Growth temperature associated protein expression and membrane fatty acid composition profiles of Salmonella enterica serovar Typhimurium

Journal of Basic Microbiology

Volumn 50, Issue 6, 2010, Pages 507-518

  Balamurugan, Sampathkumar ^a  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

Author keywords

Growth temperature; Membrane fatty acid composition profile; Protein expression profile; Salmonella sp.

Indexed keywords

BACTERIAL PROTEIN; FATTY ACID; PROTEOME;

ARTICLE; BIOSYNTHESIS; CELL MEMBRANE; CHEMISTRY; CYTOPLASM; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGICAL STRESS; SALMONELLA TYPHIMURIUM; TEMPERATURE; TWO DIMENSIONAL GEL ELECTROPHORESIS;

BACTERIAL PROTEINS; CELL MEMBRANE; CYTOPLASM; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FATTY ACIDS; GENE EXPRESSION REGULATION, BACTERIAL; PROTEOME; SALMONELLA TYPHIMURIUM; STRESS, PHYSIOLOGICAL; TEMPERATURE;

SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA SP.; SALMONELLA TYPHIMURIUM;

EID: 78650373725     PISSN: 0233111X     EISSN: 15214028     Source Type: Journal    
DOI: 10.1002/jobm.201000037     Document Type: Article

References (81)

