Bacterial adaptation to low temperature: Implications for cold-inducible genes

Journal of Plant Research

Volumn 112, Issue 2, 1999, Pages 263-272

  Fukunaga, Noriyuki ^a   Sahara, Takehiko ^a   Takada, Yasuhiro ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Cold shock proteins; Cold adapted enzyme; Gene expression; Low temperature; Psychrophilic bacteria

Indexed keywords

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA; VIBRIO; VIBRIO SP.;

EID: 0033245213     PISSN: 09189440     EISSN: None     Source Type: Journal    
DOI: 10.1007/pl00013883     Document Type: Conference Paper

References (91)

1. Aguilar, P.S., Cronan, J.E. Jr. and DeMendoza, D. 1998. A Bacillus subtilis gene induced by cold shock encodes a membrane phospholipid desaturase. J. Bacteriol. 180: 2194-2200.
2. Arpigny, J.L., Feller, G. and Gerday, C. 1995. Cloning, sequence and structural features of a lipase from the antarctic facultative psychrophile Psychrobacter immobilis B10. Biochim. Biophys. Acta. 1263: 103.
3. Bae, W. Jones, P.G. and Inouye, M. 1997. CspA, the major cold shock protein of Escherichia coli, negatively regulates its own gene expression. J. Bacteriol. 179: 7081-7088.
4. Berger, F., Morellet, N., Menu, F. and Potier, P. 1996. Cold shock and cold acclimation proteins in the psychotropic bacterium Arthrobacter globiformis SI55. J. Bacteriol. 178: 2999-3007.
5. Brandi, A., Pietroni, P., Gualerzi, C.O. and Pon, C.L. 1996. Post-transcriptional regulation of CspA expression in Escherichia coli. Mol. Microbiol. 19: 231-240.
6. Brock, T.D., and Madigan, M.T. 1980. Biology of Microorganisms, 5th ed. Engelwood Cliffs, NJ: Prentice Hall, pp. 330-335
7. Chang, F.N., 1978. Temperature-dependent variation in the extent of methylation of ribosomal proteins L7 and L12 in Escherichia coli. J. Bacteriol. 135: 1165-1166.
8. Chapot-Chartier, M-P., Schouler, C., Lepeuple, A-S., Gripon, J-C. and Chopin, M-C. 1997. Characterization of cspB, a cold-shock-inducible gene from Lacfococcus lactis, and evidence for a family of genes homologous to the Escherichia coli cspA major cold shock gene. J. Bacteriol. 179: 5589-5593.
9. Choo, D-W., Kurihara, T., Suzuki, T., Soda, K. and Esaki, N. 1998. A cold-adapted lipase of an alaskan psychrotroph, Pseudomonas sp. strain B11-1: gene cloning and enzyme purification and characterization. Appl. Environ. Microbiol. 64: 486-491.
10. Colucci, M.S. and Iniss, W.E. 1996. Ethylene glycol utilization, cold and ethylene glycol shock and acclimation proteins in a psychrotrophic bacterium. Curr. Microbiol. 32: 179-182.
11. Cozzone, A.J., 1998. Regulation of acetate metabolism by protein phosphorylation in enteric bacteria. Ann. Rev. Microbiol. 52: 127-164.
12. Cronan, J.E. and Rock. C.O. 1996. Biosynthesis of membrane lipids, p. 612-636. In F.C. Neidhardt, R. Curtis III, J.L. Ingraham, E.C.C. Lin, K.B. Low, B. Magasanik, W.S. Resnikoff, M. Riley, M. Schaechter, and H.E. Umbarger, eds., Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd ed. ASM Press, Washington, D.C.
13. Davail, S., Feller, G., Narinx, E. and Gerday, C. 1994. Cold adaptation of proteins: purification, characterization, and sequence of the heatlabile subtilisin from the antarctic psychrophile Bacillus TA41. J. Biol. Chem. 269: 17448-17453.
14. Dersch, P., Kneip, S. and 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: 255-259.
15. Donovan, W.P. and Kusher. S.R. 1986. Polynucleotide phosphorylase and ribonuclease II are required for cell viability and mRNA turnover in Escherichia coli K-12. Proc. Natl. Acad. Sci. USA. 83: 120-124.
16. Eikmanns, B.J., Rittmann, D., and Sahm, H. 1995. Cloning, sequence analysis, expression, and inactivation of the Corynebacterium glutamicum icd gene encoding IDH and biochemical characterization of the enzyme. J. Bacteriol. 177: 774-782.
