Skip to main content
Log in

Temperature Matters: Bacterial Response to Temperature Change

  • Review
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Temperature is one of the most important factors in all living organisms for survival. Being a unicellular organism, bacterium requires sensitive sensing and defense mechanisms to tolerate changes in temperature. During a temperature shift, the structure and composition of various cellular molecules including nucleic acids, proteins, and membranes are affected. In addition, numerous genes are induced during heat or cold shocks to overcome the cellular stresses, which are known as heat- and cold-shock proteins. In this review, we describe the cellular phenomena that occur with temperature change and bacterial responses from a molecular perspective, mainly in Escherichia coli.

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. 3

Similar content being viewed by others

References

  • Abduljalil, J. M. (2018). Bacterial riboswitches and rna thermometers: Nature and contributions to pathogenesis. Non-coding RNA Research, 3, 54–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adnan, M., Morton, G., Singh, J., & Hadi, S. (2010). Contribution of rpoS and bolA genes in biofilm formation in Escherichia coli K-12 MG1655. Molecular and Cellular Biochemistry, 342, 207–213.

    Article  CAS  PubMed  Google Scholar 

  • Ahmad, I., Cimdins, A., Beske, T., & Römling, U. (2017). Detailed analysis of c-di-GMP mediated regulation of csgD expression in Salmonella typhimurium. BMC Microbiology, 17, 27.

    Article  PubMed  PubMed Central  Google Scholar 

  • Al-Husini, N., Tomares, D. T., Bitar, O., Childers, W. S., & Schrader, J. M. (2018). α-Proteobacterial RNA degradosomes assemble liquid-liquid phase-separated RNP bodies. Molecular Cell, 71, 1027–1039.

    Article  CAS  PubMed  Google Scholar 

  • Alderson, T. R., Kim, J. H., & Markley, J. L. (2016). Dynamical structures of Hsp70 and Hsp70-Hsp40 complexes. Structure (London, England : 1993), 24, 1014–1030.

    Article  CAS  PubMed  Google Scholar 

  • Álvarez-Ordóñez, A., Fernández, A., López, M., Arenas, R., & Bernardo, A. (2008). Modifications in membrane fatty acid composition of Salmonella typhimurium in response to growth conditions and their effect on heat resistance. International Journal of Food Microbiology, 123, 212–219.

    Article  PubMed  Google Scholar 

  • Awano, N., Inouye, M., & Phadtare, S. (2008). RNase activity of polynucleotide phosphorylase is critical at low temperature in Escherichia coli and is complemented by RNase II. Journal of Bacteriology, 190, 5924–5933.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azaldegui, C. A., Vecchiarelli, A. G., & Biteen, J. S. (2021). The emergence of phase separation as an organizing principle in bacteria. Biophysical Journal, 120, 1123–1138.

    Article  CAS  PubMed  Google Scholar 

  • Balagopal, V., & Parker, R. (2009). Polysomes, P bodies and stress granules: States and fates of eukaryotic mRNAs. Current Opinion in Cell Biology, 21, 403–408.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balchin, D., Hayer-Hartl, M., & Hartl, F. U. (2016). In vivo aspects of protein folding and quality control. Science, 353, aac4354.

    Article  PubMed  Google Scholar 

  • Banani, S. F., Lee, H. O., Hyman, A. A., & Rosen, M. K. (2017). Biomolecular condensates: Organizers of cellular biochemistry. Nature Reviews Molecular Cell Biology, 18, 285–298.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Battesti, A., Majdalani, N., & Gottesman, S. (2011). The RpoS-mediated general stress response in Escherichia coli. Annual Review of Microbiology, 65, 189–213.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bayas, C. A., Wang, J., Lee, M. K., Schrader, J. M., Shapiro, L., & Moerner, W. (2018). Spatial organization and dynamics of RNase E and ribosomes in Caulobacter crescentus. Proceedings of the National Academy of Sciences of the United States of America, 115, E3712–E3721.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bittner, L. M., Arends, J., & Narberhaus, F. (2017). When, how and why? Regulated proteolysis by the essential ftsh protease in Escherichia coli. Biological Chemistry, 398, 625–635.

    Article  CAS  PubMed  Google Scholar 

  • Bogdanov, M., Pyrshev, K., Yesylevskyy, S., Ryabichko, S., Boiko, V., Ivanchenko, P., Kiyamova, R., Guan, Z., Ramseyer, C., & Dowhan, W. (2020). Phospholipid distribution in the cytoplasmic membrane of Gram-negative bacteria is highly asymmetric, dynamic, and cell shape-dependent. Science Advances, 6, eaaz6333.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borowitzka, L. J. (1981). Solute accumulation and regulation of cell water. In L. G. Paleg, & D. Aspinall (Eds.), The physiology and biochemistry of Drought Resistance in plants (pp. 97–130). Sydney, Australia: Academic Press.

    Google Scholar 

  • Brangwynne, C. P., Eckmann, C. R., Courson, D. S., Rybarska, A., Hoege, C., Gharakhani, J., Jülicher, F., & Hyman, A. A. (2009). Germline P granules are liquid droplets that localize by controlled dissolution / condensation. Science, 324, 1729–1732.

