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PMID: 9603876 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Posttranscriptional modifications in 16S and 23S rRNAs of the archaeal hyperthermophile Sulfolobus solfataricus.

Journal of bacteriology ·Vol. 180 ·No. 11 ·1998-06-00 ·Pages 2883-8

Noon KR, Bruenger E, McCloskey JA

Abstract

Posttranscriptional modification is common to many types of RNA, but the majority of information concerning structure and function of modification is derived principally from tRNA. By contrast, less is known about modification in rRNA in spite of accumulating evidence for its direct participation in translation. The structural identities and approximate molar levels of modifications have been established for 16S and 23S rRNAs of the archaeal hyperthermophile Sulfolobus solfactaricus by using combined chromatography-mass spectrometry-based methods. Modification levels are exceptionally high for prokaryotic organisms, with approximately 38 modified sites in 16S rRNA and 50 in 23S rRNA for cells cultured at 75 degrees C, compared with 11 and 23 sites, respectively, in Escherichia coli. We structurally characterized 10 different modified nucleosides in 16S rRNA, 64% (24 residues) of which are methylated at O-2' of ribose, and 8 modified species in 23S rRNA, 86% (43 residues) of which are ribose methylated, a form of modification shown in earlier studies to enhance stability of the polynucleotide chain. From cultures grown at progressively higher temperatures, 60, 75, and 83 degrees C, a slight trend toward increased ribose methylation levels was observed, with greatest net changes over the 23 degrees C range shown for 2'-O-methyladenosine in 16S rRNA (21% increase) and for 2'-O-methylcytidine (24%) and 2'-O-methylguanosine (22%) in 23S rRNA. These findings are discussed in terms of the potential role of modification in stabilization of rRNA in the thermal environment.

