1887

Abstract

The number of copies of rRNA genes in bacterial genomes differs greatly among bacterial species. It is difficult to determine the functional significance of the heterogeneity of each rRNA operon fully due to the existence of multiple rRNA operons and because the sequence heterogeneity among the rRNA genes is extremely low. To overcome this problem, we sequentially deleted the ten operons of and constructed seven mutant strains that each harboured a single operon (either , , , , , or ) in their genome. The growth rates and sporulation frequencies of these mutants were reduced drastically compared with those of the wild-type strain, and this was probably due to decreased levels of ribosomes in the mutants. Interestingly, the ability to sporulate varied significantly among the mutant strains. These mutants have proved to be invaluable in our initial attempts to reveal the functional significance of the heterogeneity of each rRNA operon.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.035295-0
2010-10-01
2020-07-09
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/10/2944.html?itemId=/content/journal/micro/10.1099/mic.0.035295-0&mimeType=html&fmt=ahah

References

  1. Asai T., Zaporojets D., Squires C., Squires C. L.. 1999a; An Escherichia coli strain with all chromosomal rRNA operons inactivated: complete exchange of rRNA genes between bacteria. Proc Natl Acad Sci U S A96:1971–1976
    [Google Scholar]
  2. Asai T., Condon C., Voulgaris J., Zaporojets D., Shen B., Al-omar M., Squires C., Squires C. L.. 1999b; Construction and initial characterization of Escherichia coli strains with few or no intact chromosomal rRNA operons. J Bacteriol181:3803–3809
    [Google Scholar]
  3. Ashikaga S., Nanamiya H., Ohashi Y., Kawamura F.. 2000; Natural genetic competence in Bacillus subtilis Natto OK2. J Bacteriol182:2411–2415
    [Google Scholar]
  4. Chibazakura T., Kawamura F., Takahashi H.. 1991; Differential regulation of spo0A transcription in Bacillus subtilis: glucose represses promoter switching at the initiation of sporulation. J Bacteriol173:2625–2632
    [Google Scholar]
  5. Condon C., Philips J., Fu Z.-Y., Squires C., Squires C. L.. 1992; Comparison of the expression of the seven ribosomal RNA operons in Escherichia coli. EMBO J11:4175–4185
    [Google Scholar]
  6. Condon C., Liveris D., Squires C., Schwartz I., Squires C. L.. 1995; rRNA operon multiplicity in Escherichia coli and the physiological implications of rrn inactivation. J Bacteriol177:4152–4156
    [Google Scholar]
  7. Ellwood M., Nomura M.. 1980; Deletion of a ribosomal ribonucleic acid operon in Escherichia coli. J Bacteriol143:1077–1080
    [Google Scholar]
  8. Fraser C. M., Gocayne J. D., White O., Adams M. D., Clayton R. A., Fleischmann R. D., Bult C. J., Kerlavage A. R., Sutton G.. & other authors 1995; The minimal gene complement of Mycoplasma genitalium. Science270:397–403
    [Google Scholar]
  9. Grossman A. D.. 1995; Genetic networks controlling the initiation of sporulation and the development of genetic competence in Bacillus subtilis. Annu Rev Genet29:477–508
    [Google Scholar]
  10. Gunderson J. H., Sogin M. L., Wollett G., Hollingdale M., de la Cruz V. F., Waters A. P., McCutchan T. F.. 1987; Structurally distinct, stage-specific ribosomes occur in Plasmodium. Science238:933–937
    [Google Scholar]
  11. Henkin T. M.. 2002; Ribosomes, protein synthesis factors, and tRNA synthetases. In Bacillus subtilis and its Closest Relatives: from Genes to Cells. pp313–322 Edited by Sonenshein A. L., Hoch J. A., Losick R.. Washington, DC: American Society for Microbiology;
  12. Hirabayashi N., Sato N. S., Suzuki T.. 2006; Conserved loop sequence of helix 69 in Escherichia coli 23S rRNA is involved in A-site tRNA binding and translational fidelity. J Biol Chem281:17203–17211