17. Fang, L., Jiang, W., Bae, W. and Inouye, M. 1997. Promoter-independent cold-shock induction of cspA and its derepression at 37 C by mRNA stabilization. Mol. Microbiol. 23: 355-364
18. Farewell, A. and Neidhardt, F.C. 1998. Effect of temperature on in vivo protein synthetic capacity in Escherichia coli. J. Bacteriol. 180: 4704-4719
19. Feller, G., Lonhienne, T., Deroanne, C., Libioulle, C., Beeumen, J.V. and Gerday, C. 1992. Purification, characterization, and nucleotide sequence of the thermolabile α-amylase from the antarctic psychrotroph Alteromonas haloplanctis A23. J. Biol. Chem. 267: 5217-5221.
20. Feller, G., Narinx, E., Arpigny, J.L., Aittaleb, M., Baise, E., Genicot, S. and Gerday, C. 1996. Enzymes from psychrophilic organisms. FEMS Microbiol. Rev. 18: 189-202.
21. Feller, G., Zekhnini, Z., Lamotte-Brasseur, J. and Gerday, C. 1997. Enzymes from cold-adapted microorganisms: the class C β-lactamase from the antarctic psychrophile Psychrobacter immobilis A5. Eur. J. Biochem. 244: 186-191.
22. Friedman, H., Lu, P. and Rich, A. 1969. Ribosomal subunits produced by cold sensitive initiation of protein synthesis. Nature 223: 909-913.
23. Friedman, H., Lu, P. and Rich, A. 1971. Temperature control of initiation of protein synthesis in Escherichia coli. J. Mol. Biol. 61: 105-121.
24. Friedman, D.I., Olson, E.R., Georgopoulos, C., Tilly, K., Herskowitz, I. and Banuett, F. 1984. Interaction of bacteriophage and host macromolecules in the growth of bacteriophage lambda. Microbiol. Rev. 48: 299-325.
25. Fujii, D.K. and Fulco, J.A. 1977. Biosynthesis of unsaturated fatty acid in bacilli: hyperinduction and modulation of desaturase synthesis. J. Biol. Chem. 252: 3660-3670.
26. Fukunaga, N., Yoshida, S., Ishii, A., Imagawa, S., Takada, Y. and Sasaki, S. 1988. Isolation and characterization of a mutant defective in one of two isozymes of the isocitrate dehydrogenase from a psychrophilic bacterium, Vibrio sp. strain ABE-1. J. Gen. Appl. Microbiol. 34: 457-465.
27. Fukunaga, N., Imagawa, S., Sahara, T., Ishii, A. and Suzuki, M. 1992. Purification and characterization of monomeric isocitrate dehydrogenase with NADP-specificity from Vibrio parahaemolyticus Y4. J. Biochem. 112: 849-855.
28. Gerday, C., Aittateb, M., Arpigny, J.L., Baise, E., Chessa, J-P., Garsoux, G., Petrescu, I. and Feller, G. 1997. Psychrophilic enzymes: a thermodynamic challenge. Biochim. Biophys. Acta 1342: 119-131.
29. Gerike, U., Danson, M.J., Russell, N.J. and Hough, D.W. 1997. Sequencing and expression of the gene encoding a cold-active citrate synthase from an Antarctic bacterium, strain DS2-3R. Eur. J. Biochem. 248: 49-57.
30. Goldenberg, D., Azar, I. and Oppenheim, A.B. 1996. Differential mRNA stability of the cspA gene in the cold-shock response of Escherichia coli. Mol. Microbiol. 19: 241-248.
31. Goldstein, J., Pollitt, N.S. and Inouye, M. 1990. Major cold shock protein in Escherichia coli. Proc. Natl. Acad. Sci. USA 87: 283-287.
32. Goransson, M., Sonden, S., Nilsson, P., Dagberg, B., Forsman, K., Emanuelsson, K. and Uhlin, B.E. 1990. Transcriptional silencing and thermoregulation of gene expression in Escherichia coli. Nature, 344: 682-685.
33. Graumann, P.L. and Marahiel, M.A. 1998. A superfamily of proteins that contain the cold shock domain. TIBS. 23: 286-290.
