sec-incorporating organisms . It has been suggested that this protein can play a role in Sec biosynthesis and/or regulation. The synthesis of selenophosphate is catalyzed by selenophosphate synthetase (SelD) from ATP and selenide in both prokaryotes and eukaryotes.
Selenophosphate has also been described as a precursor for the last step of the synthesis of the modified base 5-methylaminomethyl-2-selenouridine in the wobble position of the anticodons of Lys, Glu and Gln tRNAs , and this reaction was reported to be catalyzed by YbbB in Escherichia coli . The function of this modified base is not known.
Thus, considerable efforts in recent years have been made to elucidate molecular details of Sec decoding in the three domains of life. In addition, the selenoproteome of several species has been the subject of intensive research [5, 6, 14–16]. Despite this progress, fundamental issues relating to the evolution of Sec utilization remain unclear. On the basis of the complexity and similarity of the Sec-insertion mechanisms in different organisms, it has been proposed that the Sec-decoding trait arose once, before the division of the three domains of life, and was subsequently lost in some lineages. It is also thought that once an organism has lost the Sec-insertion system, it cannot re-emerge. Whether the Sec biosynthesis and insertion pathway evolved before the fixation of the genetic code or whether this was a late addition is not known [17–19].
Here we provide a map of Sec-incorporating and selenouridine-utilizing organisms within the tree of life, based on the analysis of completely sequenced genomes. From phylogenetic analysis of all components of the Sec-decoding machinery, we present clear evidence for the loss of the trait in many lineages at different taxonomic levels, and examples of acquisition of the trait by horizontal gene transfer (HGT). In addition, we describe and explain the maintenance of selenophosphate synthetase in non-Sec-incorporating organisms, and use this information to define a selenouridine-utilization trait as well as a general selenium-utilization trait. We find that the 2-selenouridine pathway can also be acquired by HGT. These data suggest that the loss of selenium utilization is not irreversible.
A map of selenium utilization within the tree of life
Despite the bias among the prokaryotic genomes so far sequenced , in which proteobacteria are over-represented and some phyla are not represented at all, the taxa distribution of Sec incorporation revealed interesting features of this trait. First, the trait is widely distributed and present in numerous bacterial phyla (Proteobacteria, Firmicutes, Spirochaetes, Actinobacteria, Aquificae). Second, we observed the presence and absence of the trait in taxa within monophyletic groups. This phenomenon takes place within clades at different evolutionary levels, namely phylum, class, order, family, genera, and even species and is illustrated in Figure 1. Considering the genus level, we observed this phenomenon within Pseudomonas, Treponema, Clostridium and Yersinia. The more revealing case of this absence/presence pattern is that of the KIM, biovar Mediaevalis and CO92 strains of Yersinia pestis. Whereas the KIM strain possesses a functional Sec-decoding machinery, the CO92 and Mediaevalis strains carry a confirmed sequenced selB pseudogene, whose coding region is disrupted by a frameshift . Furthermore, the CO92 and the Mediaevalis strains possess selA, selC and selD, indicating that the loss of the ability to decode Sec is very recent. Moreover, at position 203 of the α-subunit of formate dehydrogenase type O there is a UGA codon in the three strains, which is decoded as Sec by the KIM strain, but could not be decoded as such in the CO92 and the Mediaevalis strains. The three strains also possess formate dehydrogenase type H with a Cys-containing α-subunit (fdhH).
SelB and selC can be considered as the gene signature of organisms able to decode Sec: their presence in genomes always coincides with that of selA (excluding archaeal and eukaryote domains), selD, and selenoproteins. A putative ortholog of selA is present in Helicobacter pylori (a Sec-non-incorporating organism). The presence of this protein in the two strains of this species is intriguing and raises the question of whether this protein serves a different function or is just a remnant of the Sec-decoding machinery. The case of selD is different, because it is present in several species that lack other genes necessary for Sec decoding. SelD orthologs are indicated in red in Figure 1.
The fact that selenophosphate is also the precursor for the synthesis of 2-selenouridine , a modified base that is present at the wobble position of Lys, Glu and Gln tRNAs, suggests that selD may have been maintained in these organisms to generate selenophosphate for 2-selenouridine synthesis. Thus, we investigated the distribution of ybbB, a gene encoding the catalyst of the last step of 2-selenouridine synthesis , and its association with selD.