    [Google Scholar]
  13. Hobbie S. N., Bruell C., Kalapala S., Akshay S., Schmidt S., Pfister P., Böttger E. C.. 2006; A genetic model to investigate drug–target interactions at the ribosomal decoding site. Biochimie88:1033–1043
    [Google Scholar]
  14. Hoch J. A.. 1993; Regulation of the phosphorelay and the initiation of sporulation in Bacillus subtilis. Annu Rev Microbiol47:441–465
    [Google Scholar]
  15. Klappenbach J. A., Dunbar J. M., Schmidt T. M.. 2000; rRNA operon copy number reflects ecological strategies of bacteria. Appl Environ Microbiol66:1328–1333
    [Google Scholar]
  16. Klappenbach J. A., Saxman P. R., Cole J. R., Schmidt T. M.. 2001; rrndb: the ribosomal RNA operon copy number database. Nucleic Acids Res29:181–184
    [Google Scholar]
  17. Kunst F., Ogasawara N., Moszer I., Albertini A. M., Alloni G., Azevedo V., Bertero M. G., Bessieres P., Bolotin A.. other authors 1997; The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature390:249–256
    [Google Scholar]
  18. Leighton T. J., Doi R. H.. 1971; The stability of messenger ribonucleic acid during sporulation in Bacillus subtilis. J Biol Chem246:3189–3195
    [Google Scholar]
  19. Loughney K., Lund E., Dahlberg J. E.. 1982; tRNA genes are found between the 16S and 23S rRNA genes in Bacillus subtilis. Nucleic Acids Res10:1607–1624
    [Google Scholar]
  20. Monshupanee T., Fa-aroonsawat S., Chungjatupornchai W.. 2006; A cyanobacterial strain with all chromosomal rRNA operons inactivated: a single nucleotide mutation of 23S rRNA confers temperature-sensitive phenotypes. Microbiology152:1417–1425
    [Google Scholar]
  21. Natori Y., Nanamiya H., Akanuma G., Kosono S., Kudo T., Ochi K., Kawamura F.. 2007; A fail-safe system for the ribosome under zinc-limiting conditions in Bacillus subtilis. Mol Microbiol63:294–307
    [Google Scholar]
  22. Nomura M.. 1999; Engineering of bacterial ribosomes: replacement of all seven Escherichia coli rRNA operons by a single plasmid-encoded operon. Proc Natl Acad Sci U S A96:1820–1822
    [Google Scholar]
  23. Ogasawara N., Moriya S., Yoshikawa H.. 1983; Structure and organization of rRNA operons in the region of the replication origin of the Bacillus subtilis chromosome. Nucleic Acids Res11:6301–6318
    [Google Scholar]
  24. Predich M., Nair G., Smith I.. 1992; Bacillus subtilis early sporulation genes kinA, spo0F, and spo0A are transcribed by the RNA polymerase containing σH. J Bacteriol174:2771–2778
    [Google Scholar]
  25. Recht M. I., Puglisi J. D.. 2001; Aminoglycoside resistance with homogeneous and heterogeneous populations of antibiotic-resistant ribosomes. Antimicrob Agents Chemother45:2414–2419
    [Google Scholar]
  26. Rutberg L.. 1969; Mapping a temperate bacteriophage active on Bacillus subtilis. J Virol3:38–44
    [Google Scholar]
  27. Sambrook J., Russell D.. 2001; Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  28. Sander P., Prammananan T., Böttger E. C.. 1996; Introducing mutations into a chromosomal rRNA gene using a genetically modified eubacterial host with a single rRNA operon. Mol Microbiol22:841–848
    [Google Scholar]
  29. Schaeffer P., Millet J., Aubert J.. 1965; Catabolic repression of bacterial sporulation. Proc Natl Acad Sci U S A54:704–711
    [Google Scholar]
  30. Sergiev P. V., Lesnyak D. V., Kiparisov S. V., Burakovsky D. E., Leonov A. A., Bogdanov A. A., Brimacombe R., Dontsova O. A.. 2005; Function of the ribosomal E-site: a mutagenesis study. Nucleic Acids Res33:6048–6056
    [Google Scholar]
  31. Widom R. L., Jarvis E. D., LaFauci G., Rudner R.. 1988; Instability of rRNA operons in Bacillus subtilis. J Bacteriol170:605–610
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.035295-0
Loading
/content/journal/micro/10.1099/mic.0.035295-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error