    Article  CAS  PubMed  Google Scholar 

  • Brockwell, D. J., & Radford, S. E. (2007). Intermediates: Ubiquitous species on folding energy landscapes? Current Opinion in Structural Biology, 17, 30–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Budiman, C., Koga, Y., Takano, K., & Kanaya, S. (2011). FK506-binding protein 22 from a psychrophilic bacterium, a cold shock-inducible peptidyl prolyl isomerase with the ability to assist in protein folding. International Journal of Molecular Sciences, 12, 5261–5284.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calloni, G., Chen, T., Schermann, S. M., Chang, H. C., Genevaux, P., Agostini, F., Tartaglia, G. G., Hayer-Hartl, M., & Hartl, F. U. (2012). DnaK functions as a central hub in the E. coli chaperone network. Cell Reports, 1, 251–264.

    Article  CAS  PubMed  Google Scholar 

  • Cezairliyan, B. O., & Sauer, R. T. (2007). Inhibition of regulated proteolysis by RseB. Proceedings of the National Academy of Sciences of the United States of America, 104, 3771–3776.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaba, R., Grigorova, I. L., Flynn, J. M., Baker, T. A., & Gross, C. A. (2007). Design principles of the proteolytic cascade governing the σE -mediated envelope stress response in Escherichia coli: Keys to graded, buffered, and rapid signal transduction. Genes & Development, 21, 124–136.

    Article  CAS  Google Scholar 

  • Charollais, J., Dreyfus, M., & Iost, I. (2004). CsdA, a cold-shock RNA helicase from Escherichia coli, is involved in the biogenesis of 50S ribosomal subunit. Nucleic Acids Research, 32, 2751–2759.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Csonka, L. N. (1989). Physiological and genetic responses of bacteria to osmotic stress. Microbiological Reviews, 53, 121–147.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Danese, P. N., Pratt, L. A., Dove, S. L., & Kolter, R. (2000). The outer membrane protein, antigen 43, mediates cell-to‐cell interactions within Escherichia coli biofilms. Molecular Microbiology, 37, 424–432.

    Article  CAS  PubMed  Google Scholar 

  • Dartigalongue, C., Missiakas, D., & Raina, S. (2001). Characterization of the Escherichia coli σE regulon. Journal of Biological Chemistry, 276, 20866–20875.

    Article  CAS  PubMed  Google Scholar 

  • Dash, S., Palma, C. S., Baptista, I. S., Almeida, B. L., Bahrudeen, M. N., Chauhan, V., Jagadeesan, R., & Ribeiro, A. S. (2022). Alteration of DNA supercoiling serves as a trigger of short-term cold shock repressed genes of E. coli. Nucleic Acids Research, 50, 8512–8528.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Maio, A., & Hightower, L. (2021). The interaction of heat shock proteins with cellular membranes: A historical perspective. Cell Stress and Chaperones, 26, 769–783.

    Article  PubMed  PubMed Central  Google Scholar 

  • Deuerling, E., Patzelt, H., Vorderwülbecke, S., Rauch, T., Kramer, G., Schaffitzel, E., Mogk, A., Schulze-Specking, A., Langen, H., & Bukau, B. (2003). Trigger factor and DnaK possess overlapping substrate pools and binding specificities. Molecular Microbiology, 47, 1317–1328.

    Article  CAS  PubMed  Google Scholar 

  • Deville, C., Carroni, M., Franke, K. B., Topf, M., Bukau, B., Mogk, A., & Saibil, H. R. (2017). Structural pathway of regulated substrate transfer and threading through an Hsp100 disaggregase. Science Advances, 3, e1701726.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dorman, C. J., & Corcoran, C. P. (2009). Bacterial DNA topology and infectious disease. Nucleic Acids Research, 37, 672–678.

    Article  CAS  PubMed  Google Scholar 

  • Doyle, M. P., & Schoeni, J. L. (1984). Survival and growth characteristics of Escherichia coli associated with hemorrhagic colitis. Applied and Environmental Microbiology, 48, 855–856.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ellis, R. J., & Van der Vies, S. M. (1991). Molecular chaperones. Annual Review of Biochemistry, 60, 321–347.

    Article  CAS  PubMed  Google Scholar 

  • Farewell, A., & Neidhardt, F. C. (1998). Effect of temperature on in vivo protein synthetic capacity in Escherichia coli. Journal of Bacteriology, 180, 4704–4710.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feller, G. (2018). Protein folding at extreme temperatures: Current issues. Seminars in Cell & Developmental Biology, 84, 129–137.

    Article  CAS  Google Scholar 

  • Feller, G., & Gerday, C. (2003). Psychrophilic enzymes: Hot topics in cold adaptation. Nature Reviews Microbiology, 1, 200–208.

    Article  CAS  PubMed  Google Scholar 

  • Galinski, E. A., & Trüper, H. G. (1994). Microbial behaviour in salt-stressed ecosystems. FEMS Microbiology Reviews, 15, 95–108.

    Article  CAS  Google Scholar 

  • Gamer, J., Bujard, H., & Bukau, B. (1992). Physical interaction between heat shock proteins DnaK, DnaJ, and GrpE and the bacterial heat shock transcription factor σ32. Cell, 69, 833–842.

    Article  CAS  PubMed  Google Scholar 

  • Genevaux, P., Keppel, F., Schwager, F., Langendijk-Genevaux, P. S., Hartl, F. U., & Georgopoulos, C. (2004). In vivo analysis of the overlapping functions of DnaK and trigger factor. EMBO Reports, 5, 195–200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giuliodori, A. M., Di Pietro, F., Marzi, S., Masquida, B., Wagner, R., Romby, P., Gualerzi, C. O., & Pon, C. L. (2010). The cspA mRNA is a thermosensor that modulates translation of the cold-shock protein CspA. Molecular Cell, 37, 21–33.

