Skip to main content
Log in

Genome-wide survey of mRNA half-lives in Bacillus subtilis identifies extremely stable mRNAs

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

We have used DNA microarrays to survey rates of mRNA decay on a genomic scale in early stationary-phase cultures of Bacillus subtilis. The decay rates for mRNAs corresponding to about 1500 genes could be estimated. About 80% of these mRNAs had a half-life of less than 7 min. More than 30 mRNAs, including both mono- and polycistronic transcripts, were found to be extremely stable, i.e. to have a half-life of ≥15 min. Only two such transcripts were known previously in B. subtilis. The results provide the first overview of mRNA decay rates in a gram-positive bacterium and help to identify polycistronic operons. We could find no obvious correlation between the stability of an mRNA and the function of the encoded protein. We have also not found any general features in the 5′ regions of mRNAs that distinguish stable from unstable transcripts. The identified set of extremely stable mRNAs may be useful in the construction of stable recombinant genes for the overproduction of biomolecules in Bacillus species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3A, B.
Fig. 4.
Fig. 5.
Fig. 6.

Similar content being viewed by others

References

  • Agaisse H, Lereclus D (1996) STAB-SD: a Shine-Dalgarno sequence in the 5′ untranslated region is a determinant of mRNA stability. Mol Microbiol 20:633–643

    Google Scholar 

  • Allmansberger R (1996) Degradation of the Bacillus subtilis xynA transcript is accelerated in response to stress. Mol Gen Genet 251:108–112

    Google Scholar 

  • Ayer DE, Dynan WS (1988) Simian virus 40 major late promoter: a novel tripartite structure that includes intragenic sequences. Mol Cell Biol 8:2021–2033

    Google Scholar 

  • Belasco J, Brawerman G (1993) Control of messenger RNA stability. Academic Press, San Diego

  • Bernstein JA, Khodursky AB, Lin PH, Lin-Chao S, Cohen SN (2002) Global analysis of mRNA decay and abundance in Escherichia coli at single-gene resolution using two-color fluorescent DNA microarrays. Proc Natl Acad Sci USA 99:9697–9702

    Google Scholar 

  • Condon C (2003) RNA processing and degradation in Bacillus subtilis. Microbiol Mol Biol rev 67:157–174

  • Condon C, Putzer H (2002) The phylogenetic distribution of bacterial ribonucleases. Nucleic Acids Res 30:5339–5346

    Google Scholar 

  • DiMari JF, Bechhofer DH (1993) Initiation of mRNA decay in Bacillus subtilis. Mol Microbiol 7:705–717

    Google Scholar 

  • Emory SA, Bouvet P, Belasco JG (1992) A 5′-terminal stem-loop structure can stabilize mRNA in Escherichia coli. Genes Dev 6:135–148

    Google Scholar 

  • Fortnagel P, Freese E (1968) Analysis of sporulation mutants. II. Mutants blocked in the citric acid cycle. J Bacteriol 95:1431–1438

    Google Scholar 

  • Fry M, Israeli-Reches M, Artman M (1972) Stabilization and breakdown of Escherichia coli messenger ribonucleic acid in the presence of chloramphenicol. Biochemistry 11:3054–3059

    Google Scholar 

  • Glatz E, Nilsson RP, Rutberg L, Rutberg B (1996) A dual role for the Bacillus subtilis glpD leader and the GlpP protein in the regulated expression of glpD: antitermination and control of mRNA stability. Mol Microbiol 19:319–328

    Google Scholar 

  • Hambraeus G, Persson M, Rutberg B (2000) The aprE leader is a determinant of extreme mRNA stability in Bacillus subtilis. Microbiology 146:3051–3059

    Google Scholar 

  • Hambraeus G, Karhumaa K, Rutberg B (2002) A 5′ stem-loop and ribosome binding but not translation are important for the stability of Bacillus subtilis aprE leader mRNA. Microbiology 148:1795–1803

    Google Scholar 

  • Hue KK, Cohen SD, Bechhofer DH (1995) A polypurine sequence that acts as a 5′ mRNA stabilizer in Bacillus subtilis. J Bacteriol 177:3465–3471

    Google Scholar 

  • Ingraham JL, Maaloe O, Neidhardt FC (1983) Growth of the bacterial cell. Sinauer Associates, Sunderland, Mass.

