1932

Abstract

Bacteria often encounter temperature fluctuations in their natural habitats and must adapt to survive. The molecular response of bacteria to sudden temperature upshift or downshift is termed the heat shock response (HSR) or the cold shock response (CSR), respectively. Unlike the HSR, which activates a dedicated transcription factor that predominantly copes with heat-induced protein folding stress, the CSR is mediated by a diverse set of inputs. This review provides a picture of our current understanding of the CSR across bacteria. The fundamental aspects of CSR involved in sensing and adapting to temperature drop, including regulation of membrane fluidity, protein folding, DNA topology, RNA metabolism, and protein translation, are discussed. Special emphasis is placed on recent findings of a CSR circuitry in mediated by cold shock family proteins and RNase R that monitors and modulates messenger RNA structure to facilitate global translation recovery during acclimation.

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2021-11-23
2024-05-04
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Literature Cited

  1. 1. 
    Agafonov DE, Kolb VA, Nazimov IV, Spirin AS. 1999. A protein residing at the subunit interface of the bacterial ribosome. PNAS 96:2212345–49
    [Google Scholar]
  2. 2. 
    Agafonov DE, Kolb VA, Spirin AS. 2001. Ribosome-associated protein that inhibits translation at the aminoacyl-tRNA binding stage. EMBO Rep 2:5399–402
    [Google Scholar]
  3. 3. 
    Aguilar PS, Cronan JE Jr., de Mendoza D. 1998. A Bacillus subtilis gene induced by cold shock encodes a membrane phospholipid desaturase. J. Bacteriol. 180:82194–200
    [Google Scholar]
  4. 4. 
    Aguilar PS, Hernandez-Arriaga AM, Cybulski LE, Erazo AC, de Mendoza D. 2001. Molecular basis of thermosensing: a two-component signal transduction thermometer in Bacillus subtilis. EMBO J 20:71681–91
    [Google Scholar]
  5. 5. 
    Aguirre AA, Vicente AM, Hardwick SW, Alvelos DM, Mazzon RR et al. 2017. Association of the cold shock DEAD-box RNA helicase RhlE to the RNA degradosome in Caulobacter crescentus. J. Bacteriol. 199:13e00135-17
    [Google Scholar]
  6. 6. 
    Anderson KL, Roberts C, Disz T, Vonstein V, Hwang K et al. 2006. Characterization of the Staphylococcus aureus heat shock, cold shock, stringent, and SOS responses and their effects on log-phase mRNA turnover. J. Bacteriol. 188:196739–56
    [Google Scholar]
  7. 7. 
    Al-Fageeh MB, Smales CM. 2006. Control and regulation of the cellular responses to cold shock: the responses in yeast and mammalian systems. Biochem. J. 397:2247–59
    [Google Scholar]
  8. 8. 
    Araki T. 1991. The effect of temperature shifts on protein synthesis by the psychrophilic bacterium Vibrio sp. strain ANT-300. J. Gen. Microbiol. 137:4817–26
    [Google Scholar]
  9. 9. 
    Awano N, Rajagopal V, Arbing M, Patel S, Hunt J et al. 2010. Escherichia coli RNase R has dual activities, helicase and RNase. J. Bacteriol. 192:51344–52
    [Google Scholar]
  10. 10. 
    Awano N, Xu C, Ke H, Inoue K, Inouye M, Phadtare S. 2007. Complementation analysis of the cold-sensitive phenotype of the Escherichia coli csdA deletion strain. J. Bacteriol. 189:165808–15
    [Google Scholar]
  11. 11. 
    Bae W, Jones PG, Inouye M. 1997. CspA, the major cold shock protein of Escherichia coli, negatively regulates its own gene expression. J. Bacteriol. 179:227081–88
    [Google Scholar]
  12. 12. 
    Bae W, Xia B, Inouye M, Severinov K. 2000. Escherichia coli CspA-family RNA chaperones are transcription antiterminators. PNAS 97:147784–89
    [Google Scholar]
  13. 13. 
    Bayles DO, Annous BA, Wilkinson BJ. 1996. Cold stress proteins induced in Listeria monocytogenes in response to temperature downshock and growth at low temperatures. Appl. Environ. Microbiol. 62:31116–19
    [Google Scholar]
  14. 14. 
    Becker LA, Evans SN, Hutkins RW, Benson AK. 2000. Role of ςB in adaptation of Listeria monocytogenes to growth at low temperature. J. Bacteriol. 182:247083–87
    [Google Scholar]
  15. 15. 
    Beckering CL, Steil L, Weber MHW, Völker U, Marahiel MA. 2002. Genomewide transcriptional analysis of the cold shock response in Bacillus subtilis. J. Bacteriol. 184:226395–402
    [Google Scholar]
  16. 16. 
    Berger F, Morellet N, Menu F, Potier P. 1996. Cold shock and cold acclimation proteins in the psychrotrophic bacterium Arthrobacter globiformis SI55. J. Bacteriol. 178:112999–3007
    [Google Scholar]
  17. 17. 