The analysis of selA, selB, selC, selD and ybbB genes also revealed that, within the set of species that incorporate Sec, many, but not all, organisms, possess ybbB and vice versa. In other words, the set of species that incorporate Sec into protein overlaps with, but is different from, the set of species that possess ybbB (Figure 1). It is important to note that a low-identity homolog to bacterial ybbB is present in Methanococcus jannaschii and Methanopyrus kandleri, and absent in other archaea, suggesting that this base modification might not be unique to bacteria.
Finally, we investigated the presence of additional genes linked to the selenouridine synthesis trait by searching genomes for genes that occur in organisms possessing ybbB and are absent in organisms lacking ybbB. This search did not identify any additional gene associated with this trait. Thus, the overall analysis allows us to corroborate that the two products of these genes form a pathway with 2-selenouridine in the tRNA as the final product. However, only ybbB is the gene signature of this trait. On the other hand, the dual use of selenophosphate (for Sec decoding and 2-selenouridine biosynthesis) makes selD a signature of a broader trait of selenium utilization, and our data suggest that both Sec decoding and selenouridine traits are independently maintained, but both require selD.
Phylogeny of selA, selB, selC, selD and ybbB: evidence of horizontal gene transfer (HGT) of Sec-decoding and selenouridine synthesis traits
The phylogenies of selA, selB, selC, selD and ybbB shown in Figure 2 are neither mutually coherent nor match the 'species tree' (Figure 1). This does not necessarily imply an error in the phylogenetic reconstruction since the evolutionary history of each gene could be different. Many nodes are mutually consistent across different methods and have high statistical support. Certain anomalous situations occur with distantly related organisms (deep nodes), which could be due to the limitations of these analyses. However, some of the inconsistencies may be considered as 'genuine' and raise HGT as the most likely alternative explanation.
A striking observation is the clustering of P. profundum (a γ-proteobacterium) with T. denticola (a spirochete) at a basal position of the selA, selB and selC trees. This topology is consistent in various phylogenetic reconstruction methods and has high statistical support in all cases. The congruence of the trees sustains the idea that these genes were horizontally transferred to P. profundum. Several facts provide further support for this proposition. The P. profundum genome encodes four selenoproteins: two glycine reductases A, one glycine reductase B and selenophosphate synthetase. This selenoproteome is entirely distinct from that of γ-proteobacteria and very similar to that of T. denticola, which consists of glycine reductase A, two glycine reductases B, selenophosphate synthetase, glutathione peroxidase and thioredoxin. Furthermore, glycine reductase is absent in every other proteobacterial genome. In addition, P. profundum is the single prokaryotic genome that has two selDs: one encodes a Sec-containing isoform that is located next to the selAB operon, on chromosome II; the second encodes a Cys-containing enzyme that is adjacent to ybbB on chromosome I. The phylogeny of selD places the Cys isoform within the γ-proteobacterial clade as expected according to the organismal phylogeny, whereas the Sec isoform does not cluster with T. denticola or with γ-proteobacteria. Altogether, these results indicate that it is highly unlikely that P. profundum has acquired the Sec-decoding trait by vertical descent, raising HGT as the obvious alternative. In addition, we analyzed the codon usage of selA and selB, looking for an anomalous pattern, using the method described by García-Vallvé . These genes do not display biased values of codon usage with respect to the rest of the genes. This result could indicate that P. profundum has already adapted the codon usage of these genes to its internal values. A recent paper suggested that the compatible codon usage between foreign genes and recipient genomes increases the probability of HGT . Since T. denticola and P. profundum do not share the same environment, it is likely that the HGT took place from a species of spirochete, a bacterial phylum exhibiting great variability in habitat and physiology .
An additional incongruence is observed when the selA, selB, selC and the species trees are compared among Pseudomomas spp. (γ-proteobacteria), Sinorhizobium meliloti (α-proteobacterium) and Burkholderia spp. (β-proteobacteria) (Figure 2). The evolutionary history of these genes is, however, difficult to solve.
