Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter December 9, 2005

RNA thermometers are common in α- and γ-proteobacteria

  • Torsten Waldminghaus , Anja Fippinger , Juliane Alfsmann and Franz Narberhaus
From the journal Biological Chemistry

Abstract

Expression of many rhizobial small heat-shock genes is controlled by the ROSE element, a thermoresponsive structure in the 5′-untranslated region of the corresponding mRNAs. Using a bioinformatics approach, we found more than 20 new potential ROSE-like RNA thermometers upstream of small heat-shock genes in a wide variety of α- and γ-proteobacteria. Northern blot analyses revealed heat-inducible transcripts of the representative candidate Caulobacter crescentus CC2258, Escherichia coli ibpA and Salmonella typhimurium ibpA genes. Typical σ32-type promoters were mapped upstream of the potential RNA thermometers by primer extension. Additional translational control was demonstrated in a lacZ reporter system and by site-directed mutagenesis. RNA secondary structure predictions strongly suggest that the Shine-Dalgarno sequence in the RNA thermometers is masked at low temperatures. Combining two regulatory modules, a σ32 promoter and a ROSE-type RNA thermometer, provides a novel stringent mechanism to control expression of small heat-shock genes.

:

Corresponding author

References

Allen, S.P., Polazzi, J.O., Gierse, J.K., and Easton, A.M. (1992). Two novel heat shock genes encoding proteins produced in response to heterologous protein expression in Escherichia coli. J. Bacteriol.174, 6938–6947.10.1128/jb.174.21.6938-6947.1992Search in Google Scholar

Altuvia, S., Kornitzer, D., Teff, D., and Oppenheim, A.B. (1989). Alternative mRNA structures of the cIII gene of bacteriophage lambda determine the rate of its translation initiation. J. Mol. Biol.210, 265–280.10.1016/0022-2836(89)90329-XSearch in Google Scholar

Babst, M., Hennecke, H., and Fischer, H.M. (1996). Two different mechanisms are involved in the heat-shock regulation of chaperonin gene expression in Bradyrhizobium japonicum. Mol. Microbiol.19, 827–839.10.1046/j.1365-2958.1996.438968.xSearch in Google Scholar

Balsiger, S., Ragaz, C., Baron, C., and Narberhaus, F. (2004). Replicon-specific regulation of small heat shock genes in Agrobacterium tumefaciens. J. Bacteriol.186, 6824–6829.10.1128/JB.186.20.6824-6829.2004Search in Google Scholar

Chowdhury, S., Ragaz, C., Kreuger, E., and Narberhaus, F. (2003). Temperature-controlled structural alterations of an RNA thermometer. J. Biol. Chem.278, 47915–47921.10.1074/jbc.M306874200Search in Google Scholar

Chuang, S.E. and Blattner, F.R. (1993). Characterization of twenty-six new heat shock genes of Escherichia coli. J. Bacteriol.175, 5242–5252.10.1128/jb.175.16.5242-5252.1993Search in Google Scholar

Chuang, S.E., Burland, V., Plunkett, G. III, Daniels, D.L., and Blattner, F.R. (1993). Sequence analysis of four new heat-shock genes constituting the hslTS/ibpAB and hslVU operons in Escherichia coli. Gene134, 1–6.10.1016/0378-1119(93)90167-2Search in Google Scholar

El-Samad, H., Kurata, H., Doyle, J.C., Gross, C.A., and Khammash, M. (2005). Surviving heat shock: control strategies for robustness and performance. Proc. Natl. Acad. Sci. USA102, 2736–2741.10.1073/pnas.0403510102Search in Google Scholar PubMed PubMed Central

Guzman, L.M., Belin, D., Carson, M.J., and Beckwith, J. (1995). Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol.177, 4121–4130.10.1128/jb.177.14.4121-4130.1995Search in Google Scholar PubMed PubMed Central