    Brandi A, Pietroni P, Gualerzi CO, Pon CL. 1996. Post-transcriptional regulation of CspA expression in Escherichia coli. Mol. Microbiol. 19:2231–40
    [Google Scholar]
  18. 18. 
    Brandi A, Spurio R, Gualerzi CO, Pon CL. 1999. Massive presence of the Escherichia coli “major cold-shock protein” CspA under non-stress conditions. EMBO J 18:61653–59
    [Google Scholar]
  19. 19. 
    Bylund GO, Wipemo LC, Lundberg LA, Wikström PM. 1998. RimM and RbfA are essential for efficient processing of 16S rRNA in Escherichia coli. J. Bacteriol. 180:173–82
    [Google Scholar]
  20. 20. 
    Cairrão F, Cruz A, Mori H, Arraiano CM 2003. Cold shock induction of RNase R and its role in the maturation of the quality control mediator SsrA/tmRNA. Mol. Microbiol. 50:41349–60
    [Google Scholar]
  21. 21. 
    Carranza P, Grunau A, Schneider T, Hartmann I, Lehner A et al. 2010. A gel-free quantitative proteomics approach to investigate temperature adaptation of the food-borne pathogen Cronobacter turicensis 3032. Proteomics 10:183248–61
    [Google Scholar]
  22. 22. 
    Carty SM, Sreekumar KR, Raetz CR. 1999. Effect of cold shock on lipid A biosynthesis in Escherichia coli. Induction at 12 degrees C of an acyltransferase specific for palmitoleoyl-acyl carrier protein. J. Biol. Chem. 274:149677–85
    [Google Scholar]
  23. 23. 
    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 Res 32:92751–59
    [Google Scholar]
  24. 24. 
    Chattopadhyay MK, Jagannadham MV. 2001. Maintenance of membrane fluidity in Antarctic bacteria. Polar Biol 24:5386–88
    [Google Scholar]
  25. 25. 
    Chattopadhyay MK, Jagannadham MV, Vairamani M, Shivaji S. 1997. Carotenoid pigments of an Antarctic psychrotrophic bacterium Micrococcus roseus: temperature dependent biosynthesis, structure, and interaction with synthetic membranes. Biochem. Biophys. Res. Commun. 239:185–90
    [Google Scholar]
  26. 26. 
    Cheng Z-F, Deutscher MP. 2003. Quality control of ribosomal RNA mediated by polynucleotide phosphorylase and RNase R. PNAS 100:116388–93
    [Google Scholar]
  27. 27. 
    Court DL, Gan J, Liang Y-H, Shaw GX, Tropea JE et al. 2013. RNase III: genetics and function; structure and mechanism. Annu. Rev. Genet. 47:405–31
    [Google Scholar]
  28. 28. 
    Crooke E, Wickner W 1987. Trigger factor: a soluble protein that folds pro-OmpA into a membrane-assembly-competent form. PNAS 84:155216–20
    [Google Scholar]
  29. 29. 
    Cybulski LE, Martín M, Mansilla MC, Fernández A, de Mendoza D. 2010. Membrane thickness cue for cold sensing in a bacterium. Curr. Biol. 20:171539–44
    [Google Scholar]
  30. 30. 
    Dammel CS, Noller HF. 1995. Suppression of a cold-sensitive mutation in 16S rRNA by overexpression of a novel ribosome-binding factor, RbfA. Genes Dev 9:5626–37
    [Google Scholar]
  31. 31. 
    Datta PP, Bhadra RK. 2003. Cold shock response and major cold shock proteins of Vibrio cholerae. Appl. Environ. Microbiol. 69:116361–69
    [Google Scholar]
  32. 32. 
    Datta PP, Wilson DN, Kawazoe M, Swami NK, Kaminishi T et al. 2007. Structural aspects of RbfA action during small ribosomal subunit assembly. Mol. Cell 28:3434–45
    [Google Scholar]
  33. 33. 
    Dersch P, Kneip S, Bremer E 1994. The nucleoid-associated DNA-binding protein H-NS is required for the efficient adaptation of Escherichia coli K-12 to a cold environment. Mol. Gen. Genet. 245:2255–59
    [Google Scholar]
  34. 34. 
    D'Lima NG, Khitun A, Rosenbloom AD, Yuan P, Gassaway BM et al. 2017. Comparative proteomics enables identification of nonannotated cold shock proteins in E. coli. J. Proteome Res. 16:103722–31
    [Google Scholar]
  35. 35. 
    Eshwar AK, Guldimann C, Oevermann A, Tasara T 2017. Cold-shock domain family proteins (Csps) are involved in regulation of virulence, cellular aggregation, and flagella-based motility in Listeria monocytogenes. Front. Cell. Infect. Microbiol. 7:453
    [Google Scholar]
  36. 36. 
