Cold shock response of Bacillus subtilis: Isoleucine-dependent switch in the fatty acid branching pattern for membrane adaptation to low temperatures

Journal of Bacteriology

Volumn 181, Issue 17, 1999, Pages 5341-5349

  Klein, Wolfgang ^a   Weber, Michael H W ^a   Marahiel, Mohamed A ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; ISOLEUCINE;

AMINO ACID TRANSPORT; ARTICLE; BACILLUS SUBTILIS; BACTERIAL GROWTH; BACTERIAL MEMBRANE; CELL MEMBRANE FLUIDITY; CELLULAR DISTRIBUTION; COLD STRESS; COLD TOLERANCE; CONCENTRATION RESPONSE; FATTY ACID SYNTHESIS; LIPID COMPOSITION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STRAIN DIFFERENCE;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); POSIBACTERIA;

EID: 0032860247     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.181.17.5341-5349.1999     Document Type: Article

References (49)

1. Aguilar, P. S., J. E. Cronan, Jr., and D. de Mendoza. 1998. A Bacillus subtilis gene induced by cold shock encodes a membrane phospholipid desaturase. J. Bacteriol. 180:2194-2200.
2. Akamatsu, T., H. Moriyama, and T. Kaneda. 1993. Genetic mapping of bfmA mutation causing fatty acid deficiency in Bacillus subtilis. Can. J. Microbiol. 39:629-633.
3. 15:O fatty acid in the growth of Listeria monocytogenes at low temperatures. Appl. Environ. Microbiol. 63:3887-3894.
4. Boos W., and J. M. Lucht. 1996. Periplasmic binding protein-dependent ABC transporters, p. 1175-1209. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed., vol. 1. ASM Press, Washington, D.C.
5. de Mendoza, D., and J. E. Cronan. 1983. Thermal regulation of membrane lipid fluidity in bacteria. Trends Biochem. Sci. 8:49-52.
6. Feller, G., E. Narinx, J. L. Arpigny, A. M. E. Baise, S. Genicot, and C. Gerday. 1996. Enzymes from psychrophilic organisms. FEMS Microbiol. Rev. 18:189-202.
7. Fink, P. S. 1993. Biosynthesis of branched-chain amino acids, p. 307-318. In A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and other gram-positive bacteria: biochemistry, physiology, and molecular genetics. American Society for Microbiology, Washington, D.C.
8. Fisher, S. H. 1993. Utilization of amino acids and other nitrogen-containing compounds, p. 221-228. In A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and other gram-positive bacteria: biochemistry, physiology, and molecular genetics. American Society for Microbiology, Washington, D.C.
9. Fulco, A. J. 1983. Fatty acid metabolism in bacteria. Prog. Lipid Res. 22: 133-160.
10. Gombos, Z., H. Wada, and N. Murata. 1992. Unsaturation of fatty acids in membrane lipids enhances tolerance of the cyanobacterium Synechocystis PCC 6803 to low-temperature photoinhibition. Proc. Natl. Acad. Sci. USA 89:9959-9963.
11. Gombos, Z., H. Wada, Z. Varkonyi, D. A. Los, and N. Murata. 1996. Characterization of the Fad12 mutant of Synechocystis that is defective in delta 12 acyl-lipid desaturase activity. Biochim. Biophys. Acta 1299:117-123.
12. Grau, R., and D. de Mendoza. 1993. Regulation of the synthesis of unsaturated fatty acids by growth temperature in Bacillus subtilis. Mol. Microbiol. 8: 535-542.
13. Grau, R., D. Gardiol, G. C. Glikin, and D. de Mendoza. 1994. DNA super-coiling and thermal regulation of unsaturated fatty acid synthesis in Bacillus subtilis. Mol. Microbiol. 11:933-941.
14. Graumann, P., T. M. Wendrich, M. H. W. Weber, K. Schröder, and M. A. Marahiel. 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. 25:741-756.
15. Graumann, P. L., and M. A. Marahiel. 1998. A superfamily of proteins that contain the cold-shock domain. Trends Biochem. Sci. 23:286-290.
16. Harwood, C. R., and S. M. Cutting. 1990. Molecular biological methods for Bacillus. John Wiley & Sons Ltd., Chichester, England.
17. Hoch, J. A., and J. L. Mathews. 1973. Chromosomal location of pleiotropic negative sporulation mutations in Bacillus subtilis. Genetics 73:215-228.