Conflicts relating to the selenouridine synthesis trait were also observed. The consistent and statistically supported cluster between Bordetella bronchiseptica (a β-proteobacterium) and Pseudomonas spp., within the γ-proteobacteria clade in both selD and ybbB gene trees, strongly suggests an event of HGT from Pseudomonas spp. to B. bronchiseptica. A situation that cannot be explained by vertical descent is also the cluster of Nitrosomonas europae (a β-proteobacterium) and Bdellovibrio bacteriovorus (δ-proteobacteria) in selD and ybbB phylogenies (Figure 2). The location of ybbB and selD genes also supports this possibility: while arranged in an operon in N. europeae and B. bacteriovorus; they are distant in the genomes of the other δ-proteobacteria (Figure 3). Furthermore, B. bacteriovorus is a predatory bacterium with a multiplication phase within many Gram-negative bacteria . Thus, the ready access to the prey's genetic information and vice versa might be a possible explanation for this HGT event.
The distribution of the Sec-decoding trait within the 'species tree' prompts the question of how it evolved. A supported conclusion from our data is the common origin of selA, selB, selC and selD in the domain Bacteria. This is based on the absence of close paralogs for Sec-decoding genes in bacteria, the high bootstrap value for the bacterial node in all phylogenies, and the presence of bacterial sequence signatures in selA, selB, selC and selD sequences (see Additional data files). The phylogenies of selB, selC and selD also indicate that the archaeal and eukaryal Sec-decoding genes cluster together. This is further supported by the similar overall organization of the Sec-decoding machinery in Archaea and Eukarya [26–28]. The emergence of the Sec-decoding trait before the division of the three domains has been previously postulated [18, 29]. The evolution of the Sec insertion system only once is certainly the most parsimonious evolutionary scenario. However, this does not necessarily imply that every gene involved in Sec-decoding has a common origin. This is exemplified by selA: no clear ortholog has been found in Archaea and Eukarya. This suggests that the mechanism of Sec biosynthesis and insertion could have been adjusted during evolution.
Assuming the common origin of the Sec-decoding trait, it is possible to sketch a scenario compatible with our results in order to explain the pattern of presence/absence of the Sec-decoding trait. We propose that this pattern is the result of two mechanisms, primarily speciation and differential gene loss, with some contribution from HGT. Regarding the selenouridine synthesis trait, the results also suggest a common origin in the bacterial domain, as well as the possibility that 2-selenouridine pathway can be acquired by HGT.
An important issue in the evolution of Se utilization traits relates to the selective forces operating to maintain, loose or acquire the traits. Although it is not possible to draw conclusions, the search for a common biochemical, physiological or ecological trait in organisms possessing/lacking either or both traits provides interesting clues. The analysis of the prokaryotic selenoproteome revealed that formate dehydrogenase is present in most organisms capable of Sec decoding, exceptions being T. denticola, P. profundum, Clostridium perfringens and Thermoanerobacter tengcongensis . Formate dehydrogenase plays a key role in anaerobic respiration. Indeed, most of these species are obligatory anaerobes or facultative aerobes; the sole exception was S. meliloti, a symbiotic nitrogen-fixing obligatory aerobe that lives in the oxygen-limited environment of the nodule . Formate dehydrogenase is the single Sec-containing polypeptide encoded in the Sinorhizobium meliloti genome [6, 30], suggesting that the presence of the trait may be important for respiration under conditions of restricted oxygen supply. On the other hand, glycine reductase is present in T. denticola, P. profundum and T. tengcongensis and several species of the genera Clostridium except C. perfringens. Glycine reductase is an enzymatic complex that allows certain anaerobic bacteria to conserve energy via a soluble substrate level phosphorylation system . Sec is more reactive than Cys by virtue of the lower pKa and higher nucleophilicity of selenol group compared to that of the thiol group , and can increase the pH range at which certain enzymes are active . This might have conferred a selective advantage improving catalytic efficiency of proteins.
Regarding selective forces operating on the evolution of the selenouridine synthesis trait, we begin from the fact that synthesis of 2-selenouridine is carried out exclusively at the wobble position (first of the anticodon) of the tRNAs for lysine, glutamate and glutamine (the only amino acids encoded by twofold purine-ending codons). Several modifications of this base have been reported to be essential for correct decoding; thiouridine, in particular, would convert the base into an ionized form that would favor pairing with A and G, and avoid pairing with U or C, contributing to the discrimination of twofold codons ending in purine from those ending in pyrimidine . The low pKa value of 2-selenouridine of these tRNAs would be consistent with this argument and it has been suggested that this would also favor base-pairing with G . Thus, we postulate that selenium modification of tRNAs matching twofold codons might be a refinement in the base discrimination at the wobble position. The interaction of the first base of the anticodon with the third base of the codon plays an important role in the efficiency and accuracy of the translation process, suggesting that this base modification could be linked to certain aspects of codon usage. In any case, it should be stressed that ybbB null E. coli has no apparent phenotypic differences to wild type-E. coli and does not alter nonsense suppression phenotype .