    Fang L, Jiang W, Bae W, Inouye M. 1997. Promoter-independent cold-shock induction of cspA and its derepression at 37°C by mRNA stabilization. Mol. Microbiol. 23:2355–64
    [Google Scholar]
  37. 37. 
    Feng Y, Huang H, Liao J, Cohen SN. 2001. Escherichia coli poly(A)-binding proteins that interact with components of degradosomes or impede RNA decay mediated by polynucleotide phosphorylase and RNase E. J. Biol. Chem. 276:3431651–56
    [Google Scholar]
  38. 38. 
    Fujita J. 1999. Cold shock response in mammalian cells. J. Mol. Microbiol. Biotechnol. 1:2243–55
    [Google Scholar]
  39. 39. 
    Garwin JL, Klages AL, Cronan JE Jr 1980. Beta-ketoacyl-acyl carrier protein synthase II of Escherichia coli. Evidence for function in the thermal regulation of fatty acid synthesis. J. Biol. Chem. 255:83263–65
    [Google Scholar]
  40. 40. 
    Garwin JL, Klages AL, Cronan JE Jr 1980. Structural, enzymatic, and genetic studies of beta-ketoacyl-acyl carrier protein synthases I and II of Escherichia coli. J. Biol. Chem. 255:2411949–56
    [Google Scholar]
  41. 41. 
    Giaever HM, Styrvold OB, Kaasen I, Strøm AR 1988. Biochemical and genetic characterization of osmoregulatory trehalose synthesis in Escherichia coli. J. Bacteriol. 170:62841–49
    [Google Scholar]
  42. 42. 
    Giangrossi M, Brandi A, Giuliodori AM, Gualerzi CO, Pon CL. 2007. Cold-shock-induced de novo transcription and translation of infA and role of IF1 during cold adaptation. Mol. Microbiol. 64:3807–21
    [Google Scholar]
  43. 43. 
    Giangrossi M, Giuliodori AM, Gualerzi CO, Pon CL. 2002. Selective expression of the β-subunit of nucleoid-associated protein HU during cold shock in Escherichia coli. Mol. Microbiol. 44:1205–16
    [Google Scholar]
  44. 44. 
    Giuliodori AM, Brandi A, Giangrossi M, Gualerzi CO, Pon CL. 2007. Cold-stress-induced de novo expression of infC and role of IF3 in cold-shock translational bias. RNA 13:81355–65
    [Google Scholar]
  45. 45. 
    Giuliodori AM, Di Pietro F, Marzi S, Masquida B, Wagner R et al. 2010. The cspA mRNA is a thermosensor that modulates translation of the cold-shock protein CspA. Mol. Cell 37:121–33
    [Google Scholar]
  46. 46. 
    Goldenberg D, Azar I, Oppenheim AB. 1996. Differential mRNA stability of the cspA gene in the cold-shock response of Escherichia coli. Mol. Microbiol. 19:2241–48
    [Google Scholar]
  47. 47. 
    Goldstein J, Pollitt NS, Inouye M. 1990. Major cold shock protein of Escherichia coli. PNAS 87:1283–87
    [Google Scholar]
  48. 48. 
    Grau R, Gardiol D, Glikin GC, de Mendoza D. 1994. DNA supercoiling and thermal regulation of unsaturated fatty acid synthesis in Bacillus subtilis. Mol. Microbiol. 11:5933–41
    [Google Scholar]
  49. 49. 
    Graumann P, Wendrich TM, Weber MH, Schröder K, Marahiel MA. 1997. A family of cold shock proteins in Bacillus subtilis is essential for cellular growth and for efficient protein synthesis at optimal and low temperatures. Mol. Microbiol. 25:4741–56
    [Google Scholar]
  50. 50. 
    Graumann P, Schröder K, Schmid R, Marahiel MA. 1996. Cold shock stress-induced proteins in Bacillus subtilis. J. Bacteriol. 178:154611–19
    [Google Scholar]
  51. 51. 
    Graumann P, Marahiel MA. 1998. A superfamily of proteins that contain the cold-shock domain. Trends Biochem. Sci. 23:8286–90
    [Google Scholar]
  52. 52. 
    Grothe S, Krogsrud RL, McClellan DJ, Milner JL, Wood JM. 1986. Proline transport and osmotic stress response in Escherichia coli K-12. J. Bacteriol. 166:1253–59
    [Google Scholar]
  53. 53. 
    Gualerzi CO, Giuliodori AM, Pon CL. 2003. Transcriptional and post-transcriptional control of cold-shock genes. J. Mol. Biol. 331:3527–39
    [Google Scholar]
  54. 54. 
    Gul N, Poolman B. 2013. Functional reconstitution and osmoregulatory properties of the ProU ABC transporter from Escherichia coli. Mol. Membr. Biol. 30:2138–48
    [Google Scholar]
  55. 55. 
    Guthrie C, Nashimoto H, Nomura M. 1969. Structure and function of E. coli ribosomes. 8. Cold-sensitive mutants defective in ribosome assembly. PNAS 63:2384–91
    [Google Scholar]
  56. 56. 