MeSH Terms
Alkylation Methylation RNA Processing, Post-Transcriptional/physiology RNA, Ribosomal, 16S/metabolism RNA, Ribosomal, 23S/metabolism Ribonucleosides/metabolism Ribose/metabolism Sulfolobus/genetics,metabolism Temperature
Chemicals
RNA, Ribosomal, 16S RNA, Ribosomal, 23S Ribonucleosides Ribose
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Noon K R
Department of Medicinal Chemistry, University of Utah, Salt Lake City, Utah 84112, USA.
Bruenger E
McCloskey J A
References (48)
48 references, click to expand
  1. Pseudouridine in the large-subunit (23 S-like) ribosomal RNA. The site of peptidyl transfer in the ribosome?
    FEBS Lett. 1992 May 4;302(1):1-4 PMID: 1587345
  2. Analysis of RNA hydrolyzates by liquid chromatography-mass spectrometry.
    Methods Enzymol. 1990;193:796-824 PMID: 1706064
  3. The effects of methionine deprivation on ribosome synthesis in HeLa cells.
    Proc Natl Acad Sci U S A. 1967 Oct;58(4):1527-34 PMID: 5237886
  4. The effect of growth temperatures on the in vivo ribose methylation of Bacillus stearothermophilus transfer RNA.
    Arch Biochem Biophys. 1973 Jan;154(1):277-82 PMID: 4689778
  5. Transfer RNA modification.
    Annu Rev Biochem. 1987;56:263-87 PMID: 3304135
  6. Structural domains of transfer RNA molecules.
    Science. 1976 Nov 19;194(4267):796-806 PMID: 790568
  7. The phylogenetic relationships of three sulfur dependent archaebacteria.
    Syst Appl Microbiol. 1984;5:97-105 PMID: 11541975
  8. In vitro complementation analysis localizes 23S rRNA posttranscriptional modifications that are required for Escherichia coli 50S ribosomal subunit assembly and function.
    RNA. 1996 Oct;2(10):1011-21 PMID: 8849777
  9. Heat-induced stability of tRNA from an extreme thermophile, Thermus thermophilus.
    Biochem Biophys Res Commun. 1976 Oct 4;72(3):1137-44 PMID: 985514
  10. The role of posttranscriptional modification in stabilization of transfer RNA from hyperthermophiles.
    Biochemistry. 1994 Jun 28;33(25):7869-76 PMID: 7516708
  11. Clustering of modified nucleotides at the functional center of bacterial ribosomal RNA.
    FASEB J. 1993 Jan;7(1):161-7 PMID: 8422963
  12. Biochemical and physical characterization of an unmodified yeast phenylalanine transfer RNA transcribed in vitro.
    Proc Natl Acad Sci U S A. 1988 Feb;85(4):1033-7 PMID: 3277187
  13. Detailed analysis of the higher-order structure of 16S-like ribosomal ribonucleic acids.
    Microbiol Rev. 1983 Dec;47(4):621-69 PMID: 6363901
  14. Summary: the modified nucleosides of RNA.
    Nucleic Acids Res. 1994 Jun 25;22(12):2183-96 PMID: 7518580
  15. Ribosome activity and modification of 16S RNA are influenced by deletion of ribosomal protein S20.
    Mol Microbiol. 1993 Mar;7(6):983-92 PMID: 7683367
  16. A modified nucleotide in tRNA as a possible regulator of aerobiosis: synthesis of cis-2-methyl-thioribosylzeatin in the tRNA of Salmonella.
    Cell. 1984 Feb;36(2):523-31 PMID: 6362893
  17. The RDP (Ribosomal Database Project).
    Nucleic Acids Res. 1997 Jan 1;25(1):109-11 PMID: 9016515
  18. Mapping to nucleotide resolution of pseudouridine residues in large subunit ribosomal RNAs from representative eukaryotes, prokaryotes, archaebacteria, mitochondria and chloroplasts.
    J Mol Biol. 1997 Feb 21;266(2):246-68 PMID: 9047361
  19. Complete analysis of tRNA-modified nucleosides by high-performance liquid chromatography: the 29 modified nucleosides of Salmonella typhimurium and Escherichia coli tRNA.
    Anal Biochem. 1983 Feb 15;129(1):1-13 PMID: 6190418
  20. The absence of modified nucleotides affects both in vitro assembly and in vitro function of the 30S ribosomal subunit of Escherichia coli.
    Biochimie. 1991 Jun;73(6):789-96 PMID: 1764523
  21. A novel method for the determination of post-transcriptional modification in RNA by mass spectrometry.
    Nucleic Acids Res. 1993 Sep 25;21(19):4577-85 PMID: 8233793
  22. Relation between functions and conformational characteristics of modified nucleosides found in tRNAs.
    Nucleic Acids Symp Ser. 1991;(25):49-50 PMID: 1726811
  23. Sulfolobus: a new genus of sulfur-oxidizing bacteria living at low pH and high temperature.
    Arch Mikrobiol. 1972;84(1):54-68 PMID: 4559703
