Evolutionary dynamics of eukaryotic selenoproteomes: large selenoproteomes may associate with aquatic life and small with terrestrial life

Abstract

Background: Selenocysteine (Sec) is a selenium-containing amino acid that is co-translationally inserted into nascent polypeptides by recoding UGA codons. Selenoproteins occur in both eukaryotes and prokaryotes, but the selenoprotein content of organisms (selenoproteome) is highly variable and some organisms do not utilize Sec at all.

Results: We analyzed the selenoproteomes of several model eukaryotes and detected 26 and 29 selenoprotein genes in the green algae Ostreococcus tauri and Ostreococcus lucimarinus, respectively, five in the social amoebae Dictyostelium discoideum, three in the fly Drosophila pseudoobscura, and 16 in the diatom Thalassiosira pseudonana, including several new selenoproteins. Distinct selenoprotein patterns were verified by metabolic labeling of O. tauri and D. discoideum with 75Se. More than half of the selenoprotein families were shared by unicellular eukaryotes and mammals, consistent with their ancient origin. Further analyses identified massive, independent selenoprotein losses in land plants, fungi, nematodes, insects and some protists. Comparative analyses of selenoprotein-rich and -deficient organisms revealed that aquatic organisms generally have large selenoproteomes, whereas several groups of terrestrial organisms reduced their selenoproteomes through loss of selenoprotein genes and replacement of Sec with cysteine.

Conclusion: Our data suggest many selenoproteins originated at the base of the eukaryotic domain and show that the environment plays an important role in selenoproteome evolution. In particular, aquatic organisms apparently retained and sometimes expanded their selenoproteomes, whereas the selenoproteomes of some terrestrial organisms were reduced or completely lost. These findings suggest a hypothesis that, with the exception of vertebrates, aquatic life supports selenium utilization, whereas terrestrial habitats lead to reduced use of this trace element due to an unknown environmental factor.

Figure 1

Ostreococcus SECIS elements. (a) The most characteristic features of O. tauri and O. lucimarinus SECIS elements are a long mini-stem and an unpaired G preceding the SECIS quartet (core). A SelT SECIS element is shown as a typical example (left structure). Only two exceptions were found, including a type I SECIS element in SelH (middle structure) and a SECIS element with an unpaired A nucleotide preceding the SECIS core (right structure). (b) Alignment of nucleotide sequences of all O. tauri SECIS elements. Location of the SECIS core is indicated. Conserved nucleotides are highlighted. Black and grey highlighting shows sequence conservation.

Figure 2

Metabolic labeling of O. tauri and D. discoideum with ⁷⁵Se. O. tauri and D. discoideum cells were grown in the presence of ⁷⁵Se [selenite], cell lysates prepared, proteins resolved by SDS-PAGE and analyzed using a PhosphorImager. (a) O. tauri. Three middle lanes represent the soluble fraction, homogenate and pellet fraction as shown above the gel. For comparison, HEK 293 cells were metabolically labeled with ⁷⁵Se, and migrations of thioredoxin reductase 1 (TR1) and glutathione peroxidase 1 (GPx1) are shown. (b) D. discoideum. Two middle lanes represent two independent samples of ⁷⁵Se-labeled D. discoideum cells. The four radioactive bands correspond to the indicated selenoproteins identified in silico. For comparison, monkey CV-1 cells were metabolically labeled with ⁷⁵Se, and migrations of TR1 and GPx1 are shown on the right.

Figure 3

Sec tRNA. (a) Cloverleaf structures of Sec tRNAs from C. reinhardtii, O. tauri and C. merolae. (b) Nucleotide sequence alignment of C. reinhardtii and C. merolae Sec tRNAs with known Sec tRNAs. Black and grey highlighting shows sequence conservation.

Figure 4

Red algae selenoprotein O. SECIS elements in O. tauri (green alga) and P. haitanensis (red alga) SelO genes. The P. haitanensis SECIS element belongs to type I, while O. tauri to type II structures.

Figure 5

Dictyostelium discoideum SECIS elements. (a) SECIS elements in D. discoideum selenoprotein genes. Sequences conserved in eukaryotic SECIS elements are shown in red, and Dictyostelium-specific conserved sequences are shown in blue. (b) Alignment of D. discoideum SECIS elements. A UGUA sequence preceding the SECIS core, and a U-U mismatch in the stem-loop structure represent additional conserved features in Dictyostelium SECIS elements. Black and grey highlighting shows sequence conservation.

Figure 6

Eukaryotic selenoproteomes. (a) A simplified cladogram of model organisms discussed in the text that illustrates distribution of selenoproteins in eukaryotes. The number of selenoproteins in each indicated model organism is shown in red (current study) and gray (previously analyzed and other model organisms) squares, and is proportional to the size of the bars on the left. Yellow circles show possible origins of various selenoprotein families, and red crosses examples of massive selenoprotein loss. (b) Selenoprotein evolution in plants. The 'mountain' symbols show terrestrial organisms, and 'anchors' those that live in aquatic environments. Green checkmarks indicate the presence of an indicated selenoprotein in the corresponding genome. The presence of Cys-containing homologs is shown by blue checkmarks. Crossed red circles indicate absence of either Sec- or Cys-containing homologs. Unfilled spots correspond to lack of data due to unfinished genomes, unclear relationship between proteins and lineage specific gene duplications.

Figure 7

Aquatic invertebrates have more selenoproteins than terrestrial organisms. Numbers of detected selenoproteins were plotted against the total number of available (redundant) ESTs for organisms that are represented by more than 25,000 ESTs. Vertebrate ESTs were excluded from this analysis due to large size of these organisms. Blue circles correspond to aquatic and brown squares to terrestrial organisms. The difference is statistically significant (P value is less than 2 × 10^-6).