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PMID: 12490706 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Comparative analysis of ribosomal proteins in complete genomes: an example of reductive evolution at the domain scale.

Nucleic acids research ·Vol. 30 ·No. 24 ·2002-12-15 ·Pages 5382-90

Lecompte O, Ripp R, Thierry JC, Moras D, Poch O

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. Thirty-four 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 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 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.

MeSH Terms
Animals Archaea/genetics Bacteria/genetics Binding Sites/genetics Databases, Protein Eukaryotic Cells/metabolism Evolution, Molecular Genome Humans Models, Molecular Phylogeny Protein Binding RNA, Ribosomal/chemistry,metabolism Ribosomal Proteins/chemistry,genetics,metabolism Ribosomes/chemistry,metabolism
Chemicals
RNA, Ribosomal Ribosomal Proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Lecompte Odile
Laboratoire de Biologie et Génomique Structurales, Institut de Génétique et de Biologie Moléculaire et Cellulaire (CNRS, INSERM, ULP), BP163, 67404 Illkirch Cedex, France.
Ripp Raymond
Thierry Jean-Claude
Moras Dino
Poch Olivier
References (77)
77 references, click to expand
  1. Photolabeling of protein components in the pactamycin binding site of rat liver ribosomes.
    Biochim Biophys Acta. 1986 Dec 18;868(4):249-53 PMID: 3790569
  2. Comparative genomics of the Archaea (Euryarchaeota): evolution of conserved protein families, the stable core, and the variable shell.
    Genome Res. 1999 Jul;9(7):608-28 PMID: 10413400
  3. Genome alignment, evolution of prokaryotic genome organization, and prediction of gene function using genomic context.
    Genome Res. 2001 Mar;11(3):356-72 PMID: 11230160
  4. Conservation of gene order: a fingerprint of proteins that physically interact.
    Trends Biochem Sci. 1998 Sep;23(9):324-8 PMID: 9787636
  5. Native 3D structure of eukaryotic 80s ribosome: morphological homology with E. coli 70S ribosome.
    J Cell Biol. 1996 May;133(3):495-505 PMID: 8636226
  6. Evidence that eukaryotes and eocyte prokaryotes are immediate relatives.
    Science. 1992 Jul 3;257(5066):74-6 PMID: 1621096
  7. Affinity labelling of rat liver ribosomal protein S26 by heptauridylate containing a 5'-terminal alkylating group.
    Mol Biol Rep. 1984 Jan;9(4):219-22 PMID: 6708946
  8. Microsporidian Encephalitozoon cuniculi, a unicellular eukaryote with an unusual chromosomal dispersion of ribosomal genes and a LSU rRNA reduced to the universal core.
    Nucleic Acids Res. 1998 Aug 1;26(15):3513-20 PMID: 9671812
  9. Evolution of organelles and eukaryotic genomes.
    Science. 1975 May 30;188(4191):891-8 PMID: 1138359
  10. Multiple functions of an evolutionarily conserved RNA binding domain.
    Mol Cell. 2000 Apr;5(4):761-6 PMID: 10882112
  11. Comprehensive comparison of structural characteristics in eukaryotic cytoplasmic large subunit (23 S-like) ribosomal RNA.
    J Mol Biol. 1996 Mar 8;256(4):701-19 PMID: 8642592
  12. Structure and evolution of the L11, L1, L10, and L12 equivalent ribosomal proteins in eubacteria, archaebacteria, and eucaryotes.
    Can J Microbiol. 1989 Jan;35(1):234-44 PMID: 2497941
  13. Life with 6000 genes.
    Science. 1996 Oct 25;274(5287):546, 563-7 PMID: 8849441
  14. The organization of cytoplasmic ribosomal protein genes in the Arabidopsis genome.
    Plant Physiol. 2001 Oct;127(2):398-415 PMID: 11598216
  15. High resolution structure of the large ribosomal subunit from a mesophilic eubacterium.
    Cell. 2001 Nov 30;107(5):679-88 PMID: 11733066
  16. Sequence alignment and evolutionary comparison of the L10 equivalent and L12 equivalent ribosomal proteins from archaebacteria, eubacteria, and eucaryotes.
    J Mol Evol. 1989 Nov;29(5):448-62 PMID: 2515294
  17. The structural basis of ribosome activity in peptide bond synthesis.
    Science. 2000 Aug 11;289(5481):920-30 PMID: 10937990
  18. Genomic Analysis of the Genes Encoding Ribosomal Proteins in Eight Eubacterial Species and Saccharomyces cerevisiae.
    Genome Inform Ser Workshop Genome Inform. 1998;9:3-12 PMID: 11072316
  19. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution.
    Science. 2000 Aug 11;289(5481):905-20 PMID: 10937989
  20. A map of 75 human ribosomal protein genes.
    Genome Res. 1998 May;8(5):509-23 PMID: 9582194
  21. RefSeq and LocusLink: NCBI gene-centered resources.
    Nucleic Acids Res. 2001 Jan 1;29(1):137-40 PMID: 11125071
  22. Ribosome structure and the mechanism of translation.
    Cell. 2002 Feb 22;108(4):557-72 PMID: 11909526
  23. Structural compensation for the deficit of rRNA with proteins in the mammalian mitochondrial ribosome. Systematic analysis of protein components of the large ribosomal subunit from mammalian mitochondria.