    Guy C. 1999. Molecular responses of plants to cold shock and cold acclimation. J. Mol. Microbiol. Biotechnol. 1:2231–42
    [Google Scholar]
  57. 57. 
    Hatfield GW, Benham CJ. 2002. DNA topology-mediated control of global gene expression in Escherichia coli. Annu. Rev. Genet. 36:175–203
    [Google Scholar]
  58. 58. 
    Hawkins JS, Silvis MR, Koo B-M, Peters JM, Osadnik H et al. 2020. Mismatch-CRISPRi reveals the co-varying expression-fitness relationships of essential genes in Escherichia coli and Bacillus subtilis. Cell Syst 11:5523–35.e9
    [Google Scholar]
  59. 59. 
    Hébraud M, Potier P. 1999. Cold shock response and low temperature adaptation in psychrotrophic bacteria. J. Mol. Microbiol. Biotechnol. 1:2211–19
    [Google Scholar]
  60. 60. 
    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. J. Bacteriol. 173:247918–24
    [Google Scholar]
  61. 61. 
    Herendeen SL, VanBogelen RA, Neidhardt FC. 1979. Levels of major proteins of Escherichia coli during growth at different temperatures. J. Bacteriol. 139:1185–94
    [Google Scholar]
  62. 62. 
    Hoffmann T, Bremer E. 2011. Protection of Bacillus subtilis against cold stress via compatible-solute acquisition. J. Bacteriol. 193:71552–62
    [Google Scholar]
  63. 63. 
    Hunger K, Beckering CL, Wiegeshoff F, Graumann PL, Marahiel MA. 2006. Cold-induced putative DEAD box RNA helicases CshA and CshB are essential for cold adaptation and interact with cold shock protein B in Bacillus subtilis. J. Bacteriol. 188:1240–48
    [Google Scholar]
  64. 64. 
    Ingolia NT, Ghaemmaghami S, Newman JRS, Weissman JS. 2009. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324:5924218–23
    [Google Scholar]
  65. 65. 
    Iost I, Bizebard T, Dreyfus M. 2013. Functions of DEAD-box proteins in bacteria: current knowledge and pending questions. Biochim. Biophys. Acta 1829:8866–77
    [Google Scholar]
  66. 66. 
    Izutsu K, Wada C, Komine Y, Sako T, Ueguchi C et al. 2001. Escherichia coli ribosome-associated protein SRA, whose copy number increases during stationary phase. J. Bacteriol. 183:92765–73
    [Google Scholar]
  67. 67. 
    Jagannadham MV, Chattopadhyay MK, Subbalakshmi C, Vairamani M, Narayanan K et al. 2000. Carotenoids of an Antarctic psychrotolerant bacterium, Sphingobacterium antarcticus, and a mesophilic bacterium, Sphingobacterium multivorum. Arch. Microbiol. 173:5–6418–24
    [Google Scholar]
  68. 68. 
    Jagessar KL, Jain C. 2010. Functional and molecular analysis of Escherichia coli strains lacking multiple DEAD-box helicases. RNA 16:71386–92
    [Google Scholar]
  69. 69. 
    Jiang W, Fang L, Inouye M. 1996. The role of the 5′-end untranslated region of the mRNA for CspA, the major cold-shock protein of Escherichia coli, in cold-shock adaptation. J. Bacteriol. 178:164919–25
    [Google Scholar]
  70. 70. 
    Jiang W, Hou Y, Inouye M. 1997. CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J. Biol. Chem. 272:1196–202
    [Google Scholar]
  71. 71. 
    Jones PG, Inouye M. 1996. RbfA, a 30S ribosomal binding factor, is a cold-shock protein whose absence triggers the cold-shock response. Mol. Microbiol. 21:61207–18
    [Google Scholar]
  72. 72. 
    Jones PG, Krah R, Tafuri SR, Wolffe AP. 1992. DNA gyrase, CS7.4, and the cold shock response in Escherichia coli. J. Bacteriol. 174:185798–802
    [Google Scholar]
  73. 73. 
    Jones PG, Mitta M, Kim Y, Jiang W, Inouye M. 1996. Cold shock induces a major ribosomal-associated protein that unwinds double-stranded RNA in Escherichia coli. PNAS 93:176–80
    [Google Scholar]
  74. 74. 
    Jones PG, VanBogelen RA, Neidhardt FC. 1987. Induction of proteins in response to low temperature in Escherichia coli. J. Bacteriol. 169:52092–95
    [Google Scholar]
  75. 75. 
    Jozefczuk S, Klie S, Catchpole G, Szymanski J, Cuadros-Inostroza A et al. 2010. Metabolomic and transcriptomic stress response of Escherichia coli. Mol. Syst. Biol. 6:364
    [Google Scholar]
  76. 76. 
    Kandror O, DeLeon A, Goldberg AL. 2002. Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. PNAS 99:159727–32
    [Google Scholar]
  77. 77. 