Hapfelmeier, S., Stecher, B., Barthel, M., Kremer, M., Muller, A.J., Heikenwalder, M., Stallmach, T., Hensel, M., Pfeffer, K., Akira, S., and Hardt, W.D. (2005). The Salmonella pathogenicity island (SPI)-2 and SPI-1 type III secretion systems allow Salmonella serovar typhimurium to trigger colitis via MyD88-dependent and MyD88-independent mechanisms. J. Immunol.174, 1675–1685.10.4049/jimmunol.174.3.1675Search in Google Scholar PubMed

Hoe, N.P. and Goguen, J.D. (1993). Temperature sensing in Yersinia pestis: translation of the LcrF activator protein is thermally regulated. J. Bacteriol.175, 7901–7909.10.1128/jb.175.24.7901-7909.1993Search in Google Scholar

Homuth, G., Masuda, S., Mogk, A., Kobayashi, Y., and Schumann, W. (1997). The dnaK operon of Bacillus subtilis is heptacistronic. J. Bacteriol.179, 1153–1164.10.1128/jb.179.4.1153-1164.1997Search in Google Scholar

Hurme, R., Berndt, K.D., Normark, S.J., and Rhen, M. (1997). A proteinaceous gene regulatory thermometer in Salmonella. Cell90, 55–64.10.1016/S0092-8674(00)80313-XSearch in Google Scholar

Johansson, J., Mandin, P., Renzoni, A., Chiaruttini, C., Springer, M., and Cossart, P. (2002). An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell110, 551–561.10.1016/S0092-8674(02)00905-4Search in Google Scholar

Mandal, M. and Breaker, R.R. (2004). Gene regulation by riboswitches. Nat. Rev. Mol. Cell. Biol.5, 451–463.10.1038/nrm1403Search in Google Scholar

Mathews, D.H., Sabina, J., Zuker, M., and Turner, D.H. (1999). Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol.288, 911–940.10.1006/jmbi.1999.2700Search in Google Scholar

Miller, J.H. (1972). Experiments in Molecular Genetics (Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press).Search in Google Scholar

Minton, N.P. (1984). Improved plasmid vectors for the isolation of translational lac gene fusions. Gene31, 269–273.10.1016/0378-1119(84)90220-8Search in Google Scholar

Morita, M., Kanemori, M., Yanagi, H., and Yura, T. (1999a). Heat-induced synthesis of σ32 in Escherichia coli: structural and functional dissection of rpoH mRNA secondary structure. J. Bacteriol.181, 401–410.10.1128/JB.181.2.401-410.1999Search in Google Scholar PubMed PubMed Central

Morita, M.T., Tanaka, Y., Kodama, T.S., Kyogoku, Y., Yanagi, H., and Yura, T. (1999b). Translational induction of heat shock transcription factor σ32: evidence for a built-in RNA thermosensor. Genes Dev.13, 655–665.10.1101/gad.13.6.655Search in Google Scholar PubMed PubMed Central

Münchbach, M., Nocker, A., and Narberhaus, F. (1999). Multiple small heat shock proteins in rhizobia. J. Bacteriol.181, 83–90.10.1128/JB.181.1.83-90.1999Search in Google Scholar PubMed PubMed Central

Nagai, H., Yano, R., Erickson, J.W., and Yura, T. (1990). Transcriptional regulation of the heat shock regulatory gene rpoH in Escherichia coli: involvement of a novel catabolite-sensitive promoter. J. Bacteriol.172, 2710–2715.10.1128/jb.172.5.2710-2715.1990Search in Google Scholar

Nakahigashi, K., Yanagi, H., and Yura, T. (1995). Isolation and sequence analysis of rpoH genes encoding σ32 homologs from gram negative bacteria: conserved mRNA and protein segments for heat shock regulation. Nucleic Acids Res.23, 4383–4390.Search in Google Scholar

Narberhaus, F. (2002a). mRNA-mediated detection of environmental conditions. Arch. Microbiol.178, 404–410.10.1007/s00203-002-0481-8Search in Google Scholar

Narberhaus, F. (2002b). α-Crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol. Mol. Biol. Rev.66, 64–93.10.1128/MMBR.66.1.64-93.2002Search in Google Scholar

