Abstract
The groESL operon of a psychrophilic bacterium, Colwellia maris, was cloned and sequenced. The operon contains two ORFs of 291 bp and 1,650 bp separated by 210 bp. Northern blot analysis suggested that the groESL operon was transcribed as a bicistronic mRNA, and that the amount of mRNA markedly increased after the temperature was raised from 10 °C to 20 °C. Although the optimum temperatures for GroESL function are different in psychrophilic, mesophilic, and thermophilic bacteria, the deduced amino acid sequences of C. maris GroES and GroEL showed remarkably high similarity with those of GroES and GroEL from mesophilic and thermophilic bacteria. A putative promoter similar to the Escherichia coli σ32 consensus sequence was identified. One specific feature of C. maris groESL was that in the putative untranslated region the G+C content was about 24 mol%, which is much lower than that of mesophilic bacteria such as E. coli. The low G+C content may be important for maintaining transcription at low temperatures.
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References
Aguilar PS, Lopez P, de Mendoza D (1999) Transcriptional control of the low-temperature-inducible des gene, encoding the Δ5 desaturase of Bacillus subtilis. J Bacteriol 181:7028–7033
Arsene F, Tomoyasu T, Bukau B (2000) The heat shock response of Eschericia coli. Int J Food Microbiol 55:3–9
Bukau B (1993) Regulation of the Escherichia coli heat-shock response. Mol Microbiol 9:671–680
Bukau B, Horwich AL (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92:351–366
Chamot D, Magee WC, Yu E, Owttrim GW (1999). A cold shock-induced cyanobacterial RNA helicase. J Bacteriol 181:1728–1732
Glatz A, Horvath I, Varvasovszki V, Kovacs E, Török Z, Vigh L (1997) Chaperonin genes of the Synechocystis PCC 6803 are differentially regulated under light-dark transition during heat stress. Biochem Biophys Res Commun 239:291–297
Grandvalet C, Rapoport G, Mazodier P (1998) hrcA, encoding the repressor of the groEL genes in Streptomyces albus G, is associated with a second dnaJ gene. J Bacteriol 180:5129–5134
Grantcharova V, Alm EJ, Baker D, Horwich AL (2001) Mechanisms of protein folding. Curr Opin Struct Biol 11:70–82
Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381:571–579
Hawley DK, McClure WR (1983) Compilation and analysis of Escherichia coli promoter DNA sequences. Nucleic Acids Res 11:2237–2255
Homuth G, Domm S, Kleiner D, Schumann W (2000) Transcriptional analysis of major heat shock genes of Helicobacter pylori. J Bacteriol 182:4257–4263
Horikoshi K (1973) Alkaline enzymes produced by alkalophilic microorganisms. Tanpakushitu Kakusan Koso 18:784–790
Lehel C, Los D, Wada H, Györgyei J, Horvath I, Kovacs E, Murata N, Vigh L (1993) A second groEL-like gene, organized in a groESL operon is present in the genome of Synechocystis sp. PCC 6803. J Biol Chem 268:1799–1804
Matsubara H, Goto K, Matsumura T, Mochida K, Iwaki M, Niwa M, Yamasato K (2002) Alicyclobacillus acidiphilus sp. nov., a novel thermoacidophilic, omega-alicyclic fatty acid-containing bacterium isolated from acidic beverages. Int J Syst Evol Microbiol 52:1681–1685
Minder AC, Fischer HM, Hennecke H, Narberhaus F (2000) Role of HrcA and CIRCE in the heat shock regulatory network of Bradyrhizobium japonicum. J Bacteriol 182:14–22
Mizunoe Y, Wai SN, Umene K, Kokubo T, Kawabata S, Yoshida S (1999) Cloning, sequencing, and functional expression in Escherichia coli of chaperonin (groESL) genes from Vibrio cholerae. Microbiol Immunol 43:513–520
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. J Bacteriol 181:401–410
Morita RY (1975) Psychrophilic bacteria. Bacteriol Rev 39:144–167
Narberhaus F (1999) Negative regulation of bacterial heat shock genes. Mol Microbiol 31:1–8
Ochiai T, Fukunaga N, 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
Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27 437-496
Sakamoto T, Higashi S, Wada H, Murata N, Bryant DA (1997) Low-temperature-induced desaturation of fatty acids and expression of desaturase genes in the cyanobacterium Synechococcus sp. PCC 7002. FEMS Microbiol Lett 15:313–320
Schmidt A, Schiesswohl M, Völker U, Hecker M, Schumann W (1992) Cloning, sequencing, mapping, and transcriptional analysis of the groESL operon from Bacillus subtilis. J Bacteriol 174:3993–3999
Schön U, Schumann W (1993) Molecular cloning, sequencing, and transcriptional analysis of the groESL operon from Bacillus stearothermophilus. J Bacteriol 175:2465–2469
Stetter KO (1996) Hyperthermophilic prokaryotes. FEMS Microbiol Rev 18:149–158
Takada Y, Ochiai T, Okuyama H, Nishi K, Sasaki S, (1979) An obligately psychrophilic bacterium isolated on the Hokkaido coast. J Gen Appl Microbiol 25:11–19
Tanaka N, Hiyama T, Nakamoto H (1997) Cloning, characterization and functional analysis of groESL operon from thermophilic cyanobacterium Snechococcus vulcanus. Biochim Biophys Acta 1343:335–348
Thies FL, Weishaupt A, Karch H, Hartung HP, Giegerich G (1999) Cloning, sequencing and molecular analysis of the Campylobacter jejuni groESL bicistronic operon. Microbiology 45:89–98
Tosco A, Birolo L, Madonna S, Lolli G, Sannia G, Marino G (2003) GroEL from the psychrophilic bacterium Pseudoalteromonas haloplanktis TAC 125: molecular characterization and gene cloning. Extremophiles 7:17–28
Williams JGK (1988) Construction of specific mutations in photosystemII photosynthetic reaction center by genetic engineering methods in Synechocystis PCC 6803. Methods Enzymol 167:766–778
Worsey MJ, Williams PA (1975) Metabolism of toluene and xylenes by Pseudomonas putida (arvilla) mt-2: evidence for a new function of the TOL plasmid. J Bacteriol. 124:7–13
Yamanaka K (1999) Cold shock response in Escherichia coli. J Mol Microbiol Biotechnol 1:193–202
Yayanos AA, Dietz AS, Van Boxtel R (1981) Obligately barophilic bacterium from the Mariana trench. Proc Natl Acad Sci USA 78:5212–5215
Yumoto I, Kawasaki K, Iwata H, Matsuyama H, Okuyama H (1998) Assignment of Vibrio sp. strain ABE-1 to Colwellia maris sp. nov., a new psychrophilic bacterium. Int J Syst Bacteriol 48:1357–1362
Yura T, Nakahigashi K (1999) Regulation of the heat-shock response. Curr Opin Microbiol 2:153–158
Zuber U, Schumann W (1994) CIRCE, a novel heat shock element involved in regulation of heat shock operon dnaK of Bacillus subtilis. J Bacteriol 176:1359–1363
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We thank Yoshitaka Nishiyama for critical discussions and help in the present studies.
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Yamauchi, S., Okuyama, H., Morita, E.H. et al. Gene structure and transcriptional regulation specific to the groESL operon from the psychrophilic bacterium Colwellia maris . Arch Microbiol 180, 272–278 (2003). https://doi.org/10.1007/s00203-003-0587-7
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DOI: https://doi.org/10.1007/s00203-003-0587-7