    J Biol Chem. 2001 Jun 15;276(24):21724-36 PMID: 11279069
  24. The human ribosomal protein genes: sequencing and comparative analysis of 73 genes.
    Genome Res. 2002 Mar;12(3):379-90 PMID: 11875025
  25. The plastid ribosomal proteins. Identification of all the proteins in the 50 S subunit of an organelle ribosome (chloroplast).
    J Biol Chem. 2000 Sep 15;275(37):28466-82 PMID: 10874046
  26. Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes.
    Nature. 1987 Mar 26-Apr 1;326(6111):411-4 PMID: 3550472
  27. Assembly mapping of 30 S ribosomal proteins from Escherichia coli. Further studies.
    J Biol Chem. 1974 May 25;249(10):3103-11 PMID: 4598121
  28. Growth phase coupled modulation of Escherichia coli ribosomes.
    Genes Cells. 1998 Apr;3(4):203-8 PMID: 9663655
  29. Universal protein families and the functional content of the last universal common ancestor.
    J Mol Evol. 1999 Oct;49(4):413-23 PMID: 10485999
  30. Structure of the 30S ribosomal subunit.
    Nature. 2000 Sep 21;407(6802):327-39 PMID: 11014182
  31. Ribosomal protein L32 of Saccharomyces cerevisiae regulates both splicing and translation of its own transcript.
    J Biol Chem. 1993 Sep 15;268(26):19669-74 PMID: 8366109
  32. Structure of functionally activated small ribosomal subunit at 3.3 angstroms resolution.
    Cell. 2000 Sep 1;102(5):615-23 PMID: 11007480
  33. Eocytes: a new ribosome structure indicates a kingdom with a close relationship to eukaryotes.
    Proc Natl Acad Sci U S A. 1984 Jun;81(12):3786-90 PMID: 6587394
  34. A complete map of the human ribosomal protein genes: assignment of 80 genes to the cytogenetic map and implications for human disorders.
    Genomics. 2001 Mar 15;72(3):223-30 PMID: 11401437
  35. Components of bacterial ribosomes.
    Annu Rev Biochem. 1982;51:155-83 PMID: 6180678
  36. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform.
    Nucleic Acids Res. 2002 Jul 15;30(14):3059-66 PMID: 12136088
  37. The list of cytoplasmic ribosomal proteins of Saccharomyces cerevisiae.
    Yeast. 1998 Mar 30;14(5):471-7 PMID: 9559554
  38. Archaeal phylogeny based on ribosomal proteins.
    Mol Biol Evol. 2002 May;19(5):631-9 PMID: 11961097
  39. Microsporidia: accumulating molecular evidence that a group of amitochondriate and suspectedly primitive eukaryotes are just curious fungi.
    Gene. 2000 Apr 4;246(1-2):1-8 PMID: 10767522
  40. The COG database: new developments in phylogenetic classification of proteins from complete genomes.
    Nucleic Acids Res. 2001 Jan 1;29(1):22-8 PMID: 11125040
  41. The path from the RNA world.
    J Mol Evol. 1998 Jan;46(1):1-17 PMID: 9419221
  42. Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes.
    Proc Natl Acad Sci U S A. 1989 Dec;86(23):9355-9 PMID: 2531898
  43. Isolation and characterization of a new ribosomal protein from the thermophilic eubacteria, Thermus thermophilus, T. aquaticus and T. flavus.
    Biol Chem Hoppe Seyler. 1993 Jun;374(6):377-83 PMID: 8357533
  44. Assembly map of the large subunit (50S) of Escherichia coli ribosomes.
    Proc Natl Acad Sci U S A. 1982 Feb;79(3):729-33 PMID: 7038683
  45. Affinity labelling of yeast ribosomal peptidyl transferase.
    Mol Gen Genet. 1978 Jul 6;163(1):29-34 PMID: 355841
  46. Gene context conservation of a higher order than operons.
    Trends Biochem Sci. 2000 Oct;25(10):474-9 PMID: 11050428
  47. Purification and characterization of the 30S ribosomal proteins from the bacterium Thermus thermophilus.
    Eur J Biochem. 1994 Nov 15;226(1):169-77 PMID: 7957245
  48. SETOR: hardware-lighted three-dimensional solid model representations of macromolecules.
    J Mol Graph. 1993 Jun;11(2):134-8, 127-8 PMID: 8347566
  49. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi.
    Nature. 2001 Nov 22;414(6862):450-3 PMID: 11719806
  50. Re-annotation of genome microbial coding-sequences: finding new genes and inaccurately annotated genes.
    BMC Bioinformatics. 2002;3:5 PMID: 11879526
  51. Crystal structure of the ribosome at 5.5 A resolution.
    Science. 2001 May 4;292(5518):883-96 PMID: 11283358
  52. The plastid ribosomal proteins. Identification of all the proteins in the 30 S subunit of an organelle ribosome (chloroplast).