    Kandror O, Goldberg AL. 1997. Trigger factor is induced upon cold shock and enhances viability of Escherichia coli at low temperatures. PNAS 94:104978–81
    [Google Scholar]
  78. 78. 
    Katayama S, Matsushita O, Jung CM, Minami J, Okabe A. 1999. Promoter upstream bent DNA activates the transcription of the Clostridium perfringens phospholipase C gene in a low temperature-dependent manner. EMBO J. 18:123442–50
    [Google Scholar]
  79. 79. 
    Khemici V, Carpousis AJ. 2004. The RNA degradosome and poly(A) polymerase of Escherichia coli are required in vivo for the degradation of small mRNA decay intermediates containing REP-stabilizers. Mol. Microbiol. 51:3777–90
    [Google Scholar]
  80. 80. 
    Kim K-S, Manasherob R, Cohen SN 2008. YmdB: a stress-responsive ribonuclease-binding regulator of E. coli RNase III activity. Genes Dev 22:243497–508
    [Google Scholar]
  81. 81. 
    Klein W, Weber MH, Marahiel MA. 1999. Cold shock response of Bacillus subtilis: isoleucine-dependent switch in the fatty acid branching pattern for membrane adaptation to low temperatures. J. Bacteriol. 181:175341–49
    [Google Scholar]
  82. 82. 
    Ko R, Smith LT, Smith GM. 1994. Glycine betaine confers enhanced osmotolerance and cryotolerance on Listeria monocytogenes. J. Bacteriol. 176:2426–31
    [Google Scholar]
  83. 83. 
    Koo B-M, Kritikos G, Farelli JD, Todor H, Tong K et al. 2017. Construction and analysis of two genome-scale deletion libraries for Bacillus subtilis. Cell Syst 4:3291–305.e7
    [Google Scholar]
  84. 84. 
    Kramer G, Rauch T, Rist W, Vorderwülbecke S, Patzelt H et al. 2002. L23 protein functions as a chaperone docking site on the ribosome. Nature 419:6903171–74
    [Google Scholar]
  85. 85. 
    La Teana A, Brandi A, Falconi M, Spurio R, Pon CL, Gualerzi CO 1991. Identification of a cold shock transcriptional enhancer of the Escherichia coli gene encoding nucleoid protein H-NS. PNAS 88:2310907–11
    [Google Scholar]
  86. 86. 
    Lamark T, Kaasen I, Eshoo MW, Falkenberg P, McDougall J, Strøm AR. 1991. DNA sequence and analysis of the bet genes encoding the osmoregulatory choline–glycine betaine pathway of Escherichia coli. Mol. Microbiol. 5:51049–64
    [Google Scholar]
  87. 87. 
    Li G-W, Burkhardt D, Gross C, Weissman JS. 2014. Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157:3624–35
    [Google Scholar]
  88. 88. 
    Linder P, Lasko PF, Ashburner M, Leroy P, Nielsen PJ et al. 1989. Birth of the D-E-A-D box. Nature 337:6203121–22
    [Google Scholar]
  89. 89. 
    Liou G-G, Chang H-Y, Lin C-S, Lin-Chao S. 2002. DEAD box RhlB RNA helicase physically associates with exoribonuclease PNPase to degrade double-stranded RNA independent of the degradosome-assembling region of RNase E. J. Biol. Chem. 277:4341157–62
    [Google Scholar]
  90. 90. 
    Liu B, Zhang Y, Zhang W. 2014. RNA-Seq-based analysis of cold shock response in Thermoanaerobacter tengcongensis, a bacterium harboring a single cold shock protein encoding gene. PLOS ONE 9:3e93289
    [Google Scholar]
  91. 91. 
    Liu S, Bayles DO, Mason TM, Wilkinson BJ. 2006. A cold-sensitive Listeria monocytogenes mutant has a transposon insertion in a gene encoding a putative membrane protein and shows altered (p)ppGpp levels. Appl. Environ. Microbiol. 72:63955–59
    [Google Scholar]
  92. 92. 
    Los DA, Murata N. 1999. Responses to cold shock in cyanobacteria. J. Mol. Microbiol. Biotechnol. 1:2221–30
    [Google Scholar]
  93. 93. 
    Majdalani N, Chen S, Murrow J, St John K, Gottesman S. 2001. Regulation of RpoS by a novel small RNA: the characterization of RprA. Mol. Microbiol. 39:51382–94
    [Google Scholar]
  94. 94. 
    Martinez-Hackert E, Hendrickson WA 2009. Promiscuous substrate recognition in folding and assembly activities of the trigger factor chaperone. Cell 138:5923–34
    [Google Scholar]
  95. 95. 
    Matamouros S, Hayden HS, Hager KR, Brittnacher MJ, Lachance K et al. 2018. Adaptation of commensal proliferating Escherichia coli to the intestinal tract of young children with cystic fibrosis. PNAS 115:71605–10
    [Google Scholar]
  96. 96. 
