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. 2013 Feb 17;82(1):68–76. doi: 10.1134/S0026261713010062

Search for the new potential RNA thermometers in the genome of Salmonella enterica

O Yu Limanskaya 1,2,, L A Murtazaeva 3, A P Limanskii 1
PMCID: PMC7089039  PMID: 32214462

Abstract

Currently, a number of structurally and functionally different temperature-sensitive elements such as RNA thermometers which control a variety of biological processes in bacteria, including virulence, are known. Based on computer and thermodynamic analysis of completely sequenced genomes of 25 Salmonella enterica isolates, the algorithm and criteria for the search of potential RNA thermometers were developed. It will make it possible to carry out the search for potential riboswitches in the genome of other socially important pathogens. For S. enterica, apart from the known 4U RNA thermometer, four hairpin-loop structures were identified which may probably act as additional RNA thermometers. They satisfy the necessary and sufficient conditions for formation of RNA thermometers and are highly conservative uncanonical structures, since these highly conservative structures were found in the genome of all 25 isolates of S. enterica. The hairpins forming a cruciform structure in the supercoiled pUC8 DNA were visualized by atomic force microscopy.

Keywords: RNA thermometer, Shine-Dalgarno sequence, hairpin structure, Salmonella enterica, AFM, atomic force microscopy

Footnotes

Original Russian Text © O.Yu. Limanskaya, L.A. Murtazaeva, A.P. Limanskii, 2013, published in Mikrobiologiya, 2013, Vol. 82, No. 1, pp. 69–78.