18. Kaneda, T. 1966. Biosynthesis of branched-chain fatty acids. IV. Factors affecting relative abundance of fatty acids produced by Bacillus subtilis. Can. J. Microbiol. 12:501-514.
19. Kaneda, T. 1966. Biosynthesis of branched-chain fatty acids. V. Microbial stereospecific syntheses of D-12-methyltetradecanoic and D-14-methylhexadecanoic acids. Biochim. Biophys. Acta 125:43-54.
20. Kaneda, T. 1991. Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiol. Rev. 55:288-302.
21. Kaneda, T., and E. J. Smith. 1980. Relationship of primer specificity of fatty acid de novo synthetase to fatty acid composition in 10 species of bacteria and yeasts. Can. J. Microbiol. 26:893-898.
22. Kaneda, T., E. J. Smith, and D. N. Naik. 1983. Fatty acid composition and primer specificity of de novo fatty acid synthetase in Bacillus globispores, Bacillus insolitus, and Bacillus psychrophilus. Can. J. Microbiol. 29:1634-1641.
23. Klein, W., and W. Boos. 1993. Induction of the lambda receptor is essential for effective uptake of trehalose in Escherichia coli. J. Bacteriol. 175:1682-1686.
24. Ko, R., L. T. Smith, and G. M. Smith. 1994. Glycine betaine confers enhanced osmotolerance and cryotolerance on Listeria monocytogenes. J. Bacteriol. 176:426-431.
25. Kroumova, A. B., Z. Xie, and G. J. Wagner. 1994. A pathway for the biosynthesis of straight and branched, odd- and even-length, medium-chain fatty acids in plants. Proc. Natl. Acad. Sci. USA 91:11437-11441.
26. Kunst, F., N. Ogasawara, I. Moszer, A. M. Albertini, G. Alloni, V. Azevedo, M. G. Bertero, P. Bessiéres, A. Bolotin, S. Borchert, R. Borriss, L. Boursier, A. Brans, M. Braun, S. C. Brignell, S. Bron, S. Brouillet, C. V. Bruschi, B. Caldwell, V. Capuano, N. M. Carter, S.-K. Choi, J.-J. Codani, I. F. Connerton, N. J. Cummings, R. A. Daniel, F. Denizot, K. M. Devine, A. Düsterhöft, S. D. Ehrlich, P. T. Emmerson, K. D. Entian, J. Errington, C. Fabret, E. Ferrari, D. Foulger, C. Fritz, M. Fujita, Y. Fujita, S. Fuma, A. Galizzi, N. Galleron, S.-Y. Ghim, P. Glaser, A. Goffeau, E. J. Golightly, G. Grandi, G. Guiseppi, B. J. Guy, K. Haga, J. Haiech, C. R. Harwood, A. Hẽnaut, H. Hilbert, S. Holsappel, S. Hosono, M.-F. Hullo, M. Itaya, L. Jones, B. Joris, D. Karamata, Y. Kasahara, M. Klaerr-Blanchard, C. Klein, Y. Kobayashi, P. Koetter, G. Koningstein, S. Krogh, M. Kumano, K. Kurita, A. Lapidus, S. Lardinois, J. Lauber, V. Lazarevic, S.-M. Lee, A. Levine, H. Liu, S. Masuda, C. Mauël, C. Médigue, M. Medina, R. P. Mellado, M. Mizuno, D. Moestl, S. Nakai, M. Noback, D. Noone, M. O'Reilly, K. Ogawa, A. Ogiwara, B. Oudega, S.-H. Park, V. Parro, T. M. Pohl, D. Portetelle, S. Porwollik, A. M. Prescott, E. Presecan, P. Pujic, B. Purnelle, G. Rapoport, M. Rey, S. Reynolds, M. Rieger, C. Rivolta, E. Rocha, B. Roche, M. Rose, Y. Sadaie, T. Sato, E. Scanlan, S. Schleich, R. Schroeter, F. Scoffone, J. Sekiguchi, A. Sekowska, S. J. Seror, P. Serror, B.-S. Shin, B. Soldo, A. Sorokin, E. Tacconi, T. Takagi, H. Takahashi, K. Takemaru, M. Takeuchi, A. Tamakoshi, T. Tanaka, P. Terpstra, A. Tognoni, V. Tosato, S. Uchiyama, M. Vandenbol, F. Vannier, A. Vassarotti, A. Viari, R. Wambutt, E. Wedler, H. Wedler, T. Weitzenegger, P. Winters, A. Wipat, H. Yamamoto, K. Yamane, K. Yasumoto, K. Yata, K. Yoshida, H.-F. Yoshikawa, E. Zumstein, H. Yoshikawo, and A. Danchin. 1997. The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390:249-256.
27. Kuykendall, L. D., M. A. Roy, J. J. O'Neill, and T. E. Devine. 1988. Fatty acids, antibiotic resistance, and desoxyribonucleic acid homology groups of Bradyrhizobium japonicum. Int. J. Syst. Bacteriol. 38:358-361.
28. Le Rudulier, D., A. R. Strom, A. M. Dandekar, L. T. Smith, and R. C. Valentine. 1984. Molecular biology of osmoregulation. Science 224:1064-1068.