  • Jurgen B, Schweder T, Hecker M (1998) The stability of mRNA from the gsiB gene of Bacillus subtilis is dependent on the presence of a strong ribosome binding site. Mol Gen Genet 258:538–545

    Google Scholar 

  • Kennell D (2002) Processing endoribonucleases and mRNA degradation in bacteria. J Bacteriol 184:4645–4657

    Google Scholar 

  • Kunst F, et al (1997) The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390:249–256

    Google Scholar 

  • Kushner SR (2002) mRNA decay in Escherichia coli comes of age. J Bacteriol 184:4658–4665

    Google Scholar 

  • Melin L, Rutberg L, von Gabain A (1989) Transcriptional and posttranscriptional control of the Bacillus subtilis succinate dehydrogenase operon. J Bacteriol 171:2110–2115

    Google Scholar 

  • Putzer H, Gendron N, Grunberg-Manago M (1992) Co-ordinate expression of the two threonyl-tRNA synthetase genes in Bacillus subtilis: control by transcriptional antitermination involving a conserved regulatory sequence. EMBO J 11:3117–3127.

    Google Scholar 

  • Resnekov O, Rutberg L, von Gabain A (1990) Changes in the stability of specific mRNA species in response to growth stage in Bacillus subtilis. Proc Natl Acad Sci USA 87:8355–8359

    Google Scholar 

  • Resnekov O, Melin L, Carlsson P, Mannerlov M, von Gabain A, Hederstedt L (1992) Organization and regulation of the Bacillus subtilis odhAB operon, which encodes two of the subenzymes of the 2-oxoglutarate dehydrogenase complex. Mol Gen Genet 234:285–296

    Google Scholar 

  • Romeo T (1998) Global regulation by the small RNA-binding protein CsrA and the non- coding RNA molecule CsrB. Mol Microbiol 29:1321–1330

    Google Scholar 

  • Sandler P, Weisblum B (1989) Erythromycin-induced ribosome stall in the ermA leader: a barricade to 5′-to-3′ nucleolytic cleavage of the ermA transcript. J Bacteriol 171:6680–6688

    Google Scholar 

  • Selinger DW, Saxena RM, Cheung KJ, Church GM, Rosenow C (2003) Global RNA half-life analysis in Escherichia coli reveals positional patterns of transcript degradation. Genome Res 13:216–223

    Google Scholar 

  • Thomas PS (1980) Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci USA 77:5201–5205

    Google Scholar 

  • Wade C, Winkler WC, Cohen-Chalamish S, Breaker RR (2002) An mRNA structure that controls gene expression by binding FMN. Proc Natl Acad Sci USA 99:15908–15913

    Google Scholar 

  • Wang Y, Liu CL, Storey JD, Tibshirani RJ, Herschlag D, Brown PO (2002) Precision and functional specificity in mRNA decay. Proc Natl Acad Sci USA 99:5860–5865

    Google Scholar 

  • Varmus HE, Perlman RL, Pastan I (1971) Regulation of lac transcription in antibiotic-treated Escherichia coli. Nat New Biol 230:41–44

    Google Scholar 

  • Vytvytska O, Jakobsen JS, Balcunaite G, Andersen JS, Baccarini M, von Gabain A (1998) Host factor I, Hfq, binds to Escherichia coli ompA mRNA in a growth rate-dependent fashion and regulates its stability. Proc Natl Acad Sci USA 95:14118–14123

    Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the Swedish Science Research Council (621-2001-3125) and the Crafoord Foundation (20021082). We are grateful to Åke Borg and Johan Vallon-Christersson for generously providing microarray scanning instrumentation and to Blanka Rutberg for critically reading the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. Hederstedt.

Additional information

Communicated by A. Kondorosi

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hambraeus, G., von Wachenfeldt, C. & Hederstedt, L. Genome-wide survey of mRNA half-lives in Bacillus subtilis identifies extremely stable mRNAs. Mol Gen Genomics 269, 706–714 (2003). https://doi.org/10.1007/s00438-003-0883-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-003-0883-6

Keywords

Navigation