    Mazzon RR, Lang EAS, Braz VS, Marques MV. 2008. Characterization of Caulobacter crescentus response to low temperature and identification of genes involved in freezing resistance. FEMS Microbiol. Lett. 288:2178–85
    [Google Scholar]
  97. 97. 
    McCullen CA, Benhammou JN, Majdalani N, Gottesman S 2010. Mechanism of positive regulation by DsrA and RprA small noncoding RNAs: pairing increases translation and protects rpoS mRNA from degradation. J. Bacteriol. 192:215559–71
    [Google Scholar]
  98. 98. 
    Merino EJ, Wilkinson KA, Coughlan JL, Weeks KM. 2005. RNA structure analysis at single nucleotide resolution by selective 2′-hydroxyl acylation and primer extension (SHAPE). J. Am. Chem. Soc. 127:124223–31
    [Google Scholar]
  99. 99. 
    Michel V, Lehoux I, Depret G, Anglade P, Labadie J, Hebraud M. 1997. The cold shock response of the psychrotrophic bacterium Pseudomonas fragi involves four low-molecular-mass nucleic acid-binding proteins. J. Bacteriol. 179:237331–42
    [Google Scholar]
  100. 100. 
    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. Mol. Microbiol. 23:2381–86
    [Google Scholar]
  101. 101. 
    Mogk A, Tomoyasu T, Goloubinoff P, Rüdiger S, Röder D et al. 1999. Identification of thermolabile Escherichia coli proteins: prevention and reversion of aggregation by DnaK and ClpB. EMBO J 18:246934–49
    [Google Scholar]
  102. 102. 
    Morgan GJ, Burkhardt DH, Kelly JW, Powers ET 2018. Translation efficiency is maintained at elevated temperature in Escherichia coli. J. Biol. Chem. 293:3777–93
    [Google Scholar]
  103. 103. 
    Ng H, Ingraham JL, Marr AG. 1962. Damage and derepression in Escherichia coli resulting from growth at low temperatures. J. Bacteriol. 84:331–39
    [Google Scholar]
  104. 104. 
    Nishida I, Murata N. 1996. Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:541–68
    [Google Scholar]
  105. 105. 
    Nunn BL, Slattery KV, Cameron KA, Timmins-Schiffman E, Junge K. 2015. Proteomics of Colwellia psychrerythraea at subzero temperatures—a life with limited movement, flexible membranes and vital DNA repair. Environ. Microbiol. 17:72319–35
    [Google Scholar]
  106. 106. 
    O'Farrell PH. 1975. High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250:104007–21
    [Google Scholar]
  107. 107. 
    Oh E, Becker AH, Sandikci A, Huber D, Chaba R et al. 2011. Selective ribosome profiling reveals the cotranslational chaperone action of trigger factor in vivo. Cell 147:61295–308
    [Google Scholar]
  108. 108. 
    Panoff J-M, Corroler D, Thammavongs B, Boutibonnes P. 1997. Differentiation between cold shock proteins and cold acclimation proteins in a mesophilic gram-positive bacterium, Enterococcus faecalis JH2-2. J. Bacteriol. 179:134451–54
    [Google Scholar]
  109. 109. 
    Panoff J-M, Legrand S, Thammavongs B, Boutibonnes P. 1994. The cold shock response in Lactococcuslactis subsp. lactis. Curr. Microbiol. 29:4213–16
    [Google Scholar]
  110. 110. 
    Phadtare S, Inouye M 1999. Sequence-selective interactions with RNA by CspB, CspC and CspE, members of the CspA family of Escherichia coli. Mol. Microbiol. 33:51004–14
    [Google Scholar]
  111. 111. 
    Phadtare S, Inouye M 2004. Genome-wide transcriptional analysis of the cold shock response in wild-type and cold-sensitive, quadruple-csp-deletion strains of Escherichia coli. J. Bacteriol. 186:207007–14
    [Google Scholar]
  112. 112. 
    Phadtare S, Inouye M, Severinov K. 2002. The nucleic acid melting activity of Escherichia coli CspE is critical for transcription antitermination and cold acclimation of cells. J. Biol. Chem. 277:97239–45
    [Google Scholar]
  113. 113. 
    Phadtare S, Severinov K 2005. Nucleic acid melting by Escherichia coli CspE. Nucleic Acids Res 33:175583–90
    [Google Scholar]
  114. 114. 
    Polissi A, De Laurentis W, Zangrossi S, Briani F, Longhi V et al. 2003. Changes in Escherichia coli transcriptome during acclimatization at low temperature. Res. Microbiol. 154:8573–80
    [Google Scholar]
  115. 115. 
    Porankiewicz J, Clarke AK. 1997. Induction of the heat shock protein ClpB affects cold acclimation in the cyanobacterium Synechococcus sp. strain PCC 7942. J. Bacteriol. 179:165111–17
    [Google Scholar]
  116. 116. 