29. Los, D. A., M. K. Ray, and N. Murata. 1997. Differences in the control of the temperature-dependent expression of four genes for desaturases in Synechocystis sp. PCC 6803. Mol. Microbiol. 25:1167-1175.
30. Matsubara, K., K. Ohnishi, and K. Kiritani. 1992. Nucleotide sequences and characterization of liv genes encoding components of the high-affinity branched-chain amino acid transport system in Salmonella typhimurium. J. Biochem (Tokyo). 112:93-101.
31. Miller, L. T. 1982. Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxy acids. J. Clin. Microbiol. 16:584-586.
32. Murata, N., and H. Wada. 1995. Acyl-lipid desaturases and their importance in the tolerance and acclimatization to cold of cyanobacteria. Biochem. J. 308:1-8.
33. Nichols, D. S., and N. J. Russell. 1996. Fatty acid adaptation in an Arctic bacterium - changes in primer utilization. Microbiology 142:747-754.
34. Ohnishi, K., A. Hasegawa, K. Matsubara, T. Date, T. Okada, and K. Kiritani. 1988. Cloning and nucleotide sequence of the brnQ gene, the structural gene for a membrane-associated component of the LIV-II transport system for branched-chain amino acids in Salmonella typhimurium. Jpn. J. Genet. 63:343-357. (Erratum, 63:495.)
35. Ohnishi, K., A. Nakazima, K. Matsubara, and K. Kiritani. 1990. Cloning and nucleotide sequences of livB and livC, the structural genes encoding binding proteins of the high-affinity branched-chain amino acid transport in Salmonella typhimurium. J. Biochem. (Tokyo) 107:202-208.
36. Oku, H., M. Onotogi, J. Nagata, K. Wada, and I, Chinen. 1995. Selective use of L-valine and L-isoleucine for the biosynthesis of branched-chain fatty acids in rat skin. Biosci. Biotechnol. Biochem. 59:891-895.
37. Panoff, J. M., D. Corroler, B. Thammavongs, and P. Boutibonnes. 1997. Differentiation between cold shock proteins and cold acclimation proteins in a mesophilic gram-positive bacterium, Enterococcus faecalis JH2-2. J. Bacteriol. 170:4451-4454.
38. Rowbury, R. 1995. Strategies to beat the cold: antifreeze, ice nucleation, mini-greenhouse and "Follow that sun!" Sci. Prog. 78:267-280.
39. Russell, N. J. 1984. Mechanisms of thermal adaptation in bacteria: blueprints for survival. Trends Biochem. Sci. 9:108-112.
40. Sinensky, M. 1974. Homeoviscous adaptation - a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proc. Natl. Acad. Sci. USA 71:522-525.
41. Spizizen, J. 1958. Transformation of biochemically deficient strains of Bacillus subtilis by deoxyribonucleate. Proc. Natl. Acad. Sci. USA 44:1072-1084.
42. Suutari, M., and S. Laakso. 1992. Changes in fatty acid branching and unsaturation of Streptomyces griseus and Brevibacterium fermentans as a response to growth temperature. Appl. Environ. Microbiol. 58:2338-2340.
43. Suutari, M., and S. Laakso. 1994. Microbial fatty acids and thermal adaptation. Crit. Rev. Microbiol. 20:285-328.
44. Suutari, M., and S. Laakso. 1992. Unsaturated and branched chain-fatty acids in temperature adaptation of Bacillus subtilis and Bacillus megaterium. Biochim. Biophys. Acta 1126:119-124.
45. Tauch, A., T. Hermann, A. Burkovski, R. Kramer, A. Puhler, and J. Kalinowski. 1998. Isoleucine uptake in Corynebacterium glutamicum ATCC 13032 is directed by the brnQ gene product. Arch. Microbiol. 169:303-312.
46. Thieringer, H. A., P. G. Jones, and M. Inouye. 1998. Cold shock and adaptation. Bioessays 20:49-57.
47. Weber, M. H. W. Unpublished data.
48. Willecke, K., and A. B. Pardee. 1971. Fatty acid-requiring mutant of Bacillus subtilis defective in branched chain alpha-keto acid dehydrogenase. J. Biol. Chem. 246:5264-5272.
49. Womersley, C., P. S. Uster, A. S. Rudolph, and J. H. Crowe. 1986. Inhibition of dehydration-induced fusion between liposomal membranes by carbohydrates as measured by fluorescence energy transfer. Cryobiology 23:245-255.