  24. Characterization of fully 2'-modified oligoribonucleotide hetero- and homoduplex hybridization and nuclease sensitivity.
    Nucleic Acids Res. 1995 Jun 11;23(11):2019-24 PMID: 7541132
  25. Preparation and enzymatic hydrolysis of DNA and RNA for mass spectrometry.
    Methods Enzymol. 1990;193:782-90 PMID: 1706062
  26. A new model for the three-dimensional folding of Escherichia coli 16 S ribosomal RNA. II. The RNA-protein interaction data.
    J Mol Biol. 1997 Aug 29;271(4):545-65 PMID: 9281425
  27. Classification of methanogenic bacteria by 16S ribosomal RNA characterization.
    Proc Natl Acad Sci U S A. 1977 Oct;74(10):4537-41 PMID: 16592452
  28. Synthesis and hybridization studies on two complementary nona(2'-O-methyl)ribonucleotides.
    Nucleic Acids Res. 1987 Aug 11;15(15):6131-48 PMID: 3627981
  29. Functional requirement of a site-specific ribose methylation in ribosomal RNA.
    Science. 1993 Dec 17;262(5141):1886-9 PMID: 8266080
  30. Pseudouridine and O2'-methylated nucleosides. Significance of their selective occurrence in rRNA domains that function in ribosome-catalyzed synthesis of the peptide bonds in proteins.
    Biochimie. 1995;77(1-2):7-15 PMID: 7599278
  31. The RNA modification database--1998.
    Nucleic Acids Res. 1998 Jan 1;26(1):196-7 PMID: 9399834
  32. Posttranscriptional modification of tRNA in thermophilic archaea (Archaebacteria).
    J Bacteriol. 1991 May;173(10):3138-48 PMID: 1708763
  33. Probing structural differences between native and in vitro transcribed Escherichia coli valine transfer RNA: evidence for stable base modification-dependent conformers.
    Nucleic Acids Res. 1993 Oct 25;21(21):4948-53 PMID: 8177744
  34. Decoding fidelity at the ribosomal A and P sites: influence of mutations in three different regions of the decoding domain in 16S rRNA.
    Nucleic Acids Res. 1997 Mar 15;25(6):1185-93 PMID: 9092628
  35. Implications of a functional large ribosomal RNA with only three modified nucleotides.
    Biochimie. 1995;77(1-2):30-9 PMID: 7541254
  36. Phylogeny of the conserved 3' terminal structure of the RNA of small ribosomal subunits.
    Nucleic Acids Res. 1984 Mar 26;12(6):2595-604 PMID: 6709501
  37. Conformational rigidity of specific pyrimidine residues in tRNA arises from posttranscriptional modifications that enhance steric interaction between the base and the 2'-hydroxyl group.
    Biochemistry. 1992 Feb 4;31(4):1040-6 PMID: 1310418
  38. Ribosomes and translation.
    Annu Rev Biochem. 1997;66:679-716 PMID: 9242921
  39. The numerous modified nucleotides in eukaryotic ribosomal RNA.
    Prog Nucleic Acid Res Mol Biol. 1990;39:241-303 PMID: 2247610
  40. Compilation of tRNA sequences and sequences of tRNA genes.
    Nucleic Acids Res. 1998 Jan 1;26(1):148-53 PMID: 9399820
  41. The single pseudouridine residue in Escherichia coli 16S RNA is located at position 516.
    Nucleic Acids Res. 1994 Sep 11;22(18):3681-4 PMID: 7524026
  42. Posttranscriptional modification of the central loop of domain V in Escherichia coli 23 S ribosomal RNA.
    J Biol Chem. 1995 Jul 28;270(30):17758-64 PMID: 7629075
  43. 5S rRNA modification in the hyperthermophilic archaea Sulfolobus solfataricus and Pyrodictium occultum.
    FASEB J. 1993 Jan;7(1):196-200 PMID: 8422966
  44. The pseudouridine residues of ribosomal RNA.
    Biochem Cell Biol. 1995 Nov-Dec;73(11-12):915-24 PMID: 8722007
  45. 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
  46. Thermospray liquid chromatography/mass spectrometry in deuterium oxide.
    Anal Chem. 1988 Oct 15;60(20):2314-7 PMID: 2853586
  47. Ribonucleoside analysis by reversed-phase high-performance liquid chromatography.
    J Chromatogr. 1989 Jun 2;471:3-36 PMID: 2670985
  48. Archaebacterial phylogeny: perspectives on the urkingdoms.
    Syst Appl Microbiol. 1986;7:161-77 PMID: 11542063
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
DOI
10.1128/JB.180.11.2883-2888.1998
Published
1998-06-00
Pages
2883-8
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC107253
Subset
IM
Grants
NIGMS NIH HHS · R01 GM029812 · United States
NIGMS NIH HHS · GM29812 · United States
External Links
PubMed source DOI: 10.1128/JB.180.11.2883-2888.1998 PMC Full Text View journal details
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