    Porankiewicz J, Schelin J, Clarke AK. 1998. The ATP-dependent Clp protease is essential for acclimation to UV-B and low temperature in the cyanobacterium Synechococcus. Mol. Microbiol. 29:1275–83
    [Google Scholar]
  117. 117. 
    Prakash JSS, Sinetova M, Zorina A, Kupriyanova E, Suzuki I et al. 2009. DNA supercoiling regulates the stress-inducible expression of genes in the cyanobacterium Synechocystis. Mol. Biosyst. 5:121904–12
    [Google Scholar]
  118. 118. 
    Prud'homme-Généreux A, Beran RK, Iost I, Ramey CS, Mackie GA, Simons RW. 2004. Physical and functional interactions among RNase E, polynucleotide phosphorylase and the cold-shock protein, CsdA: evidence for a “cold shock degradosome. .” Mol. Microbiol. 54:51409–21
    [Google Scholar]
  119. 119. 
    Purusharth RI, Klein F, Sulthana S, Jäger S, Jagannadham MV et al. 2005. Exoribonuclease R interacts with endoribonuclease E and an RNA helicase in the psychrotrophic bacterium Pseudomonas syringae Lz4W. J. Biol. Chem. 280:1514572–78
    [Google Scholar]
  120. 120. 
    Repoila F, Gottesman S. 2001. Signal transduction cascade for regulation of RpoS: temperature regulation of DsrA. J. Bacteriol. 183:134012–23
    [Google Scholar]
  121. 121. 
    Richards J, Mehta P, Karzai AW. 2006. RNase R degrades non-stop mRNAs selectively in an SmpB-tmRNA-dependent manner. Mol. Microbiol. 62:61700–12
    [Google Scholar]
  122. 122. 
    Roberts ME, Inniss WE. 1992. The synthesis of cold shock proteins and cold acclimation proteins in the psychrophilic bacterium Aquaspirillum arcticum. Curr. Microbiol. 25:5275–78
    [Google Scholar]
  123. 123. 
    Rodrigues DF, Tiedje JM. 2008. Coping with our cold planet. Appl. Environ. Microbiol. 74:61677–86
    [Google Scholar]
  124. 124. 
    Rouskin S, Zubradt M, Washietl S, Kellis M, Weissman JS 2014. Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo. Nature 505:7485701–5
    [Google Scholar]
  125. 125. 
    Schärer K, Stephan R, Tasara T 2013. Cold shock proteins contribute to the regulation of listeriolysin O production in Listeria monocytogenes. Foodborne Pathog. Dis. 10:121023–29
    [Google Scholar]
  126. 126. 
    Schindelin H, Jiang W, Inouye M, Heinemann U. 1994. Crystal structure of CspA, the major cold shock protein of Escherichia coli. PNAS 91:115119–23
    [Google Scholar]
  127. 127. 
    Schmid B, Klumpp J, Raimann E, Loessner MJ, Stephan R, Tasara T 2009. Role of cold shock proteins in growth of Listeria monocytogenes under cold and osmotic stress conditions. Appl. Environ. Microbiol. 75:61621–27
    [Google Scholar]
  128. 128. 
    Seel W, Baust D, Sons D, Albers M, Etzbach L et al. 2020. Carotenoids are used as regulators for membrane fluidity by Staphylococcus xylosus. Sci. Rep. 10:1330
    [Google Scholar]
  129. 129. 
    Sharma IM, Woodson SA. 2020. RbfA and IF3 couple ribosome biogenesis and translation initiation to increase stress tolerance. Nucleic Acids Res 48:1359–72
    [Google Scholar]
  130. 130. 
    Shires K, Steyn L. 2001. The cold-shock stress response in Mycobacterium smegmatis induces the expression of a histone-like protein. Mol. Microbiol. 39:4994–1009
    [Google Scholar]
  131. 131. 
    Shiver AL, Osadnik H, Kritikos G, Li B, Krogan N et al. 2016. A chemical-genomic screen of neglected antibiotics reveals illicit transport of kasugamycin and blasticidin S. PLOS Genet 12:6e1006124
    [Google Scholar]
  132. 132. 
    Siegfried NA, Busan S, Rice GM, Nelson JAE, Weeks KM 2014. RNA motif discovery by SHAPE and mutational profiling (SHAPE-MaP). Nat. Methods 11:9959–65
    [Google Scholar]
  133. 133. 
    Sinensky M. 1974. Homeoviscous adaptation—a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. PNAS 71:2522–25
    [Google Scholar]
  134. 134. 
    Sledjeski DD, Gupta A, Gottesman S. 1996. The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli. EMBO J 15:153993–4000
    [Google Scholar]
  135. 135. 
    Sonna LA, Fujita J, Gaffin SL, Lilly CM. 2002. Invited review: effects of heat and cold stress on mammalian gene expression. J. Appl. Physiol. 92:41725–42
    [Google Scholar]
  136. 136. 