    Article  CAS  PubMed  Google Scholar 

  • Goldberg, A. L., Moerschell, R. P., Hachung, C., & Maurizi, M. R. (1994). ATP-dependent protease La (Lon) from Escherichia coli. Methods in Enzymology, 244, 350–375.

    Article  CAS  PubMed  Google Scholar 

  • Grigorova, I. L., Chaba, R., Zhong, H. J., Alba, B. M., Rhodius, V., Herman, C., & Gross, C. A. (2004). Fine-tuning of the Escherichia coli σE envelope stress response relies on multiple mechanisms to inhibit signal-independent proteolysis of the transmembrane anti-sigma factor, RseA. Genes & Development, 18, 2686–2697.

    Article  CAS  Google Scholar 

  • Grossman, A. D., Straus, D. B., Walter, W. A., & Gross, C. A. (1987). σ32 synthesis can regulate the synthesis of heat shock proteins in Escherichia coli. Genes & Development, 1, 179–184.

    Article  CAS  Google Scholar 

  • Gruber, T. M., & Gross, C. A. (2003). Multiple sigma subunits and the partitioning of bacterial transcription space. Annual Review of Microbiology, 57, 441–466.

    Article  CAS  PubMed  Google Scholar 

  • Gualdi, L., Tagliabue, L., Bertagnoli, S., Ieranò, T., De Castro, C., & Landini, P. (2008). Cellulose modulates biofilm formation by counteracting curli-mediated colonization of solid surfaces in Escherichia coli. Microbiology, 154, 2017–2024.

    Article  CAS  PubMed  Google Scholar 

  • Gualerzi, C. O., Giuliodori, A. M., & Pon, C. L. (2003). Transcriptional and post-transcriptional control of cold-shock genes. Journal of Molecular Biology, 331, 527–539.

    Article  CAS  PubMed  Google Scholar 

  • Guisbert, E., Herman, C., Lu, C. Z., & Gross, C. A. (2004). A chaperone network controls the heat shock response in E. coli. Genes & Development, 18, 2812–2821.

    Article  CAS  Google Scholar 

  • Gur, E., Biran, D., & Ron, E. Z. (2011). Regulated proteolysis in Gram-negative bacteria-how and when? Nature Reviews Microbiology, 9, 839–848.

    Article  CAS  PubMed  Google Scholar 

  • Gur, E., Ottofueling, R., & Dougan, D. A. (2013). Machines of Destruction – AAA + Proteases and the Adaptors that control them. In D. Dougan (Ed.), Regulated Proteolysis in Microorganisms. Subcellular biochemistry (66 vol.). Dordrecht, Netherlands: Springer.

    Google Scholar 

  • Harris, S. F., Shiau, A. K., & Agard, D. A. (2004). The crystal structure of the carboxy-terminal dimerization domain of htpG the Escherichia coli Hsp90, reveals a potential substrate binding site. Structure (London, England : 1993), 12, 1087–1097.

    Article  CAS  PubMed  Google Scholar 

  • Haslbeck, M., & Vierling, E. (2015). A first line of stress defense: Small heat shock proteins and their function in protein homeostasis. Journal of Molecular Biology, 427, 1537–1548.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Helmann, J. D. (2002). The extracytoplasmic function (ECF) sigma factors. Advances in Microbial Physiology, 46, 47–110.

    Article  CAS  PubMed  Google Scholar 

  • Hengge-Aronis, R., Klein, W., Lange, R., Rimmele, M., & Boos, W. (1991). Trehalose synthesis genes are controlled by the putative sigma factor encoded by rpoS and are involved in stationary-phase thermotolerance in Escherichia coli. Journal of Bacteriology, 173, 7918–7924.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herendeen, S. L., VanBogelen, R. A., & Neidhardt, F. C. (1979). Levels of major proteins of Escherichia coli during growth at different temperatures. Journal of Bacteriology, 139, 185–194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hlaváček, O., & Váchová, L. (2002). ATP-dependent proteinases in bacteria. Folia Microbiologica, 47, 203–212.

    Article  PubMed  Google Scholar 

  • Horváth, I., Multhoff, G., Sonnleitner, A., & Vígh, L. (2008). Membrane-associated stress proteins: More than simply chaperones. Biochimica et Biophysica Acta, 1778, 1653–1664.

    Article  PubMed  Google Scholar 

  • Horwich, A. L., Farr, G. W., & Fenton, W. A. (2006). GroEL – GroES-mediated protein folding. Chemical Reviews, 106, 1917–1930.

    Article  CAS  PubMed  Google Scholar 

  • Hsieh, L. S., Burger, R. M., & Drlica, K. (1991). Bacterial DNA supercoiling and [ATP][ADP]: Changes associated with a transition to anaerobic growth. Journal of Molecular Biology, 219, 443–450.

    Article  CAS  PubMed  Google Scholar 

  • Ivancic, T., Jamnik, P., & Stopar, D. (2013). Cold shock CspA and CspB protein production during periodic temperature cycling in Escherichia coli. BMC Research Notes, 6, 248.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Izutsu, K., Wada, C., Komine, Y., Sako, T., Ueguchi, C., Nakura, S., & Wada, A. (2001). Escherichia coli ribosome-associated protein SRA, whose copy number increases during stationary phase. Journal of Bacteriology, 183, 2765–2773.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jain, R., & Chan, M. K. (2007). Support for a potential role of E. coli oligopeptidase A in protein degradation. Biochemical and Biophysical Research Communications, 359, 486–490.

