Mapping evolution with ribosome structure: intralineage constancy and interlineage variation (original) (raw)
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Molecular Phylogenetics and Evolution, 2004
Amino acid sequence alignments of orthologous ribosomal proteins found in Bacteria, Archaea, and Eukaryota display, relative to one another, an unusual segment or block structure, with major evolutionary implications. Within each of the prokaryotic phylodomains the sequences exhibit substantial similarity, but cross-domain alignments break up into (a) universal blocks (conserved in both phylodomains), (b) bacterial blocks (unalignable with any archaeal counterparts), and (c) archaeal blocks (unalignable with any bacterial counterparts). Sequences of those eukaryotic cytoplasmic riboproteins that have orthologs in both Bacteria and Archaea, exclusively match the archaeal block structure. The distinct blocks do not correlate consistently with any identifiable functional or structural feature including RNA and protein contacts. This phylodomain-specific block pattern also exists in a number of other proteins associated with protein synthesis, but not among enzymes of intermediary metabolism. While the universal blocks imply that modern Bacteria and Archaea (as defined by their translational machinery) clearly have had a common ancestor, the phylodomain-specific blocks imply that these two groups derive from single, phylodomain-specific types that came into existence at some point long after that common ancestor. The simplest explanation for this pattern would be a major evolutionary bottleneck, or other scenario that drastically limited the progenitors of modern prokaryotic diversity at a time considerably after the evolution of a fully functional translation apparatus. The vast range of habitats and metabolisms that prokaryotes occupy today would thus reflect divergent evolution after such a restricting event. Interestingly, phylogenetic analysis places the origin of eukaryotes at about the same time and shows a closer relationship of the eukaryotic ribosome-associated proteins to crenarchaeal rather than euryarchaeal counterparts.
Molecular signatures of ribosomal evolution
Proceedings of the National Academy of Sciences, 2008
Ribosomal signatures, idiosyncrasies in the ribosomal RNA (rRNA) and/or proteins, are characteristic of the individual domains of life. As such, insight into the early evolution of the domains can be gained from a comparative analysis of their respective signatures in the translational apparatus. In this work, we identify signatures in both the sequence and structure of the rRNA and analyze their contributions to the universal phylogenetic tree using both sequence-and structure-based methods. Domain-specific ribosomal proteins can be considered signatures in their own right. Although it is commonly assumed that they developed after the universal ribosomal proteins, we present evidence that at least one may have been present before the divergence of the organismal lineages. We find correlations between the rRNA signatures and signatures in the ribosomal proteins showing that the rRNA signatures coevolved with both domain-specific and universal ribosomal proteins. Finally, we show that the genomic organization of the universal ribosomal components contains these signatures as well. From these studies, we propose the ribosomal signatures are remnants of an evolutionary-phase transition that occurred as the cell lineages began to coalesce and so should be reflected in corresponding signatures throughout the fabric of the cell and its genome.
Evolution of eukaryotes as deduced from small ribosomal subunit RNA sequences
Biochemical Systematics and Ecology, 1993
Evolutionary trees based on small ribosomal subunit RNA sequences yield a new perspective on eukaryote evolution. In agreement with classical views regarding evolution, animals, green plants, and fungi form monophyletic groups which seem to have originated nearly simultaneously. The evolution of these organisms took place in a relatively short time interval and is characterized by a massive diversification of life forms. In contrast, the dissimilarity among protoctist small ribosomal subunit RNA sequences is huge and exceeds the diversity seen in the entire prokaryotic world. Furthermore, some Protoctista branch off very soon in eukaryote evolution, while others diverge much later. Based on these ribosomal RNA data, Protoctista should be regarded as a collection of independent evolutionary lineages. Because the evolutionary distance between the different groups of Protoctista is, in several cases, larger than the evolutionary distance between plants, fungi and animals, the classification of eukaryotes into four kingdoms seems to be artificial and may not reflect true evolutionary relationships.
Promiscuous behaviour of archaeal ribosomal proteins: Implications for eukaryotic ribosome evolution
Nucleic Acids Research, 2013
In all living cells, protein synthesis occurs on ribonucleoprotein particles called ribosomes. Molecular models have been reported for complete bacterial 70S and eukaryotic 80S ribosomes; however, only molecular models of large 50S subunits have been reported for archaea. Here, we present a complete molecular model for the Pyrococcus furiosus 70S ribosome based on a 6.6 Å cryo-electron microscopy map. Moreover, we have determined cryo-electron microscopy reconstructions of the Euryarchaeota Methanococcus igneus and Thermococcus kodakaraensis 70S ribosomes and Crenarchaeota Staphylothermus marinus 50S subunit. Examination of these structures reveals a surprising promiscuous behavior of archaeal ribosomal proteins: We observe intersubunit promiscuity of S24e and L8e (L7ae), the latter binding to the head of the small subunit, analogous to S12e in eukaryotes. Moreover, L8e and L14e exhibit intrasubunit promiscuity, being present in two copies per archaeal 50S subunit, with the additional binding site of L14e analogous to the related eukaryotic r-protein L27e. Collectively, these findings suggest insights into the evolution of eukaryotic ribosomal proteins through increased copy number and binding site promiscuity.