One of the driving forces for the loss of the traits probably relates to the variability of selenium abundance in the environment. The absolute dependence of organisms on Se can compromise their existence if dietary Se becomes limiting. In these situations, enzymes containing Sec as catalytic residues could have evolved into Cys-containing proteins or, alternatively, both Sec-containing and Cys-containing forms could be maintained. This latter case is exemplified by the genome of M. maripaludis, which encodes several Sec-containing proteins and also homologs that contain cysteine in place of Sec. In a medium that contains adequate amounts of selenium, this organism represses the synthesis of the cysteine homologs, but this repression is not observed in a mutant with disrupted selB , suggesting that the cysteine homologs are a backup system in case of selenium scarcity. Nevertheless, the existence of organisms carrying only one of the selenium-utilization traits suggests that selenium availability might not be the sole factor involved in the loss of either trait. It is also possible that the higher reactivity of selenium over sulfur in biological molecules might have had a role in counterselecting the pervasive use of Sec and/or selenouridine in living systems.
This paper provides an organismal map for Sec-decoding and 2-selenouridine synthesis traits within the tree of life, and defines selB and selC as the gene signature of the Sec-decoding trait, ybbB as the gene signature of selenouridine synthesis, with selD defining overall selenium utilization. We show that the set of species that incorporate Sec overlaps with, yet is distinct from, the set of species that synthesize 2-selenouridine, and our data suggest that Sec decoding and 2-selenouridine traits can be independently maintained, and both require selD.
Analysis of the phylogenies of the Sec-decoding and 2-selenouridine synthesis genes provides evidence for the ancient origin of these traits and demonstrates that their evolution is a highly dynamic process that occurs at different evolutionary levels, namely phylum, class, order, family, genera, and even species. We show that this process can be explained as the result of speciation and differential gene loss, and provide conclusive evidence that the loss of these traits is not irreversible as previously thought, and that entire sets of genes can be acquired by HGT. It is striking that the genetic code of an organism and the amino-acid repertoire can be 'laterally' expanded.
The study of selenium-utilization traits, which directly associate protein synthesis with a discrete set of genes, can contribute to the understanding of basic questions regarding the evolution of the genetic code and the translation machinery.
Materials and methods
Sequences of selA, selB, selC, selD and ybbB
Complete genome sequences of 194 prokaryotes were retrieved from GenBank  as of 20 October 2004, representing 151 species.
Annotated sequences corresponding to selA, selB, selD and ybbB prokaryotic genes were retrieved from GenBank, and used as queries to perform local BLAST searches across a database generated with the 194 genomes. For selA, selD and ybbB, hits with an e-value below e-15 were recovered; for selB, the cutoff e-value was e-30 to decrease the number of hits corresponding to other translation factors. A total of 242 selB, 48 selA, 47 selD and 25 ybbB sequences were recovered. The sequences were aligned using ClustalW , a raw phylogenetic analysis was conducted and clear nonorthologous sequences were discarded. This dataset was manually curated, and the number of sequences was reduced to 29 selA, 32 selB, 41 selD, and 21 ybbB sequences. These datasets were used as queries for BLAST searches but no new sequences were identified. Finally, only one sequence by strain was included and the set was supplemented with sequences of three representative eukaryotes (Caenorhabditis elegans, Drosophila melanogaster and Homo sapiens).
Most sequences of selC were retrieved from GenBank or identified using tRNAscan software with default parameters [38, 39]. The sequences of Wolinella succinogenes, Helicobacter hepaticus, Burkholderia mallei and Thermoanaerobacter tencongensis, were found changing the parameters to 'Cove-only search mode' and lowering the tRNA Cove cutoff score to 6.
All sequences are provided aligned in the Additional data files.