    Article  CAS  PubMed  Google Scholar 

  • Kamal, S. M., Simpson, D. J., Wang, Z., Gänzle, M., & Römling, U. (2021). Horizontal transmission of stress resistance genes shape the ecology of beta-and gamma-proteobacteria. Frontiers in Microbiology, 12, 696522.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kandror, O., DeLeon, A., & Goldberg, A. L. (2002). Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proceedings of the National Academy of Sciences of the USA, 99, 9727–9732.

  • Kandror, O., & Goldberg, A. L. (1997). Trigger factor is induced upon cold shock and enhances viability of Escherichia coli at low temperatures. Proceedings of the National Academy of Sciences of the USA, 94, 4978–4981.

  • Kanehara, K., Ito, K., & Akiyama, Y. (2002). YaeL (EcfE) activates the σE pathway of stress response through a site-2 cleavage of anti-σE, RseA. Genes and Development, 16, 2147–2155.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanemori, M., Nishihara, K., Yanagi, H., & Yura, T. (1997). Synergistic roles of HslVU and other ATP-dependent proteases in controlling in vivo turnover of σ32 and abnormal proteins in Escherichia coli. Journal of Bacteriology, 179, 7219–7225.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kataoka, K., Mizushima, T., Ogata, Y., Miki, T., & Sekimizu, K. (1996). Heat shock-induced DNA relaxation in vitro by DNA gyrase of Escherichia coli in the presence of ATP. Journal of Biological Chemistry, 271, 24806–24810.

    Article  CAS  PubMed  Google Scholar 

  • Katikaridis, P., Römling, U., & Mogk, A. (2021). Basic mechanism of the autonomous ClpG disaggregase. Journal of Biological Chemistry, 296, 100460.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kazmierczak, M. J., Wiedmann, M., & Boor, K. J. (2005). Alternative sigma factors and their roles in bacterial virulence. Microbiology and Molecular Biology Reviews, 69, 527–543.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keenleyside, W. (2019). Microbiology: Canadian Edition PressBooks. Available online: https://doi.org/https://ecampusontario.pressbooks.pub / microbio/ (accessed on 20 August 2020).

  • Kent, B., Hunt, T., Darwish, T. A., Hauß, T., Garvey, C. J., & Bryant, G. (2014). Localization of trehalose in partially hydrated DOPC bilayers: Insights into cryoprotective mechanisms. Journal of the Royal Society Interface, 11, 20140069.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim, Y. E., Hipp, M. S., Bracher, A., Hayer-Hartl, M., & Hartl, U., F (2013). Molecular chaperone functions in protein folding and proteostasis. Annual Review of Biochemistry, 82, 323–355.

    Article  CAS  PubMed  Google Scholar 

  • Kirstein, J., Molière, N., Dougan, D. A., & Turgay, K. (2009). Adapting the machine: Adaptor proteins for Hsp100 / Clp and AAA + proteases. Nature Reviews Microbiology, 7, 589–599.

    Article  CAS  PubMed  Google Scholar 

  • Kortmann, J., & Narberhaus, F. (2012). Bacterial RNA thermometers: Molecular zippers and switches. Nature Reviews Microbiology, 10, 255–265.

    Article  CAS  PubMed  Google Scholar 

  • Kortmann, J., Sczodrok, S., Rinnenthal, J., Schwalbe, H., & Narberhaus, F. (2011). Translation on demand by a simple RNA-based thermosensor. Nucleic Acids Research, 39, 2855–2868.

    Article  CAS  PubMed  Google Scholar 

  • Krajewski, S. S., Nagel, M., & Narberhaus, F. (2013). Short ROSE-like RNA thermometers control IbpA synthesis in Pseudomonas species. Plos One, 8, e65168.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lüders, S., Fallet, C., & Franco-Lara, E. (2009). Proteome analysis of the Escherichia coli heat shock response under steady-state conditions. Proteome Science, 7, 36.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lai, D., Proctor, J. R., & Meyer, I. M. (2013). On the importance of cotranscriptional RNA structure formation. Rna, 19, 1461–1473.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laskowska, E., Kuczyńska-Wiśnik, D., Skórko‐Glonek, J., & Taylor, A. (1996). Degradation by proteases Lon, Clp and HtrA, of Escherichia coli proteins aggregated in vivo by heat shock; HtrA protease action in vivo and in vitro. Molecular Microbiology, 22, 555–571.

    Article  CAS  PubMed  Google Scholar 

  • Lee, C., Franke, K. B., Kamal, S. M., Kim, H., Lünsdorf, H., Jäger, J., Nimtz, M., Trček, J., Jänsch, L., Bukau, B. (2018). Stand-alone ClpG disaggregase confers superior heat tolerance to bacteria. Proceedings of the National Academy of Sciences of the USA, 115, E273–E282.

  • Lee, C., Wigren, E., Lünsdorf, H., & Römling, U. (2016). Protein homeostasis-more than resisting a hot bath. Current Opinion in Microbiology, 30, 147–154.

    Article  CAS  PubMed  Google Scholar 

  • Leonarski, F., Jasiński, M., & Trylska, J. (2019). Thermodynamics of the fourU RNA thermal switch derived from molecular dynamics simulations and spectroscopic techniques. Biochimie, 156, 22–32.