The origin and evolution of the ribosome
Biology Direct, 2008
The origin and early evolution of the active site of the ribosome can be elucidated through an analysis of the ribosomal proteins' taxonomic block structures and their RNA interactions. Comparison between the two subunits, exploiting the detailed three-dimensional structures of the bacterial and archaeal ribosomes, is especially informative.
Ribosomal proteins: Toward a next generation standard for prokaryotic systematics?
Molecular Phylogenetics and Evolution, 2014
The seminal work of Carl Woese and co-workers has contributed to promote the RNA component of the small subunit of the ribosome (SSU rRNA) as a ''gold standard'' of modern prokaryotic taxonomy and systematics, and an essential tool to explore microbial diversity. Yet, this marker has a limited resolving power, especially at deep phylogenetic depth and can lead to strongly biased trees. The ever-larger number of available complete genomes now calls for a novel standard dataset of robust protein markers that may complement SSU rRNA. In this respect, concatenation of ribosomal proteins (r-proteins) is being growingly used to reconstruct large-scale prokaryotic phylogenies, but their suitability for systematic and/or taxonomic purposes has not been specifically addressed. Using Proteobacteria as a case study, we show that amino acid and nucleic acid r-protein sequences contain a reliable phylogenetic signal at a wide range of taxonomic depths, which has not been totally blurred by mutational saturation or horizontal gene transfer. The use of accurate evolutionary models and reconstruction methods allows overcoming most tree reconstruction artefacts resulting from compositional biases and/or fast evolutionary rates. The inferred phylogenies allow clarifying the relationships among most proteobacterial orders and families, along with the position of several unclassified lineages, suggesting some possible revisions of the current classification. In addition, we investigate the root of the Proteobacteria by considering the time-variation of nucleic acid composition of r-protein sequences and the information carried by horizontal gene transfers, two approaches that do not require the use of an outgroup and limit tree reconstruction artefacts. Altogether, our analyses indicate that r-proteins may represent a promising standard for prokaryotic taxonomy and systematics.
Nucleic Acids Research, 2002
A comprehensive investigation of ribosomal genes in complete genomes from 66 different species allows us to address the distribution of r-proteins between and within the three primary domains. Thirty-four r-protein families are represented in all domains but 33 families are speci®c to Archaea and Eucarya, providing evidence for specialisation at an early stage of evolution between the bacterial lineage and the lineage leading to Archaea and Eukaryotes. With only one speci®c r-protein, the archaeal ribosome appears to be a small-scale model of the eukaryotic one in terms of protein composition. However, the mechanism of evolution of the protein component of the ribosome appears dramatically different in Archaea. In Bacteria and Eucarya, a restricted number of ribosomal genes can be lost with a bias toward losses in intracellular pathogens. In Archaea, losses implicate 15% of the ribosomal genes revealing an unexpected plasticity of the translation apparatus and the pattern of gene losses indicates a progressive elimination of ribosomal genes in the course of archaeal evolution. This ®rst documented case of reductive evolution at the domain scale provides a new framework for discussing the shape of the universal tree of life and the selective forces directing the evolution of prokaryotes.
Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology - COMP BIOCHEM PHYSIOL B BIOCHEM MOL BIOL, 1982
The molecular weights and the integrity of the principal rRNA species derived from the large and the small ribosomal subunit (respectively, L-rRNA and S-rRNA) of several species of Protostomia and Protozoa have been investigated. 2. Using gel electrophoresis in formamide, the molecular weights of protostomian L-rRNA species have been found to range from 1.30 × 10 6 (Annelida) to 1.61 x 10 6 (Diptera); those of the S-rRNA's cover the range 0.65 × 10 6 (Annelida~0.81 x 10 6 (Diptera). 3. Both rRNA components have incurred extensive changes among the Protozoa; the L-rRNA ranges in weight from 1.35 x 106 (T. pyriformis) to 1.57 x 10 6 (A. castellanii) and the S-rRNA from 0.70 x 10 6 of T. pyriformis to 0.85 x 106 of A. eastellanii and E. 9racilis. 4. The L-rRNA components of all the species investigated are discontinuous molecules endowed with a latent median break; depending on whether the nick is located at the centre of the L-rRNA chain, or lies off-centre, the molecular weight of the S-rRNA equals that of either both, or only one, of the two fragments composing the L-rRNA.