    J Biol Chem. 2000 Sep 15;275(37):28455-65 PMID: 10874039
  53. Triplet repeat-containing ribosomal protein L14 gene in immortalized human endothelial cell line (t-HUE4).
    Biochem Biophys Res Commun. 1998 Feb 13;243(2):531-7 PMID: 9480843
  54. Towards understanding the first genome sequence of a crenarchaeon by genome annotation using clusters of orthologous groups of proteins (COGs).
    Genome Biol. 2000;1(5):RESEARCH0009 PMID: 11178258
  55. Archaea sister group of Bacteria? Indications from tree reconstruction artifacts in ancient phylogenies.
    Mol Biol Evol. 1999 Jun;16(6):817-25 PMID: 10368959
  56. Distribution of substitution rates and location of insertion sites in the tertiary structure of ribosomal RNA.
    Nucleic Acids Res. 2001 Dec 15;29(24):5017-28 PMID: 11812832
  57. The European Large Subunit Ribosomal RNA Database.
    Nucleic Acids Res. 2001 Jan 1;29(1):175-7 PMID: 11125083
  58. Molecular phylogeny. Archaebacteria and Archezoa.
    Nature. 1989 May 11;339(6220):l00-1 PMID: 2497352
  59. Evolutionary analyses of the 12-kDa acidic ribosomal P-proteins reveal a distinct protein of higher plant ribosomes.
    Proc Natl Acad Sci U S A. 1998 Mar 3;95(5):2378-83 PMID: 9482893
  60. Two C or not two C: recurrent disruption of Zn-ribbons, gene duplication, lineage-specific gene loss, and horizontal gene transfer in evolution of bacterial ribosomal proteins.
    Genome Biol. 2001;2(9):RESEARCH 0033 PMID: 11574053
  61. Whither microbiology? Phylogenetic trees.
    Curr Biol. 1996 Sep 1;6(9):1060-3 PMID: 8805350
  62. Functional classes in the three domains of life.
    J Mol Evol. 1999 Nov;49(5):551-7 PMID: 10552036
  63. Cytoplasmic ribosomal protein genes of the fission yeast Schizosaccharomyces pombe display a unique promoter type: a suggestion for nomenclature of cytoplasmic ribosomal proteins in databases.
    Nucleic Acids Res. 1998 Jul 15;26(14):3319-22 PMID: 9649613
  64. Structure of the 80S ribosome from Saccharomyces cerevisiae--tRNA-ribosome and subunit-subunit interactions.
    Cell. 2001 Nov 2;107(3):373-86 PMID: 11701127
  65. Complete genome sequences of cellular life forms: glimpses of theoretical evolutionary genomics.
    Curr Opin Genet Dev. 1996 Dec;6(6):757-62 PMID: 8994848
  66. Archaeal genomics: do archaea have a mixed heritage?
    Curr Biol. 1998 Mar 12;8(6):R209-11 PMID: 9512414
  67. Extraribosomal functions of ribosomal proteins.
    Trends Biochem Sci. 1996 May;21(5):164-5 PMID: 8871397
  68. Genome plasticity as a paradigm of eubacteria evolution.
    J Mol Evol. 1997;44 Suppl 1:S57-64 PMID: 9395406
  69. Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics.
    Nature. 2000 Sep 21;407(6802):340-8 PMID: 11014183
  70. Visualization of protein S1 within the 30S ribosomal subunit and its interaction with messenger RNA.
    Proc Natl Acad Sci U S A. 2001 Oct 9;98(21):11991-6 PMID: 11593008
  71. Towards a reliable objective function for multiple sequence alignments.
    J Mol Biol. 2001 Dec 7;314(4):937-51 PMID: 11734009
  72. Metabolic symbiosis at the origin of eukaryotes.
    Trends Biochem Sci. 1999 Mar;24(3):88-93 PMID: 10203753
  73. Observation of Escherichia coli ribosomal proteins and their posttranslational modifications by mass spectrometry.
    Anal Biochem. 1999 Apr 10;269(1):105-12 PMID: 10094780
  74. The COG database: a tool for genome-scale analysis of protein functions and evolution.
    Nucleic Acids Res. 2000 Jan 1;28(1):33-6 PMID: 10592175
  75. Structure and evolution of mammalian ribosomal proteins.
    Biochem Cell Biol. 1995 Nov-Dec;73(11-12):933-47 PMID: 8722009
  76. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  77. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya.
    Proc Natl Acad Sci U S A. 1990 Jun;87(12):4576-9 PMID: 2112744
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
1362-4962
DOI
10.1093/nar/gkf693
Published
2002-12-15
Pages
5382-90
Language
English
Region
England
NLM ID
0411011
PMCID
PMC140077
Subset
IM
External Links
PubMed source DOI: 10.1093/nar/gkf693 PMC Full Text View journal details
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