    Article  PubMed  Google Scholar 

  • Lin, Y., Protter, D. S., Rosen, M. K., & Parker, R. (2015). Formation and maturation of phase-separated liquid droplets by RNA-binding proteins. Molecular Cell, 60, 208–219.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lins, R. D., Pereira, C. S., & Hünenberger, P. H. (2004). Trehalose–protein interaction in aqueous solution. Proteins: Structure Function and Bioinformatics, 55, 177–186.

    Article  CAS  Google Scholar 

  • MacCready, J. S., Basalla, J. L., & Vecchiarelli, A. G. (2020). Origin and evolution of carboxysome positioning systems in cyanobacteria. Molecular Biology and Evolution, 37, 1434–1451.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Macek, B., Forchhammer, K., Hardouin, J., Weber-Ban, E., Grangeasse, C., & Mijakovic, I. (2019). Protein post-translational modifications in bacteria. Nature Reviews Microbiology, 17, 651–664.

    Article  CAS  PubMed  Google Scholar 

  • Majdalani, N., Cunning, C., Sledjeski, D., Elliott, T., & Gottesman, S. (1998). DsrA RNA regulates translation of RpoS message by an anti-antisense mechanism, independent of its action as an antisilencer of transcription. Proceedings of the National Academy of Sciences of the USA, 95, 12462–12467.

  • Mansilla, M. C., Cybulski, L. E., Albanesi, D., & de Mendoza, D. (2004). Control of membrane lipid fluidity by molecular thermosensors. Journal of Bacteriology, 186, 6681–6688.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marbouty, M., Le Gall, A., Cattoni, D. I., Cournac, A., Koh, A., Fiche, J. B., Mozziconacci, J., Murray, H., Koszul, R., & Nollmann, M. (2015). Condensin-and replication-mediated bacterial chromosome folding and origin condensation revealed by Hi-C and super-resolution imaging. Molecular Cell, 59, 588–602.

    Article  CAS  PubMed  Google Scholar 

  • Martinez, A., & Kolter, R. (1997). Protection of DNA during oxidative stress by the nonspecific DNA-binding protein dps. Journal of Bacteriology, 179, 5188–5194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mashaghi, A., Kramer, G., Bechtluft, P., Zachmann-Brand, B., Driessen, A. J., Bukau, B., & Tans, S. J. (2013). Reshaping of the conformational search of a protein by the chaperone trigger factor. Nature, 500, 98–101.

    Article  CAS  PubMed  Google Scholar 

  • Mayer, M. P., Rüdiger, S., & Bukau, B. (2000). Molecular basis for interactions of the DnaK chaperone with substrates. Biological Chemistry, 381, 877–885.

    Article  CAS  PubMed  Google Scholar 

  • Mecsas, J., Rouviere, P. E., Erickson, J. W., Donohue, T., & Gross, C. A. (1993). The activity of σE, an Escherichia coli heat-inducible σ-factor, is modulated by expression of outer membrane proteins. Genes and Development, 7, 2618–2628.

    Article  CAS  PubMed  Google Scholar 

  • Meyer, A. S., & Baker, T. A. (2011). Proteolysis in the Escherichia coli heat shock response: A player at many levels. Current Opinion in Microbiology, 14, 194–199.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyer, S., Carlson, P. D., & Lucks, J. B. (2017). Characterizing the structure–function relationship of a naturally occurring RNA thermometer. Biochemistry, 56, 6629–6638.

    Article  CAS  PubMed  Google Scholar 

  • Missiakas, D., Mayer, M. P., Lemaire, M., Georgopoulos, C., & Raina, S. (1997). Modulation of the Escherichia coli σE (RpoE) heat-shock transcription‐factor activity by the RseA, RseB and RseC proteins. Molecular Microbiology, 24, 355–371.

    Article  CAS  PubMed  Google Scholar 

  • Miyake, T., Araki, S., & Tsuchido, T. (1993). Synthesis and sedimentation of a subset of 15-kDa heat shock proteins in Escherichia coli cells recovering from sublethal heat stress. Bioscience Biotechnology and Biochemistry, 57, 578–583.

    Article  CAS  Google Scholar 

  • Mizushima, T., Kataoka, K., Ogata, Y., Inoue, R., & Sekimizu, K. (1997). Increase in negative supercoiling of plasmid DNA in Escherichia coli exposed to cold shock. Molecular Microbiology, 23, 381–386.

    Article  CAS  PubMed  Google Scholar 

  • Mogk, A., Bukau, B., & Kampinga, H. H. (2018). Cellular handling of protein aggregates by disaggregation machines. Molecular Cell, 69, 214–226.

    Article  CAS  PubMed  Google Scholar 

  • Mogk, A., Deuerling, E., Vorderwülbecke, S., Vierling, E., & Bukau, B. (2003). Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Molecular Microbiology, 50, 585–595.

    Article  CAS  PubMed  Google Scholar 

  • Mogk, A., Ruger-Herreros, C., & Bukau, B. (2019). Cellular functions and mechanisms of action of small heat shock proteins. Annual Review of Microbiology, 73, 89–110.

    Article  CAS  PubMed  Google Scholar 

  • Monterroso, B., Zorrilla, S., Sobrinos-Sanguino, M., Robles‐Ramos, M. A., López‐Álvarez, M., Margolin, W., Keating, C. D., & Rivas, G. (2019). Bacterial FtsZ protein forms phase‐separated condensates with its nucleoid‐associated inhibitor SlmA. EMBO Reports, 20, e45946.

    Article  PubMed  Google Scholar 

  • Morgan, G. J., Burkhardt, D. H., Kelly, J. W., & Powers, E. T. (2018). Translation efficiency is maintained at elevated temperature in Escherichia coli. Journal of Biological Chemistry, 293, 777–793.

