Home LiteratureArticle Details
PMID: 10051579 Published · ppublish English Comparative Study Journal Article Research Support, U.S. Gov't, P.H.S. Comment

An Escherichia coli strain with all chromosomal rRNA operons inactivated: complete exchange of rRNA genes between bacteria.

Asai T, Zaporojets D, Squires C, Squires CL

Abstract

Current global phylogenies are built predominantly on rRNA sequences. However, an experimental system for studying the evolution of rRNA is not readily available, mainly because the rRNA genes are highly repeated in most experimental organisms. We have constructed an Escherichia coli strain in which all seven chromosomal rRNA operons are inactivated by deletions spanning the 16S and 23S coding regions. A single E. coli rRNA operon carried by a multicopy plasmid supplies 16S and 23S rRNA to the cell. By using this strain we have succeeded in creating microorganisms that contain only a foreign rRNA operon derived from either Salmonella typhimurium or Proteus vulgaris, microorganisms that have diverged from E. coli about 120-350 million years ago. We also were able to replace the E. coli rRNA operon with an E. coli/yeast hybrid one in which the GTPase center of E. coli 23S rRNA had been substituted by the corresponding domain from Saccharomyces cerevisiae. These results suggest that, contrary to common belief, coevolution of rRNA with many other components in the translational machinery may not completely preclude the horizontal transfer of rRNA genes.