Alignments and phylogenetic reconstruction of gene trees
Several phylogenetic gene trees were built using different inference methods performed on different sequence alignments. Sequences were aligned with T-coffee version 1.37 , ClustalW 1.8 and Dialign-2  using different parameters. The 'score' option of the T-coffee software was enabled to assess alignment quality. The alignments were then visually inspected, compared and uncertain sites were removed. In another approach, we applied the g-blocks software  to remove unstable blocks with 2 different sets of parameters. The final alignment sets were the following: i) raw alignments using each software with two different sets of parameters ii) 'sub-alignments' obtained removing the unstable blocks from the raw alignments using g-blocks software, and iii) 'sub-alignment' obtained using the '-score' option of T-coffee for evaluation of the alignment, then the low scoring regions were removed manually.
For each of these alignments, we applied several phylogenetic reconstruction methods including Neighbor Joining using MEGA software , Maximum Likelihood (ML) using phyML 2.4 software  and Bayesian approaches using MrBayes 3.0b4 . For each of these methods, different transition matrices (WAG and JTT) and evolutionary models were tested. In total, more than 80 trees were analyzed for each gene. The gene trees presented in Figure 2 were built using the T-coffee alignment evaluated with the '-score' option and manually refined. The ML and Bayesian trees were built using WAG matrix and gamma+invar model of evolutionary change. In the ML method, the assessment of node reliability was done using 100 bootstrap replicates. In the case of Bayesian analyses, four heated Markov chains were started from random trees and run for 1,000,000 generations each. Chains were sampled every 500 generations to assure independence. Sample points prior to reach stationary (200) were discarded as 'burn-in'.
Almost all trees yielded similar topologies and, more important, all of them supported the conclusions. In particular, the HGT results were reproduced with any of the alignments and phylogenetic trees.
Different species trees were initially constructed, based on small-subunit (SSU) rRNA, EF-Tu/EF-1α (a highly conserved translation elongation factor present in all organisms), and a concatenated set of 9 ortholog sequences present in all prokaryotes. A set of aligned SSU-rRNA sequences was retrieved from the Ribosomal Database Project (RDP) , release 2.1, missing sequences were retrieved from Genbank and aligned against the set from the RDP using the profile option of ClustalW.
EF-Tu and EF-1α were recovered using a similar approach to that described for selA, selB, selD and ybbB, and aligned using T-coffee. An all-against-all BLAST search was performed sequentially and best reciprocal hits were identified as putative orthologs. A set of nine genes was obtained. These sequences were aligned with ClustalW and concatenated. In all cases we used the neighbor-joining (NJ) algorithm to build the trees from different distance matrices using MEGA software . In the case of SSU-rRNA, the Tamura-Nei (TN93) distance with pairwise-deletion was calculated. For the amino-acid alignments we use the JTT transition matrix.
The different 'species trees' display some discrepancies. In any case, the conclusions drawn are maintained with any of the above mentioned 'species tree'. The SSU-rRNA was finally adopted because it is by large the commonest used, and trees inferred for this gene are sound descriptors of the general evolutionary history of prokaryotes. This tree also recovers the major groups described in Bergey's Manual .
Codon bias analyses
Codon bias was evaluated according to the method described in . This method uses the Mahalanobis distance measure for detecting outliers in a multivariate distribution.
Search for additional genes linked to Se-U trait
To study the possible association of a certain gene with ybbB we run an all-against-all BLAST search with an e-value threshold of e-10 among organisms carrying ybbB, to pick up homologs present in all these genomes. Then we used this set of genes to run a new BLAST search against a control set of closely related species lacking a ybbB homolog. This search detected no gene. When we excluded Sec-decoding species from the control set, we were able to recover a single gene: selD.
Additional data files
Additional data are available with the online version of this paper. Additional data file 1 is a table containing the gene locations of selA, selB, selC selD and ybbB in the genomes analyzed in this work. Additional data file 2 contains the sequence alignments of selA, selB, selC selD and ybbB of the genomes analyzed in this work.
This work was supported by Fogarty International Research Collaboration Award TW006959 and NIH GM061603 grant to V.N.G. We thank Dr Alexey Lobanov for help in identifying tRNASec sequences and Héctor Musto (Universidad de la República, Uruguay) for critical reading of the manuscript. We also thank the faculty, teaching assistants and students of the 'Workshop on Molecular Evolution' 2004 at the Marine Biological Laboratory, Woodshole, attended by HR, for valuable general discussion.
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