    Article  CAS  PubMed  Google Scholar 

  • Morita, M., Kanemori, M., Yanagi, H., & Yura, T. (1999). Heat-induced synthesis of σ32 in Escherichia coli: Structural and functional dissection of rpoH mRNA secondary structure. Journal of Bacteriology, 181, 401–410.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neuwald, A. F., Aravind, L., Spouge, J. L., & Koonin, E. V. (1999). AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Research, 9, 27–43.

    Article  CAS  PubMed  Google Scholar 

  • Nickerson, C. A., & Achberger, E. C. (1995). Role of curved DNA in binding of Escherichia coli RNA polymerase to promoters. Journal of Bacteriology, 177, 5756–5761.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nikaido, H., & Vaara, M. (1985). Molecular basis of bacterial outer membrane permeability. Microbiological Reviews, 49, 1–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nilsson, O. B., Müller-Lucks, A., Kramer, G., Bukau, B., & von Heijne, G. (2016). Trigger factor reduces the force exerted on the nascent chain by a cotranslationally folding protein. Journal of Molecular Biology, 428, 1356–1364.

    Article  CAS  PubMed  Google Scholar 

  • Nyquist, K., & Martin, A. (2014). Marching to the beat of the ring: Polypeptide translocation by AAA + proteases. Trends in Biochemical Sciences, 39, 53–60.

    Article  CAS  PubMed  Google Scholar 

  • Ogata, Y., Mizushima, T., Kataoka, K., Miki, T., & Sekimizu, K. (1994). Identification of DNA topoisomerases involved in immediate and transient DNA relaxation induced by heat shock in Escherichia coli. Molecular and General Genetics, 244, 451–455.

    Article  CAS  PubMed  Google Scholar 

  • Oh, E., Becker, A. H., Sandikci, A., Huber, D., Chaba, R., Gloge, F., Nichols, R. J., Typas, A., Gross, C. A., Kramer, G., et al. (2011). Selective ribosome profiling reveals the cotranslational chaperone action of trigger factor in vivo. Cell, 147, 1295–1308.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phadtare, S., & Severinov, K. (2010). RNA remodeling and gene regulation by cold shock proteins. RNA Biology, 7, 788–795.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piette, F., D’Amico, S., Struvay, C., Mazzucchelli, G., Renaut, J., Tutino, M. L., Danchin, A., Leprince, P., & Feller, G. (2010). Proteomics of life at low temperatures: Trigger factor is the primary chaperone in the antarctic bacterium Pseudoalteromonas haloplanktis TAC125. Molecular Microbiology, 76, 120–132.

    Article  CAS  PubMed  Google Scholar 

  • Piette, F., Struvay, C., & Feller, G. (2011). The protein folding challenge in psychrophiles: Facts and current issues. Environmental Microbiology, 13, 1924–1933.

    Article  CAS  PubMed  Google Scholar 

  • Protter, D. S., Rao, B. S., Van Treeck, B., Lin, Y., Mizoue, L., Rosen, M. K., & Parker, R. (2018). Intrinsically disordered regions can contribute promiscuous interactions to RNP granule assembly. Cell Reports, 22, 1401–1412.

    Article  CAS  PubMed  Google Scholar 

  • Römling, U., Galperin, M. Y., & Gomelsky, M. (2013). Cyclic di-GMP: The first 25 years of a universal bacterial second messenger. Microbiology and Molecular Biology Reviews, 77, 1–52.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rhodius, V. A., Suh, W. C., Nonaka, G., West, J., & Gross, C. A. (2006). Conserved and variable functions of the σE stress response in related genomes. PLoS Biology, 4, e2.

    Article  PubMed  Google Scholar 

  • Riback, J. A., Katanski, C. D., Kear-Scott, J. L., Pilipenko, E. V., Rojek, A. E., Sosnick, T. R., & Drummond, D. A. (2017). Stress-triggered phase separation is an adaptive, evolutionarily tuned response. Cell, 168, 1028–1040.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rinnenthal, J., Klinkert, B., Narberhaus, F., & Schwalbe, H. (2011). Modulation of the stability of the Salmonella fouru-type RNA thermometer. Nucleic Acids Research, 39, 8258–8270.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rode, D. K., Singh, P. K., & Drescher, K. (2020). Multicellular and unicellular responses of microbial biofilms to stress. Biological Chemistry, 401, 1365–1374.

    Article  CAS  PubMed  Google Scholar 

  • Roncarati, D., & Scarlato, V. (2017). Regulation of heat-shock genes in bacteria: From signal sensing to gene expression output. FEMS Microbiology Reviews, 41, 549–574.

    Article  CAS  PubMed  Google Scholar 

  • Rosen, R., Biran, D., Gur, E., Becher, D., Hecker, M., & Ron, E. Z. (2002). Protein aggregation in Escherichia coli: Role of proteases. FEMS Microbiology Letters, 207, 9–12.

    Article  CAS  PubMed  Google Scholar 

  • Rosen, R., & Ron, E. Z. (2002). Proteome analysis in the study of the bacterial heat-shock response. Mass Spectrometry Reviews, 21, 244–265.

    Article  CAS  PubMed  Google Scholar 

  • Rosenzweig, R., Moradi, S., Zarrine-Afsar, A., Glover, J. R., & Kay, L. E. (2013). Unraveling the mechanism of protein disaggregation through a ClpB-DnaK interaction. Science, 339, 1080–1083.