34. Gualerzi, C.O. and Pon, C.L. 1990. Initiation of mRNA translation in prokaryotes. Biochemistry. 29: 5881-5889.
35. Gutshall, K.R., Trimbur, D.E., Kasmir, J.J. and Brenchley, J.E. 1995. Analysis of a novel gene and β-galactosidase isozyme from a psychrotrophic Arthrobacter isolate. J. Bacteriol. 177: 1981-1988.
36. Hebraud, M., Dubos, E., Potier, P. and Labadie, J. 1994. Effect of growth temperatures on the protein levels in a psychrotrophic bacterium, Pseudomonas fragi. J. Bacteriol. 176: 4017-4024.
37. Hochachka, P.W. and Somero, G.N. 1984. Biochemical adaptation. Princeton Univ. Press, Princeton, New Jersey
38. 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.
39. Hurst, H.C., Masson, N, Jones, N.C. and Lee, K.A.W. 1990. The cellular transcription factor CREB corresponds to activating transcription factor 47 (ATF-47) and forms complex with a group of polypeptides related to ATF-43. Mol. Cell. Biol. 10: 6192-6203.
40. Ishii, A., Imagawa, S., Fukunaga, N., Sasaki, S., Minowa, O., Mizuno, Y. and Shiokawa, H. 1987. Isozymes of isocitrate dehydrogenase from an obligately psychrophilic bacterium, Vibrio sp. strain ABE-1: purification, and modulation of activities by growth conditions. J. Biochem. 102: 1489-1498.
41. Ishii, A., Suzuki, M., Sahara, T., Takada, Y., Sasaki, S. and Fukunaga, N. 1993. Genes encoding two isocitrate dehydrogenase isozymes of a psychrophilic bacterium, Vibrio sp. strain ABE-1. J. Bacteriol. 175: 6873-6880.
42. Jeffreys, A.G., Hak, K.M., Steffan, R.J., Foster, J.W. and Bej, A.K. 1998. Growth, survival and characterization of cspA in Salmonella enterdis following cold shock. Curr. Microbiol. 36: 29-35.
43. Jiang, W., Jones, P.G. and Inouye, M. 1993. Chloramphenicol induces the transcription of the major cold-shock gene of Escherichia coli, cspA. J. Bacteriol. 175: 5824-5828.
44. Jiang, W., Hou, Y. and Inouye. M. 1997. CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J. Biol. Chem. 272: 196-202.
45. Jones, P.G., VanBogelen, R.A. and Neidhardt, F.C. 1987. Induction of proteins in response to low temperature in Escherichia coli. J. Bacteriol., 169: 2092-2095.
46. Jones, P.G., Krah, R., Tafuri, S.R. and Wolffe, A.P. 1992. DNA gyrase, CS7.4, and the cold shock response in Escherichia coli. J. Bacteriol. 174: 5798-5802.
47. Jones, P.G. and Inouye. M. 1994. The cold-shock response-a hot topic. Mol. Microbiol. 11: 811-818.
48. Jones, P.G. and Inouye, M. 1996a. RbfA, a 30S ribosomal binding factor, is a cold-shock protein whose absence triggers the cold-shock response. Mol. Microbiol. 21: 1207-1218.
49. Jones, P.G., Mitta, M., Kim, Y., Jiang, W. and Inouye, M. 1996b. Cold shock induces a major ribosomal-associated protein that unwinds double stranded RNA in Escherichia coli. Proc. Natl. Acad. Sci. USA. 93: 76-80.
50. Jones, P.G., VanBogelen, R.A. and Neidhardt. F.C. 1987. Induction of proteins at low temperature in Escherichia coli. J. Bacteriol. 169: 2092-2095.
51. LaTeana, A., Brandi, A., Falconi, M., Spurio, R., Pon, C.L. and Gualerzi. C.O. 1991. Identification of a cold shock transcriptional enhancer of the Escherichia coli gene encoding nucleoid protein H-NS. Proc. Natl. Acad. Sci. USA. 88: 10907-10911.
52. Lelivelt, M.J. and Kawula, T.H. 1995. Hsc66, an Hsp70 homolog in Escherichia coli, is induced by cold shock but not heat shock. J. Bacteriol. 177: 4900-4907.
53. Lindquist, S. 1992. Heat-shock proteins and stress tolerance in microorganisms. Curr. Opn. Genet. Dev. 2: 748-755.
54. Marshall, C. J. 1997. Cold-adapted enzymes. TIBTECH. 15: 359-364.
55. Mayer, B., Kaplan, T., Lechner, S. and Scherer, S. 1996. Identification and purification of a family of dimeric major cold shock protein homologs from the psychrotrophic Bacillus cereus WSBC 10201. J. Bacteriol. 178: 2916-2925.
