The archaeal origins of the eukaryotic translational system

Abstract

Among the 78 eukaryotic ribosomal proteins, eleven are specific to Eukarya, 33 are common only to Archaea and Eukarya and 34 are homologous (at least in part) to those of both Bacteria and Archaea. Several other translational proteins are common only to Eukarya and Archaea (e.g., IF2a, SRP19, etc.), whereas others are shared by the three phyla (e.g., EFTu/EF1A and SRP54). Although this and other analyses strongly support an archaeal origin for a substantial fraction of the eukaryotic translational machinery, especially the ribosomal proteins, there have been numerous unique and ubiquitous additions to the eukaryotic translational system besides the 11 unique eukaryotic ribosomal proteins. These include peptide additions to most of the 67 archaeal homolog proteins, rRNA insertions, the 5.8S RNA and the Alu extension to the SRP RNA. Our comparative analysis of these and other eukaryotic features among the three different cellular phylodomains supports the idea that an archaeal translational system was most likely incorporated by means of endosymbiosis into a host cell that was neither bacterial nor archaeal in any modern sense. Phylogenetic analyses provide support for the timing of this acquisition coinciding with an ancient bottleneck in prokaryotic diversity.

Figure 1.

A schematic representation of the multiple alignments of the 33 ribosomal proteins common to Archaea and Eukarya. Purple marks segments alignable, and thus homologous, across both phylogenetic domains; blue marks segments unique and alignable only within Eukarya; red marks segments alignable only within Archaea. Dotted lines represent sequence regions of varying length that are unalignable across the full sets of either Eukarya or Archaea. The representative species are listed in the legend of Figure 4.

Figure 2.

A schematic representation of the multiple alignments of the archaeal and eukaryotic species for the 34 universal ribosomal proteins. Purple marks segments alignable, and thus homologous, across both the eukaryal and archaeal phylogenetic domains; blue marks segments unique and alignable only among Eukarya; red marks segments alignable only among Archaea. Dotted lines represent sequence regions of varying length that are unalignable across the full sets of either Eukarya or Archaea. The representative species are listed in the legend of Figure 4. Ribosomal protein L7ae has been identified in some, but not all, major representative Bacteria, and is therefore neither universal nor eukaryotic-archaeal specific.

Figure 3.

A schematic representation of the multiple alignments of the 34 universal ribosomal proteins common to Eukarya, Archaea and Bacteria. Orange marks segments alignable, and thus homologous, across all three phylogenetic domains; purple marks blocks alignable across Eukarya and Archaea; blue marks those blocks alignable only with in the Eukarya; red marks those blocks alignable only within the Archaea; dark green marks blocks alignable only across Archaea and Bacteria, while light green marks those alignable only within the Bacteria. The dotted lines represent sequence regions of varying length unalignable across the full sets of any of the three groups. The representative species are listed in the legend of Figure 4. Ribosomal protein L7ae has been identified in some, but not all, major representative Bacteria.

Figure 4.

Maximum-likelihood unrooted trees constructed from the positional variation among aligned sets of ribosomal proteins. (a) Tree constructed from the concatenated set of alignment blocks common in the 34 universal ribosomal proteins from the three phylodomains: Bacteria, Archaea and Eukarya, labeled by orange bars in Figure 3. (b) Tree constructed from the concatenated set of alignment blocks common to both the eukaryotic and archaeal representatives and labeled by purple bars in Figures 1 and 2. The trees were constructed by the maximum likelihood approach with the TREE-PUZZLE procedure, Quartet Puzzling, 1000 steps and the JTT model of substitution. Abbreviations are Swiss-Prot codes: Eukarya (top set): ARATH = Arabidopsis thaliana, CAEEL = Caenorhabditis elegans, DROME = Drosophila melanogaster, GUITH = Guillardia theta, HUMAN = Homo sapiens, ICTPU = Ictalurus punctatus, ORYSA = Oryza sativa, SCHPO = Schizosaccharomyces pombe, TETHY = Tetrahymena thermophila and YEAST = Saccharomyces cerevisiae; Archaea (middle set): AERPE = Aeropyrum pernix, ARCFU = Archaeoglobus fulgidus, HALMA = Haloarcula marismortui, METJA = Methanococcus jannischii, METKA = Methanopyrus kandleri, METTH = Methanobacterium thermoautotrophicum, NANEQ = Nanoarchaeum equitans, PYRAB = Pyrococcus abyssi, PYRAE = Pyrobaculum aerophilum, SULSO = Sulfolobolus solfataricus and THEAC = Thermoplasma acidophilum; Bacteria (bottom set): AQUAE = Aquifex aeolicus, BACSU = Bacillus subtilis, CAUCR = Caulobacter crescentus, CHLTR = Chlamydia trachomatis, CHLTE = Chlorobium tepidum, ECOLI = Escherichia coli, HELPY = Helicobacter pylori, STRCO = Streptomyces coelicolor, SYNY3 = Synechocystis sp. (strain PCC 6803), THEMA = Thermotoga maritima and TREPA = Treponema pallidum.