    Article  CAS  PubMed  Google Scholar 

  • Rotanova, T. V., Botos, I., Melnikov, E. E., Rasulova, F., Gustchina, A., Maurizi, M. R., & Wlodawer, A. (2006). Slicing a protease: Structural features of the ATP-dependent lon proteases gleaned from investigations of isolated domains. Protein Science, 15, 1815–1828.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryals, J., Little, R., & Bremer, H. (1982). Temperature dependence of RNA synthesis parameters in Escherichia coli. Journal of Bacteriology, 151, 879–887.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santiago, M., Ramírez-Sarmiento, C. A., Zamora, R. A., & Parra, L. P. (2016). Discovery, molecular mechanisms, and industrial applications of cold-active enzymes. Frontiers in Microbiology, 7, 1408.

    Article  PubMed  PubMed Central  Google Scholar 

  • Santos, D., & De Almeida, D. F. (1975). Isolation and characterization of a new temperature-sensitive cell division mutant of Escherichia coli K-12. Journal of Bacteriology, 124, 1502–1507.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schimmel, P. R., & Söll, D. (1979). Aminoacyl-tRNA synthetases: General features and recognition of transfer RNAs. Annual Review of Biochemistry, 48, 601–648.

    Article  CAS  PubMed  Google Scholar 

  • Schmid, F. X., Mayr, L. M., Mücke, M., & Schönbrunner, E. R. (1993). Prolyl isomerases: Role in protein folding. Advances in Protein Chemistry, 44, 25–66.

    Article  CAS  PubMed  Google Scholar 

  • Schmidpeter, P. A., & Schmid, F. X. (2015). Prolyl isomerization and its catalysis in protein folding and protein function. Journal of Molecular Biology, 427, 1609–1631.

    Article  CAS  PubMed  Google Scholar 

  • Schumann, W. (1999). FtsH–a single-chain charonin? FEMS Microbiology Reviews, 23, 1–11.

    Article  CAS  PubMed  Google Scholar 

  • Seaver, L. C., & Imlay, J. A. (2001). Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. Journal of Bacteriology, 183, 7173–7181.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shah, P., & Gilchrist, M. A. (2010). Is thermosensing property of RNA thermometers unique? Plos One, 5, e11308.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sharma, P., Mondal, K., Kumar, S., Tamang, S., Najar, I. N., Das, S., & Thakur, N. (2022). RNA thermometers in bacteria: Role in thermoregulation. Biochimica et Biophysica Acta -Gene Regulatory Mechanisms, 1865, 194871.

    Article  CAS  PubMed  Google Scholar 

  • Sherman, M. Y., & Goldberg, A. L. (1993). Heat shock of Escherichia coli increases binding of DnaK (the Hsp70 homolog) to polypeptides by promoting its phosphorylation. Proceedings of the National Academy of Sciences of the USA, 90, 8648–8652.

  • Shi, L., Ravikumar, V., Derouiche, A., Macek, B., & Mijakovic, I. (2016). Tyrosine 601 of Bacillus subtilis DnaK undergoes phosphorylation and is crucial for chaperone activity and heat shock survival. Frontiers in Microbiology, 7, 533.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shires, K., & Steyn, L. (2001). The cold-shock stress response in Mycobacterium smegmatis induces the expression of a histone‐like protein. Molecular Microbiology, 39, 994–1009.

    Article  CAS  PubMed  Google Scholar 

  • Singh, B., & Gupta, R. S. (2009). Conserved inserts in the Hsp60 (GroEL) and Hsp70 (DnaK) proteins are essential for cellular growth. Molecular Genetics and Genomics, 281, 361–373.

    Article  CAS  PubMed  Google Scholar 

  • Sledjeski, D. D., Gupta, A., & Gottesman, S. (1996). The small RNA, dsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli. The EMBO Journal, 15, 3993–4000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soini, J., Falschlehner, C., Mayer, C., Böhm, D., Weinel, S., Panula, J., Vasala, A., & Neubauer, P. (2005). Transient increase of ATP as a response to temperature up-shift in Escherichia coli. Microbial Cell Factories, 4, 9.

    Article  PubMed  PubMed Central  Google Scholar 

  • Squires, C., & Squires, C. L. (1992). The clp proteins: Proteolysis regulators or molecular chaperones? Journal of Bacteriology, 174, 1081–1085.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun, Q., Fu, Y., & Wang, W. (2022). Temperature effects on hydrophobic interactions: Implications for protein unfolding. Chemical Physics, 559, 111550.

    Article  CAS  Google Scholar 

  • Tang, M., Waring, A. J., & Hong, M. (2007). Trehalose-protected lipid membranes for determining membrane protein structure and insertion. Journal of Magnetic Resonance, 184, 222–227.

    Article  CAS  PubMed  Google Scholar 

  • Tomoyasu, T., Gamer, J., Bukau, B., Kanemori, M., Mori, H., Rutman, A. J., Oppenheim, A. B., Yura, T., Yamanaka, K., & Niki, H. (1995). Escherichia coli FtsH is a membrane-bound, ATP‐dependent protease which degrades the heat‐shock transcription factor σ32. The EMBO Journal, 14, 2551–2560.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tomoyasu, T., Ogura, T., Tatsuta, T., & Bukau, B. (1998). Levels of DnaK and DnaJ provide tight control of heat shock gene expression and protein repair in Escherichia coli. Molecular Microbiology, 30, 567–581.