MeSH Terms
Base Sequence Chromosomes, Bacterial/genetics Escherichia coli/genetics,growth & development Genes, Bacterial Operon Polymerase Chain Reaction RNA, Bacterial/genetics RNA, Ribosomal/genetics RNA, Ribosomal, 16S/genetics RNA, Ribosomal, 23S/genetics Restriction Mapping Salmonella typhimurium/genetics Sequence Deletion
Chemicals
RNA, Bacterial RNA, Ribosomal RNA, Ribosomal, 16S RNA, Ribosomal, 23S
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Asai T
Department of Molecular Biology and Microbiology, Tufts University School of Medicine, Boston, MA 02111, USA.
Zaporojets D
Squires C
Squires C L
References (35)
35 references, click to expand
  1. Resolution of multiple ribonucleic acid species by polyacrylamide gel electrophoresis.
    Biochemistry. 1967 Jun;6(6):1818-27 PMID: 6035921
  2. Reconstitution of peptide bond formation with Escherichia coli 23S ribosomal RNA domains.
    Science. 1998 Jul 31;281(5377):666-9 PMID: 9685252
  3. Hybrid 30S ribosomal particles reconstituted from components of different bacterial origins.
    Nature. 1968 Aug 24;219(5156):793-9 PMID: 4876933
  4. Establishment of exponential growth after a nutritional shift-up in Escherichia coli B/r: accumulation of deoxyribonucleic acid, ribonucleic acid, and protein.
    J Bacteriol. 1977 Feb;129(2):1020-33 PMID: 320174
  5. Deletion of a ribosomal ribonucleic acid operon in Escherichia coli.
    J Bacteriol. 1980 Aug;143(2):1077-80 PMID: 6162835
  6. Antibiotic resistance mutations in 16S and 23S ribosomal RNA genes of Escherichia coli.
    Nucleic Acids Res. 1984 Jun 11;12(11):4653-63 PMID: 6330677
  7. Evolution in bacteria: evidence for a universal substitution rate in cellular genomes.
    J Mol Evol. 1987;26(1-2):74-86 PMID: 3125340
  8. Cloning and expression in Escherichia coli of Proteus vulgaris genes for 16S ribosomal RNA.
    J Gen Microbiol. 1987 Sep;133(9):2401-9 PMID: 3329212
  9. Antibiotic resistance mutations in ribosomal RNA genes of Escherichia coli.
    Methods Enzymol. 1988;164:673-90 PMID: 3071688
  10. A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli.
    Microbiol Rev. 1989 Mar;53(1):1-24 PMID: 2540407
  11. Isolation of temperature-sensitive mutants of 16 S rRNA in Escherichia coli.
    J Mol Biol. 1989 Oct 20;209(4):645-53 PMID: 2531227
  12. The excision of intervening sequences from Salmonella 23S ribosomal RNA.
    Cell. 1990 Feb 9;60(3):405-14 PMID: 2406020
  13. Genomic organization and physical mapping of the transfer RNA genes in Escherichia coli K12.
    J Mol Biol. 1990 Apr 20;212(4):579-98 PMID: 2184240
  14. Growth rate dependence of transfer RNA abundance in Escherichia coli.
    EMBO J. 1990 Dec;9(13):4359-66 PMID: 2265611
  15. Unusual resistance of peptidyl transferase to protein extraction procedures.
    Science. 1992 Jun 5;256(5062):1416-9 PMID: 1604315
  16. Comparison of the expression of the seven ribosomal RNA operons in Escherichia coli.
    EMBO J. 1992 Nov;11(11):4175-85 PMID: 1396599
  17. Evolution by acquisition: the case for horizontal gene transfers.
    Trends Biochem Sci. 1992 Dec;17(12):489-93 PMID: 1471257
  18. Replacement of the L11 binding region within E.coli 23S ribosomal RNA with its homologue from yeast: in vivo and in vitro analysis of hybrid ribosomes altered in the GTPase centre.
    EMBO J. 1993 Apr;12(4):1499-504 PMID: 7682175
  19. Mutations in eukaryotic 18S ribosomal RNA affect translational fidelity and resistance to aminoglycoside antibiotics.
    EMBO J. 1994 Feb 15;13(4):906-13 PMID: 8112304
  20. Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment.
    Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1609-13 PMID: 7510403
  21. Lessons from an evolving rRNA: 16S and 23S rRNA structures from a comparative perspective.
    Microbiol Rev. 1994 Mar;58(1):10-26 PMID: 8177168
  22. High abundance of Archaea in Antarctic marine picoplankton.
    Nature. 1994 Oct 20;371(6499):695-7 PMID: 7935813
  23. A translational fidelity mutation in the universally conserved sarcin/ricin domain of 25S yeast ribosomal RNA.
    RNA. 1996 Mar;2(3):254-63 PMID: 8608449
  24. The translational function of nucleotide C1054 in the small subunit rRNA is conserved throughout evolution: genetic evidence in yeast.
    Proc Natl Acad Sci U S A. 1996 Mar 19;93(6):2517-22 PMID: 8637906
  25. The accuracy center of a eukaryotic ribosome.
    Biochem Cell Biol. 1995 Nov-Dec;73(11-12):1141-9 PMID: 8722031
  26. Perspectives on archaeal diversity, thermophily and monophyly from environmental rRNA sequences.
    Proc Natl Acad Sci U S A. 1996 Aug 20;93(17):9188-93 PMID: 8799176
  27. The RDP (Ribosomal Database Project).
    Nucleic Acids Res. 1997 Jan 1;25(1):109-11 PMID: 9016515
  28. Evolutionary divergence and salinity-mediated selection in halophilic archaea.
    Microbiol Mol Biol Rev. 1997 Mar;61(1):90-104 PMID: 9106366
  29. Functional importance of RNA interactions in selection of translation initiation codons.
    Mol Microbiol. 1997 Apr;24(1):19-28 PMID: 9140962
  30. Ribosomes and translation.
    Annu Rev Biochem. 1997;66:679-716 PMID: 9242921
  31. Molecular movement inside the translational engine.
    Cell. 1998 Feb 6;92(3):337-49 PMID: 9476894
  32. Possible involvement of Escherichia coli 23S ribosomal RNA in peptide bond formation.
    RNA. 1998 Mar;4(3):257-67 PMID: 9510328
  33. Chimeric rRNAs containing the GTPase centers of the developmentally regulated ribosomal rRNAs of Plasmodium falciparum are functionally distinct.
    RNA. 1998 May;4(5):594-602 PMID: 9582100
  34. Bacterial phylogeny based on comparative sequence analysis.
    Electrophoresis. 1998 Apr;19(4):554-68 PMID: 9588802
  35. Genome data shake tree of life.
    Science. 1998 May 1;280(5364):672-4 PMID: 9599142
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1999-03-02
Pages
1971-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC26721
Subset
IM
Grants
NIGMS NIH HHS · R01 GM024751 · United States
NIGMS NIH HHS · GM24751 · United States
Corrections
CommentOn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]