56. Mayo, B., Derzeille, S., Fernandez, M., Leonard, C., Ferain, T., Hols, P., Suarez, J.D. and Delcour. J. 1997. Cloning and characterization of cspL, and cspP, two cold-inducible genes from Lactobacillus plantarum. J. Bacteriol. 179: 3039-3042.
57. Mitta, M., Fang, L. and Inouye, M. 1997. Deletion analysis of cspA of E. coli, requirement of the AT-rich UP element for CspA transcribing, and the downstream box in the coding region for its cold-shock induction. Mol. Microbiol. 26: 321-335.
58. Morita, R.Y., 1975. Psychrophilic bacteria. Bacteriol. Rev. 39: 144-167
59. Murata, N. and Wada. H. 1995. Acyl-lipid desaturases and their importance in the tolerance and acclimation to cold of cyanobacteria. Biochem. J. 308: 1-8.
60. Nakashima, K., Kanamaru, K., Mizuno, T. and Horikoshi, K. 1996. A novel member of the cspA family of genes that is induced by cold shock in Escherichia coli. J. Bacteriol. 178: 2994-2997.
61. Neidhardt, R.C. and VanBogelen, R.A. 1987. Heat shock response, p. 1334-1345. In Neidhardt, F.C., lngraham, J.L., Low, K.B., Magasank, B., Schaechter, M. and Umbarger, H.E., eds., Escherichia coli and Salmonella typhimurium: cellular and molecular biology, vol. 2. American Society for Microbiology, Washington, D.C.
62. Ochiai, T., Fukunaga, N. and Sasaki, S. 1979. Purification and some properties of two NADP-specific isocitrate dehydrogenases from an obligately psychrophilic marine bacterium, Vibrio sp. strain ABE-1. J. Biochem. 86: 377-384.
63. Ochiai, T., Fukunaga, N. and Sasaki, S. 1984. Two structurally different NADP-specific isocitrate dehydrogenases in obligately psychrophilic bacterium, Vibrio sp. strain ABE-1. J. Gen. Appl. Microbiol. 30: 479-487.
64. Panoff, J.M. Corroler, D., Thammavongs, B. and 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: 4451-4454.
65. Preston, C.M., Wu, K.Y., Molinski, T.F. and DeLong, E.F. 1996. A psychrophilic crenarchaon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov. Proc. Natl. Acad. Sci. USA. 93: 6241-6246.
66. Qoronfleh, M.W., Debouck, C. and Keller, J. 1992. Identification and characterization of novel low temperature-inducible promoters of Escherichia coli. J. Bacteriol. 174: 7902-7909.
67. Rentier-Delrue, F., Mande, S.C., Moyens, S., Terpstra, P., Mainfroid, V., Goraj, K., Lion, M., Hol, W.G. and Martial, J.A. 1993. Cloning and overexpression of the triosephosphate isomerase genes from psychrophilic and thermophilic bacteria: structural comparison of the predicted protein sequence. J. Mol. Biol. 229: 85-93.
68. Roberts, M.F. and Inniss, W.E. 1992. The synthesis of cold shock proteins and cold acclimation proteins in the psychrophilic bacterium Aquaspirillum articum. Curr. Microbiol. 25: 275-278.
69. Rose, H.A., 1989. Influence of the environment on microbial lipid composition. p. 255-278. In C. Ratledge, and S.G. Wilkinson, ed., Microbial lipids, vol. 2, Academic Press, London
70. Russell, N. J. 1990. Cold adaptation of microorganisms. Phil. Trans. R. Soc. London. 326: 595-611.
71. Sahara, T., Suzuki, M., Tsuruha, J-I., Takada, Y. and Fukunaga, N. 1999. cis-Acting elements responsible for low temperature inducible expression of the gene coding for the thermolabile isocitrate dehydrogenase isozyme of a psychrophilic bacterium, Vibrio sp. strain ABE-1. J. Bacteriol. 181: 2602-2611.
72. Sakamoto, T., Higashi, S., Wada, H., Murata, N. and Bryant, D.A. 1997. Low-temperature induced desaturation of fatty acids and expression of desaturase genes in the cyanobacterium Synechococcus sp. PCC 7002. FEMS Microbiol. Lett. 152: 313-320.