    Article  CAS  PubMed  Google Scholar 

  • Townsley, L., & Yildiz, F. H. (2015). Temperature affects c-di‐GMP signalling and biofilm formation in Vibrio cholerae. Environmental Microbiology, 17, 4290–4305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsvetkova, N. M., Horváth, I., Török, Z., Wolkers, W. F., Balogi, Z., Shigapova, N., Crowe, L. M., Tablin, F., Vierling, E., Crowe, J. H. (2002). Small heat-shock proteins regulate membrane lipid polymorphism. Proceedings of the National Academy of Sciences of the USA, 99, 13504–13509.

  • Valenti, A., Perugino, G., Rossi, M., & Ciaramella, M. (2011). Positive supercoiling in thermophiles and mesophiles: Of the good and evil. Biochemical Society Transactions, 39, 58–63.

    Article  CAS  PubMed  Google Scholar 

  • van der Laan, E., Killian, J. A., & de Kruijff, B. (2004). Nonbilayer lipids affect peripheral and integral membrane proteins via changes in the lateral pressure profile. BBA-Biomembranes, 1666, 275–288.

  • van der Does, C., Swaving, J., van Klompenburg, W., & Driessen, A. J. (2000). Non-bilayer lipids stimulate the activity of the reconstituted bacterial protein translocase. Journal of Biological Chemistry, 275, 2472–2478.

    Article  PubMed  Google Scholar 

  • Van Montfort, R., Slingsby, C., & Vierlingt, E. (2001). Structure and function of the small heat shock protein/α-crystallin family of molecular chaperones. Advances in Protein Chemistry, 59, 105–156.

    Article  PubMed  Google Scholar 

  • Wang, J. C. (1996). DNA topoisomerases. Annual Review of Biochemistry, 65, 635–692.

    Article  CAS  PubMed  Google Scholar 

  • Wang, H., Yan, X., Aigner, H., Bracher, A., Nguyen, N. D., Hee, W. Y., Long, B., Price, G. D., Hartl, F., & Hayer-Hartl, M. (2019). Rubisco condensate formation by CcmM in β-carboxysome biogenesis. Nature, 566, 131–135.

    Article  CAS  PubMed  Google Scholar 

  • Welsh, D. T. (2000). Ecological significance of compatible solute accumulation by micro-organisms: From single cells to global climate. FEMS Microbiology Reviews, 24, 263–290.

    Article  CAS  PubMed  Google Scholar 

  • White-Ziegler, C. A., Um, S., Pérez, N. M., Berns, A. L., Malhowski, A. J., & Young, S. (2008). Low temperature (23 °C) increases expression of biofilm-, cold-shock-and RpoS-dependent genes in Escherichia coli K-12. Microbiology, 154, 148–166.

    Article  CAS  PubMed  Google Scholar 

  • Wickner, S., Gottesman, S., Skowyra, D., Hoskins, J., McKenney, K., & Maurizi, M. R. (1994). A molecular chaperone, ClpA, functions like DnaK and DnaJ. Proceedings of the National Academy of Sciences of the USA, 91, 12218–12222.

  • Woo, H. J., Jiang, J., Lafer, E. M., & Sousa, R. (2009). ATP-induced conformational changes in Hsp70: Molecular dynamics and experimental validation of an in silico predicted conformation. Biochemistry, 48, 11470–11477.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Y., Khoo, W. J., Zheng, Q., Chung, H. J., & Yuk, H. G. (2014). Growth temperature alters Salmonella Enteritidis heat / acid resistance, membrane lipid composition and stress / virulence related gene expression. International Journal of Food Microbiology, 172, 102–109.

    Article  CAS  PubMed  Google Scholar 

  • Yuk, H. G., & Marshall, D. L. (2003). Heat adaptation alters Escherichia coli O157:H7 membrane lipid composition and verotoxin production. Applied and Environmental Microbiology, 69, 5115–5119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, Y., Burkhardt, D. H., Rouskin, S., Li, G. W., Weissman, J. S., & Gross, C. A. (2018). A stress response that monitors and regulates MRNA structure is central to cold shock adaptation. Molecular Cell, 70, 274–286.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, Y., & Gross, C. A. (2021). Cold shock response in bacteria. Annual Review of Genetics, 55, 377–400.

    Article  PubMed  Google Scholar 

  • Zhang, W., Sun, J., Cao, H., Tian, R., Cai, L., Ding, W., & Qian, P. Y. (2016). Post-translational modifications are enriched within protein functional groups important to bacterial adaptation within a deep-sea hydrothermal vent environment. Microbiome, 4, 49.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by a Korea Polar Research Institute (KOPRI) grant funded by the Ministry of Oceans and Fisheries (KOPRI project No. PE22900). Changhan Lee received funding from the National Research Foundation of Korea (NRF) funded by the Korean government (MSIT) (grant 2021R1C1C1011690), the Basic Science Research Program through the NRF funded by the Ministry of Education (grant 2021R1A6A1A10044950), and the new faculty research fund from Ajou University.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Hyunhee Kim or Changhan Lee.

Ethics declarations

Conflict of interest

The authors have no conflict of interest to report.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Seongjoon Moon, Soojeong Ham, Juwon Jeong and Heechan Ku  have contributed equally to this work.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moon, S., Ham, S., Jeong, J. et al. Temperature Matters: Bacterial Response to Temperature Change. J Microbiol. 61, 343–357 (2023). https://doi.org/10.1007/s12275-023-00031-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-023-00031-x

Keywords

Navigation