References

  • 1.Narberhaus F., Vogel J. Regulatory RNAs in Prokaryotes: Here, There and Everywhere. Mol. Microbiol. 2009;74(2):261–269. doi: 10.1111/j.1365-2958.2009.06869.x. [DOI] [PubMed] [Google Scholar]
  • 2.Klinkert B., Narberhaus F. Microbial Thermosensors. Cell Mol. Life Sci. 2009;66(16):2661–2676. doi: 10.1007/s00018-009-0041-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Morita M.T. Translational Induction of Heat Shock Transcription Factor r32: Evidence for a Built-in RNA Thermosensor. Genes Dev. 1999;13(6):655–665. doi: 10.1101/gad.13.6.655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Lybecker M.C., Samuels D.S. Temperature-Induced Regulation of RpoS by a Small RNA in Borrelia burgdorferi. Mol. Microbiol. 2007;64(4):1075–1089. doi: 10.1111/j.1365-2958.2007.05716.x. [DOI] [PubMed] [Google Scholar]
  • 5.Waldminghaus T., Fippinger A., Alfsmann J., Narberhaus F. RNA Thermometers Are Common in Alpha- and Gamma-Proteobacteria. Biol. Chem. 2005;386(12):1279–1286. doi: 10.1515/BC.2005.145. [DOI] [PubMed] [Google Scholar]
  • 6.Waldminghaus T., Heidrich N., Brantl S., Narberhaus F. FourU: A Novel Type of RNA Thermometer in Salmonella. Mol. Microbiol. 2007;65(2):413–424. doi: 10.1111/j.1365-2958.2007.05794.x. [DOI] [PubMed] [Google Scholar]
  • 7.Hoe N.P., Goguen J.D. Temperature Sensing in Yersinia pestis: Translation of the LcrF Activator Protein Is Thermally Regulated. J. Bacteriol. 1993;175(24):7901–7909. doi: 10.1128/jb.175.24.7901-7909.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Waldminghaus T., Gaubig L.C., Narberhaus F. Genome-Wide Bioinformatic Prediction and Experimental Evaluation of Potential RNA Thermometers. Mol. Genet. Genomics. 2007;278:555–564. doi: 10.1007/s00438-007-0272-7. [DOI] [PubMed] [Google Scholar]
  • 9.Neupert J., Karcher D., Bock R. Design of Simple Synthetic RNA Thermometers for Temperature-Controlled Gene Expression in Escherichia coli. Nucleic Acid Res. 2008;36(19):e124. doi: 10.1093/nar/gkn545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Wieland M., Hartig J.S. RNA Quadruplex-Based Modulation of Gene Expression. Chem. Biol. 2007;14(7):757–763. doi: 10.1016/j.chembiol.2007.06.005. [DOI] [PubMed] [Google Scholar]
  • 11.UNAFold: Software for Nucleic Acid Folding and Hybridization. http://mfold.bioinfo.rpi.edu/cgi-bin/rna-form1.cgi [DOI] [PubMed]
  • 12.Brodskii L.I., Drachev A.L., Tatuzov R.L., Chumakov K.M. GeneBee: a Package of Programs for Biopolymers Sequence Analysis. Biopol. Cell. 1991;7:10–14. [Google Scholar]
  • 13.Limanskaya O., Limanskii A. Imaging Compaction of Single Supercoiled DNA Molecules by Atomic Force Microscopy. Gen. Physiol. Biophys. 2008;27(4):322–337. [PubMed] [Google Scholar]
  • 14.Spirin A.S. Molekulyarnaya biologiya. Struktura ribosomy i biosintez belka. Moscow: Vysshaya Shkola; 1986. [Google Scholar]
  • 15.Chowdhury S., Maris C., Allain F., Narberhaus F. Molecular Basis for Temperature Sensing by an RNA Thermometer. EMBO J. 2006;25:2487–2497. doi: 10.1038/sj.emboj.7601128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Lilley D. Hairpin-Loop Formation by Inverted Repeats in Supercoiled DNA Molecules. Proc. Natl. Acad. Sci. U. S. A. 1980;77(11):6468–6472. doi: 10.1073/pnas.77.11.6468. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Sinden R., Pettijohn D. Cruciform Transitions in DNA. J. Biol. Chem. 1984;259(10):6593–6600. [PubMed] [Google Scholar]
  • 18.Lyamichev V., Panyutin I., Mirkin S. The Absence of Cruciform Structures from pAO3 Plasmid DNA in vivo. J. Biomol. Struct. Dyn. 1984;2(2):291–301. doi: 10.1080/07391102.1984.10507568. [DOI] [PubMed] [Google Scholar]
  • 19.Bevilacqua P., Blose J. Structures, Kinetics, Thermodynamics, and Biological Functions of RNA Hairpins. Ann. Rev. Phys. Chem. 2008;58:79. doi: 10.1146/annurev.physchem.59.032607.093743. [DOI] [PubMed] [Google Scholar]
  • 20.Cantor Ch., Schimmel P. Behavior of Biological Macromolecules, part 3. San Francisco: Freeman and Co.; 1980. [Google Scholar]
  • 21.Antao V., Tinoco I. Thermodynamic Parameters for Loop Formation in RNA and DNA Hairpin Tetraloops. Nucleic Acid Res. 1992;20(4):819. doi: 10.1093/nar/20.4.819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Panyutin, I., Lyamichev, V., and Lyubchenko, Y., A Sharp Structural Transition in pAO3 Plasmid DNA Caused by Increased Superhelix Density, FEBS Lett., 1982, vol. 148, no. 2. [DOI] [PubMed]
  • 23.Panyutin I., Klishko V., Lyamichev V. Kinetics of Cruciform Formation and Stability of Cruciform Structure in Superhelical DNA. J. Biomol. Struct. Dyn. 1984;1(4):1311–1324. doi: 10.1080/07391102.1984.10507522. [DOI] [PubMed] [Google Scholar]
  • 24.Zarudnaya M., Potyagailo A., Govorun D. Conservative Structural Motifs in the 3′ Untranslated Region of SARS Coronavirus. Biopol. Cell. 2003;19(3):298–303. [Google Scholar]
  • 25.Limanskii A.P. Visualization of Cruciform Structure in Supercoiled DNA by Atomic Force Microscopy. Biophysics. 2000;45(6):1007–1010. [PubMed] [Google Scholar]
  • 26.De Smit M., van Duin J. Secondary Structure of the Ribosome Binding Site Determines Translational Efficiency: A Quantitative Analysis. Proc. Natl. Acad. Sci. U. S. A. 1990;87:7668–7672. doi: 10.1073/pnas.87.19.7668. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Limanskaya O.Yu., Limanskii A.P. Imaging of T7 RNA Polymerase Elongation Complexes by Atomic Force Microscopy. Mol. Biol. 2008;42(3):469–477. doi: 10.1134/S0026893308030175. [DOI] [PubMed] [Google Scholar]
  • 28.Limanskaya L.A., Limanskii A.P. S-DNA, Oversupercoiled DNA with a 1.94- to 2.19-Pair. Mol. Biol. 2006;40(1):107–120. doi: 10.1134/S0026893306010158. [DOI] [PubMed] [Google Scholar]
  • 29.Limanskaya L.A., Limanskii A.P. Compaction of Single Supercoiled DNA Molecules Adsorbed onto Amino Mica. Russ. J. Bioorg. Chem. 2006;32(5):444–459. doi: 10.1134/S1068162006050074. [DOI] [PubMed] [Google Scholar]
  • 30.Johansson J., Mandin P., Renzoni A., Chlaruttini C., Springer M., Cossart P. An RNA Thermosensor Controls Expression of Virulence Genes in Listeria monocytogenes. Cell. 2002;110:551–561. doi: 10.1016/S0092-8674(02)00905-4. [DOI] [PubMed] [Google Scholar]

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