73. Salotra, P., Singh, D.K., Seal, K.P., Krishna, N., Jaffe, H. and Bhatnagar, R. 1995. Expression of DnaK and GroEL homologs in Leuconostoc esenteroides in response to heat shock, cold shock or chemical stress. FEMS Microbiol. Lett. 131: 57-62.
74. Schindelin, H., Marahiel, M.A. and Heinemann, U. 1993. Universal nucleic-acid binding domain revealed by crystal structure of the B. subtilis major cold shock protein. 1993. Nature, 364: 164-168.
75. Schindelin, H., Cordes, F., Jiang, W., Inouye, M. and Heinemann, U. 1994. Crystal structure of the major cold-shock protein of Escherichia coli. Proc. Natl. Acad. Sci. USA. 91: 5119-5123.
76. Schleper, C., Swanson, R.V., Mathur, E.J. and DeLong, E.F. 1997. Characterization of a DNA polymerase from the uncultivated psychrophilic archaeon Cenarchaeum symbiosum. J. Bacteriol. 179: 7803-7811.
77. Shinozaki, K. and Yamaguchi-Shinozaki, K. 1997. Gene expression and signal transduction in water-stress response. Plant Physiol. 115: 327-334.
78. Stockinger, E.J., Gilmour, S.J. and Thomashaw, M.F. 1997. Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc. Natl. Acad. Sci. USA, 94: 1035-1040.
79. Sugino, A., Peebles, C., Kreuzer, K.N. and Cozzarelli, N.R. 1977. Mechanism of action of nalidixic acid: Purification of Escherichia coli nalA gene product and its relationship to DNA gyrase and a novel nicking-closing enzyme. Proc. Natl. Acad. Sci. USA. 74: 4267-4771.
80. Suzuki, M., Sahara, T., Tsuruha, J-I., Takada, Y. and Fukunaga, N. 1995. Differential expression in Escherichia coli of the Vibrio sp. strain ABE-1 icdI and icdII genes encoding structurally different isocitrate dehydrogenase isozymes. J. Bacteriol. 177: 2138-2142.
81. Tanabe, H., Goldstein, J., Yang, M. and Inouye, M. 1992. Identification of the promoter region of the Escherichia coli major cold shock gene, cspA. J. Bacteriol., 174: 3867-3873.
82. Takada, Y., Ochiai, T., Okuyama, H., Nishi, K. and Sasaki, S. 1979. An obligately psychrophilic bacterium isolated on the Hokkaido coast. J. Gen. Appl. Microbiol. 25: 11-19.
83. Thieringer, H.A., Jones, P.G. and Inouye, M. 1998. Cold shock and adaptation. BioEssays, 20: 49-57.
84. Tokuhisa, J.G., Vijayan, P., Feldmann, K.A. and Browse, J.A. 1998. Chloroplast development at low temperatures requires a homolog of DIM1, a yeast gene encoding the 18S rRNA dimethylase. Plant Cell, 10: 699-711.
85. VanBogelen, R.A. and Neidhardt, F.C. 1990. Ribomes as sensors of heat and cold shock in Escherichia coli. Proc. Natl. Acad. Sci. USA. 87: 5589-5593.
86. Walker, G.C., 1984. Mutagenesis and inducible response to deoxyribonucleic acid damage in Escherichia coli. Microbiol. Rev. 48: 60-93.
87. White-Ziegler, C.A. and Low. D.A. 1992. Thermoregulation of the pap operon: evidence for the involvement of RimJ, the N-terminal acetylase of ribosomal protein S5. J. Bacteriol. 174: 7003-7012.
88. Whyte, L.G. and Inniss, W.E. 1992. Cold shock proteins and cold acclimation proteins in a psychrotrophic bacterium. Can. J. Microbiol. 38: 1281-1285.
89. Willimsky, G., Bang, H., Fischer, G. and Marahiel, H.A. Characterization of cspB, a Bacillus subtilis inducible cold shock gene affecting cell viability at low temperatures. 1992. J. Bacteriol. 174: 6326-6335.
90. Wolffe, A.P., Tafuri, S., Ranjan, M. and Familari, M. 1992. The Y-box factors: a family of nucleic acid binding proteins conserved from Escherichia coli to man. New Biol. 4: 290-298.
91. Yamaguchi-Shinozaki, K. and Shinozaki, K. 1994. A novel cis-element in an arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6: 251-264.