    Spaniol V, Wyder S, Aebi C 2013. RNA-Seq-based analysis of the physiologic cold shock-induced changes in Moraxella catarrhalis gene expression. PLOS ONE 8:7e68298
    [Google Scholar]
  137. 137. 
    Subczynski WK, Markowska E, Gruszecki WI, Sielewiesiuk J. 1992. Effects of polar carotenoids on dimyristoylphosphatidylcholine membranes: a spin-label study. Biochim. Biophys. Acta 1105:197–108
    [Google Scholar]
  138. 138. 
    Toone WM, Rudd KE, Friesen JD 1991. deaD, a new Escherichia coli gene encoding a presumed ATP-dependent RNA helicase, can suppress a mutation in rpsB, the gene encoding ribosomal protein S2. J. Bacteriol. 173:113291–302
    [Google Scholar]
  139. 139. 
    VanBogelen RA, Neidhardt FC. 1990. Ribosomes as sensors of heat and cold shock in Escherichia coli. PNAS 87:155589–93
    [Google Scholar]
  140. 140. 
    Vila-Sanjurjo A, Schuwirth B-S, Hau CW, Cate JHD. 2004. Structural basis for the control of translation initiation during stress. Nat. Struct. Mol. Biol. 11:111054–59
    [Google Scholar]
  141. 141. 
    Vorachek-Warren MK, Carty SM, Lin S, Cotter RJ, Raetz CRH. 2002. An Escherichia coli mutant lacking the cold shock-induced palmitoleoyltransferase of lipid A biosynthesis: absence of unsaturated acyl chains and antibiotic hypersensitivity at 12 degrees C. J. Biol. Chem. 277:1614186–93
    [Google Scholar]
  142. 142. 
    Wada A. 1986. Analysis of Escherichia coli ribosomal proteins by an improved two dimensional gel electrophoresis. II. Characterization of four new proteins. J. Biochem. 100:61595–605
    [Google Scholar]
  143. 143. 
    Wang W, Bechhofer DH 1996. Properties of a Bacillus subtilis polynucleotide phosphorylase deletion strain. J. Bacteriol. 178:82375–82
    [Google Scholar]
  144. 144. 
    Weber MHW, Marahiel MA. 2002. Coping with the cold: the cold shock response in the Gram-positive soil bacterium Bacillus subtilis. Philos. Trans. R. Soc. B 357: 1423.895–907
    [Google Scholar]
  145. 145. 
    Weber MHW, Marahiel MA. 2003. Bacterial cold shock responses. Sci. Prog. 86:1–29–75
    [Google Scholar]
  146. 146. 
    White-Ziegler CA, Um S, Pérez NM, Berns AL, Malhowski AJ, Young S. 2008. Low temperature (23 degrees C) increases expression of biofilm-, cold-shock- and RpoS-dependent genes in Escherichia coli K-12. Microbiology 154:1148–66
    [Google Scholar]
  147. 147. 
    Wouters JA, Rombouts FM, de Vos WM, Kuipers OP, Abee T 1999. Cold shock proteins and low-temperature response of Streptococcus thermophilus CNRZ302. Appl. Environ. Microbiol. 65:104436–42
    [Google Scholar]
  148. 148. 
    Xia B, Ke H, Inouye M. 2001. Acquirement of cold sensitivity by quadruple deletion of the cspA family and its suppression by PNPase S1 domain in Escherichia coli. Mol. Microbiol. 40:1179–88
    [Google Scholar]
  149. 149. 
    Xia B, Ke H, Shinde U, Inouye M. 2003. The role of RbfA in 16S rRNA processing and cell growth at low temperature in Escherichia coli. J. Mol. Biol. 332:3575–84
    [Google Scholar]
  150. 150. 
    Yamanaka K, Inouye M. 2001. Selective mRNA degradation by polynucleotide phosphorylase in cold shock adaptation in Escherichia coli. J. Bacteriol. 183:92808–16
    [Google Scholar]
  151. 151. 
    Yamanaka K, Zheng W, Crooke E, Wang YH, Inouye M 2001. CspD, a novel DNA replication inhibitor induced during the stationary phase in Escherichia coli. Mol. Microbiol. 39:61572–84
    [Google Scholar]
  152. 152. 
    Zangrossi S, Briani F, Ghisotti D, Regonesi ME, Tortora P, Dehò G. 2000. Transcriptional and post-transcriptional control of polynucleotide phosphorylase during cold acclimation in Escherichia coli. Mol. Microbiol. 36:61470–80
    [Google Scholar]
  153. 153. 
    Zhang Y, Burkhardt DH, Rouskin S, Li G-W, Weissman JS, Gross CA. 2018. A stress response that monitors and regulates mRNA structure is central to cold shock adaptation. Mol. Cell 70:2274–86.e7
    [Google Scholar]
  154. 154. 
    Zubradt M, Gupta P, Persad S, Lambowitz AM, Weissman JS, Rouskin S. 2017. DMS-MaPseq for genome-wide or targeted RNA structure probing in vivo. Nat. Methods 14:175–82
    [Google Scholar]
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