Narberhaus, F., Käser, R., Nocker, A., and Hennecke, H. (1998). A novel DNA element that controls bacterial heat shock gene expression. Mol. Microbiol.28, 315–323.10.1046/j.1365-2958.1998.00794.xSearch in Google Scholar

Narberhaus, F., Waldminghaus, T., and Chowdhury, S. (2006). RNA thermometers. FEMS Microbiol. Rev., in press (doi: 10.1111/j.1574-6976.2005.00004.x).Search in Google Scholar

Nocker, A., Hausherr, T., Balsiger, S., Krstulovic, N.P., Hennecke, H., and Narberhaus, F. (2001a). A mRNA-based thermosensor controls expression of rhizobial heat shock genes. Nucleic Acids Res.29, 4800–4807.10.1093/nar/29.23.4800Search in Google Scholar

Nocker, A., Krstulovic, N.P., Perret, X., and Narberhaus, F. (2001b). ROSE elements occur in disparate rhizobia and are functionally interchangeable between species. Arch. Microbiol.176, 44–51.10.1007/s002030100294Search in Google Scholar

Norrander, J., Kempe, T., and Messing, J. (1983). Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene26, 101–106.10.1016/0378-1119(83)90040-9Search in Google Scholar

Nudler, E. and Mironov, A.S. (2004). The riboswitch control of bacterial metabolism. Trends Biochem. Sci.29, 11–17.10.1016/j.tibs.2003.11.004Search in Google Scholar

Poindexter, J.S. (1964). Biological properties and classification of the Caulobacter group. Bacteriol. Rev.28, 231–295.10.1128/br.28.3.231-295.1964Search in Google Scholar

Pridmore, R.D. (1987). New and versatile cloning vectors with kanamycin-resistance marker. Gene56, 309–312.10.1016/0378-1119(87)90149-1Search in Google Scholar

Richmond, C.S., Glasner, J.D., Mau, R., Jin, H., and Blattner, F.R. (1999). Genome-wide expression profiling in Escherichia coli K-12. Nucleic Acids Res.27, 3821–3835.10.1093/nar/27.19.3821Search in Google Scholar PubMed PubMed Central

Sambrook, J.E., Fritsch, F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual (Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press).Search in Google Scholar

Stülke, J. and Hillen, W. (2000). Regulation of carbon catabolism in Bacillus species. Annu. Rev. Microbiol.54, 849–880.10.1146/annurev.micro.54.1.849Search in Google Scholar PubMed

Tews, I., Findeisen, F., Sinning, I., Schultz, A., Schultz, J.E., and Linder, J.U. (2005). The structure of a pH-sensing mycobacterial adenylyl cyclase holoenzyme. Science308, 1020–1023.10.1126/science.1107642Search in Google Scholar PubMed

Winkler, W.C. (2005). Metabolic monitoring by bacterial mRNAs. Arch. Microbiol.183, 151–159.10.1007/s00203-005-0758-9Search in Google Scholar PubMed

Yamanaka, K., Mitta, M., and Inouye, M. (1999). Mutation analysis of the 5′ untranslated region of the cold shock cspA mRNA of Escherichia coli. J. Bacteriol.181, 6284–6291.10.1128/JB.181.20.6284-6291.1999Search in Google Scholar PubMed PubMed Central

Yura, T., Kanemori, M., and Morita, M. (2000). The heat shock response: regulation and function. In: Bacterial Stress Responses, R. Hengge-Aronis and G. Storz, eds. (Washington, DC, USA: ASM Press), pp. 3–18.Search in Google Scholar

Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res.31, 3406–3415.10.1093/nar/gkg595Search in Google Scholar PubMed PubMed Central

Published Online: 2005-12-09
Published in Print: 2005-12-01

©2005 by Walter de Gruyter Berlin New York

Downloaded on 24.4.2024 from https://www.degruyter.com/document/doi/10.1515/BC.2005.145/html
Scroll to top button