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Comparative analysis of ribosomal proteins in complete genomes: ribosome “striptease” in Archaea

BlastP Hit between RL40_METJA (Query) and RL40_HUMAN >SW:RL40_HUMAN P14793 60S RIBOSOMAL PROTEIN L40 (CEP52). 10/2001 Length = 52 Score = 31.6 bits (70), Expect = 1.8 Identities = 18/34 (52%), Positives = 20/34 (57%), Gaps = 3/34 (8%)

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Comparative analysis of ribosomal proteins in complete genomes: ribosome “striptease” in Archaea

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BlastP Hit between RL40_METJA (Query) and RL40_HUMAN >SW:RL40_HUMAN P14793 60S RIBOSOMAL PROTEIN L40 (CEP52). 10/2001 Length = 52 Score = 31.6 bits (70), Expect = 1.8 Identities = 18/34 (52%), Positives = 20/34 (57%), Gaps = 3/34 (8%) Query: 13 KKICMRCNARNPWRATKCR--KCGY-KGLRPKAK 43 K IC +C AR RA CR KCG+ LRPK K Sbjct: 17 KMICRKCYARLHPRAVNCRKKKCGHTNNLRPKKK 50 100% of the family representatives in both blastp and tblastn >50% of the family representatives in blastp <50% of the family representatives in blastp 0% of the family representatives in both blastp and tblastn 0% of the family representatives in blastp but detected by tblastn (gene missed during annotation process) Comparative analysis of ribosomal proteins in complete genomes: ribosome “striptease” in Archaea Odile Lecompte, Raymond Ripp, Jean-Claude Thierry, Dino Moras and Olivier Poch Laboratoire de Biologie et Génomique Structurales, Institut de Génétique et de Biologie Moléculaire et Cellulaire (CNRS, INSERM, ULP), BP163, 67404 Illkirch Cedex, France Ribosomal gene detection : cross-validation needed ! Abstract 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. 34 r-protein families are represented in all domains but 33 families are specific 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 specific r-protein, the archaeal ribosome appears to be a small-scale model of the eukaryotic one in term 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 first 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. An initial set of ribosomal proteins classified into 102 families was obtained at http://www.expasy.ch/cgi-bin/lists?ribosomp.txt. For each family, representatives of various lineages across Bacteria, Archaea and Eucarya were used as probes and systematically compared to a non-redundant protein database consisting of SwissProt, SpTrEMBL and SpTrEMBLNEW using the BlastP program (1) with a cut-off of E<0.001. The results of the BlastP comparison were cross-validated by a TBlastN search against a complete genome database including 66 different species. The putative new gene sequences detected by the TBlastN searches were examined in the light of their genomic context to eliminate false-positives “hits”. For each r-protein family, the likely r-protein sequences obtained by the BlastP and TBlastN searches were included in a multiple alignment constructed by MAFFT (2). All alignments were refined by RASCAL (3) and their quality assessed by NorMD (4). These alignments were manually examined to remove false-positives observed in some ribosomal protein families, in particular those containing ubiquitous RNA-binding domains. Small size and biased composition of r-proteins Genes often missed during annotation process Difficulty of protein detection by similarity search Protocol of ribosomal gene detection R-protein families Complete genomes 102 r-protein families Genomic context analysis 45 Bacteria Multiple alignment of complete sequences 14 Archaea 7 Eucarya Creation of 24 missed genes • Coherence of the protein family • Elimination of false-positives • Correction of protein sequences All the alignments are available at http://www-igbmc.u-strasbg.fr/BioInfo/Rproteins Protein detected by : Validation of protein sequences for each family A complex Last Universal Common Ancestor ? Interdomain distribution Ribosomal protein losses in each of the three domains • Prevalence of r-proteins within the universal pool that may be present in the last universal common ancestor (LUCA) • specialization of bacterial versus archaeal/eukaryotic ribosomes • the majority of archeal and eucaryotic r-proteins appears before the split between Archaea and Eucarya, suggesting a complex cenancestor Full circles indicate proteins absent in all complete genomes investigated in the indicated taxon. Empty circles stand for proteins absent in some complete genomes of the indicated taxon Localisation in the 3D structures Bacteria-specific proteins (colored in different shades of red) are preferentially located at the periphery of the ribosome Progressive elimination of 10 r-proteins (15%) in the course of archaeal evolution First example of reductive evolution at domain-scale Lecompte et al. Nucleic Acids Research (2002) ? the 30S ribosomal subunit of Thermus thermophilus (5) (back side) Reductive evolution as a general trend in Archaea ? In Procaryotes ? A complex Last Universal Common Ancestor (LUCA) ? Which evolutionary scenario ? References: 1 Altschul,S.F., Madden,T.L., Schaffer,A.A., Zhang,J., Zhang,Z., Miller,W. and Lipman,D.J. (1997) Nucleic Acids Res., 25, 3389-3402. 2 Katoh,K., Misawa,K., Kuma,K. and Miyata,T. (2002) Nucleic Acids Res., 30, 3059-3066. 3 Thompson,J.D., Thierry,J.C., Poch,O. (2003) Bioinformatics, 19, 1155-61.   4 Thompson,J.D., Plewniak,F., Ripp,R., Thierry,J.C. and Poch,O. (2001) J. Mol. Biol., 314, 937-951. 5 Wimberly,B.T., Brodersen,D.E., Clemons,W.M., Jr., Morgan-Warren,R.J., Carter,A.P., Vonrhein,C., Hartsch,T. and Ramakrishnan,V. (2000) Nature, 407, 327-339. 6 Harms,J., Schluenzen,F., Zarivach,R., Bashan,A., Gat,S., Agmon,I., Bartels,H., Franceschi,F. and Yonath,A. (2001) Cell, 107, 679-688. the 50S ribosomal subunit of Deinococcus radodurans (6) (crown view rotated by 180°)

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