1. Aibara, S., Kato, M., Ishinaga, M., Kito, M., 1972. Changes in positional distribution of fatty acids in the phospholipids of Escherichia coli after shift down in temperature. Biochim. Biophys. Acta, 270, 301-306.
2. Álvarez-Ordóñez, A., Fernández, A., López, M., Arenas, R. et al., 2008. Modifications in membrane fatty acid composition of Salmonella typhimurium in response to growth conditions and their effect on heat resistance. Int. J. Food Microbiol., 123, 212-219.
3. Andrade, A., Giron, J.A., Amhaz, J.M.K., Trabulsi, L.R. et al., 2002. Expression and characterization of flagella in nonmotile enteroinvasive Escherichia coli isolated from diarrhea cases. Infect. Immun., 70, 5882-5886.
4. Bae, W., Jones, P.G., Inouye, M., Severinov, K., 2000. Escherichia coli CspA-family RNA chaperones are transcription antiterminators. Proc. Natl. Acad. Sci. USA, 97, 7784-7789.
5. Bayles, D.O., Annous, B.A., Wilkinson, B.J., 1996. Cold stress proteins in Listeria monocytogenes in response to temperature down-shock and growth at low temperatures. Appl. Environ. Microbiol., 62, 1116-1119.
6. Beney, L., Gervais, P., 2001. Influence of the fluidity of the membrane on the response of microorganisms to environmental stresses. Appl. Environ. Microbiol., 57, 34-42.
7. Beran, R.K., Simons, R.W., 2001. Cold-temperature induction of Escherichia coli polynucleotide phosphorylase occurs by reversal of its autoregulation. Mol. Microbiol., 39, 112-115.
8. Berry, E.D., Foefeding, P.M., 1997. Cold temperature adaptation and growth of microorganisms. J. Food Prot., 60, 1583-1594.
9. Bisset, K.A., Pease, P., 1957. The distribution of flagella in dividing bacteria. J. Gen. Microbiol., 16, 382-384.
10. Bollman, J., Ismond, A., Blank, G., 2001. Survival of Escherichia coli O157:H7 in frozen foods: impact of the cold shock response. Int. J. Food Microbiol., 64, 127-138.
11. Bradford, M.M., 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254.
12. Brandi, A., Pietroni, P., Gualerzi, C.O., Pon, C.L., 1996. Post-transcriptional regulation of CspA expression in Escherichia coli. Mol. Microbiol., 19, 231-240.
13. Bright-Gaertner, E., Proulx, P., 1972. Metabolism of phosphoglycerides in Escherichia coli during growth at 37 °C and during a cold-induced lag phase. Biochim. Biophys. Acta, 270, 40-49.
14. Chandramouli, K., Johnson, M.K., 2006. HscA and HscB stimulate [2Fe-2S] cluster transfer from IscU to apo-ferredoxin in an ATP-dependent reaction. Biochem., 45, 11087-11095.
15. Corry, P.M., Robinson, S., Getz, S., 1977. Hyperthermic effects on DNA repair mechanisms. Radiology, 123, 475-482.
16. Craig, E.A., Gambill, B.D., Nelson, R.J., 1993. Heat shock proteins: Molecular chaperones of protein biogenesis. Microbiol. Rev., 57, 402-414.
17. Cronan Jr., J. E., LaPorte, D., 1996. Tricarboxylic acid cycle and glyoxylate bypass. p. 206-216. In: F.C. Neidhart, et al. (eds.), Escherichia coli and Salmonella: Cellular and Molecular Biology ASM Press, Washington, D.C. pp. 206-216.
18. Cullen, J., Phillips, M.C., Shipley, G.G., 1971. The effects of temperature on the composition and physical properties of the lipids of Pseudomonas fluorescens. Biochem. J., 125, 733-742.
19. De Mendoza, D., Cronan, J.E., 1983. Thermal regulation of membrane lipid fluidity in bacteria. Trends Biochem. Sci., 8, 49-52.
20. Ellis, R.J., van der Vies, S. M., 1991. Molecular chaperones. Annu. Rev. Biochem., 60, 321-347.
21. Farber, J.M., Brown, B.E., 1990. Effect of prior heat shock on heat resistance of Listeria monocytogenes in meat. Appl. Environ. Microbiol., 56, 1584-1587.
22. Farewell, A., Neidhardt, F.C., 1998. Effect of temperature on in vivo protein synthesis capacity of Escherichia coli. J. Bacteriol., 180, 4704-4710.
23. Farris, M., Grant, A., Richardson, T.B., O'Connor, C.D., 1998. BipA: a tyrosine-phosphorylated GTPase that mediates interactions between enteropathogenic Escherichia coli (EPEC) and epithelial cells. Mol. Microbiol., 28, 265-279.
24. Fehlhaber, K., Kruger, G., 1998. The study of Salmonella enteritidis growth kinetics using rapid automated bacterial impedance technique. J. Appl. Microbiol., 84, 945-949.
25. Feng, Y., Huang, H., Liao, J., Cohen, S.N., 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, 31651-31656.
26. Freestone, P., Nystrom, T., Trinei, M., Norris, V., 1997. The universal stress protein, UspA, of Escherichia coli is phosphorylated in response to stasis. J. Mol. Biol., 274, 318-324.
27. Gadgil, M., Kapur, V., Hu, W.S., 2005. Transcriptional response of Escherichia coli to temperature shift. Biotechnol. Prog., 21, 689-699.
28. Goldenberg, D., Azar, I., Oppenheim, A.B., 1996. Differential mRNA stability of the cspA gene in the cold-shock response of Escherichia coli. Mol. Microbiol., 19, 241-248.
29. Görg, A., Obermaier, C., Boguth, G., Harder, A. et al., 2000. The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis, 21, 1037-1053.
30. Gounaris, A.D., Hager, L.P., 1961. A resolution of the Escherichia coli pyruvate dehydrogenase complex. J. Biol. Chem., 236, 1013-1018.
31. Gragerov, A.I., Martin, E.S., Krupenko, M.A., Kashlev, M.V. et al., 1991. Protein aggregation and inclusion body formation in Escherichia coli rpoH mutant defective in heat shock protein induction. FEBS Lett., 291, 222-224.
32. Herendeen, S.L., VanBogelen, R.A., Neidhardt, F.C., 1979. Levels of major proteins of Escherichia coli during growth at different temperatures. J. Bacteriol., 139, 185-194.
33. 32 the heat shock regulation in Escherichia coli, is governed by HflB. Proc. Natl. Acad. Sci. USA, 92, 3516-3520.
34. Ingraham, J.L., Marr, A.G., 1963. Control of enzyme biosynthesis at temperatures near the minimum for growth of Escherichia coli. Collo. Int. CNRS, 124, 319-328.
35. Jaenicke, R., 1991. Protein folding: local structures, domains, subunits, assemblies. Biochem., 30, 3147-3161.
36. Jiang, W., Hou, Y., Inouye, M., 1997. CspA, the major cold-shock protein of Escherichia coli is an RNA chaperone. J. Biol. Chem., 272, 196-202.
37. Jones, P.G., VanBogelen, R.A., Neidhardt, F.C., 1987. Induction of proteins in response to low temperature in Escherichia coli. J. Bacteriol., 169, 2029-2095.
38. Kadner, R.J., 1996. Cytoplasmic membrane. p. 58-87. In: F.C. Neidhardt et al. (eds.), Escherichia coli and Salmonella: Cellular and Molecular Biology ASM Press, Washington, D.C. pp. 58-87
39. Kerridge, D., 1960. The effect of inhibitors on the formation of flagella by Salmonella typhimurium. J. Gen. Microbiol., 23, 519-538.
40. Knivett, V.A., Cullen, J., 1965. Some factors affecting cyclopropane acid formation in Escherichia coli. Biochem. J., 96, 771-776.
41. Lelivelt, M.J., Kawula, T.H., 1995. Hsc66, an Hsp70 homolog in Escherichia coli, is induced by cold shock but not by heat shock. J. Bacteriol., 177, 4900-4907.
42. Marr, A.G., Ingraham, J.L., Squires, C.L., 1964. Effect of the temperature of growth of Escherichia coli on the formation of β -galactosidase. J. Bacteriol., 87, 356-362.
43. McGroarty, E.J., Koffler, H., Smith, R.W., 1973. Regulation of flagellar morphogenesis by temperature: involvement of the bacterial cell surface in the synthesis of flagellin and the flagellum. J. Bacteriol., 113, 295-303.
44. Mejia, R., Carmen Gomez-Eichelmann, M., Fernandez, M.S., 1995. Membrane fluidity of Escherichia coli during heat-shock. Biochim. Biophys. Acta, 1239, 195-200.
45. Mihoub, F., Mistou, M.-Y., Guillot, A., Leveau, J.-Y., et al., 2003. Cold adaptation of Escherichia coli: microbiological and proteomic approaches. Int. J. Food Microbiol., 89, 171-184.
46. Morrison, R.B., 1961. The effect of temperature and chloramphenicol on the development of flagella and motility in a strain of Escherichia coli. J. Path. Bacteriol., 82, 189-192.
47. Morrison, R.B., McCapra, J., 1961. Flagellar changes in Escherichia coli induced by temperature of the environment. Nature (London), 192, 774-776.
48. Neuhaus, K., Rapposch, S., Francis, K.P., Scherer, S., 2000. Restart of exponential growth of cold-shocked Yersinia enterocolitica occurs after down regulation of cspA1/A2 mRNA. J. Bacteriol., 182, 3285-3288.
49. Okuyama, H., 1969. Phospholipid metabolism in Escherichia coli after a shift in temperature. Biochim. Biophys. Acta, 176, 125-134.
50. Pfennig, P.L., Flower, A.M., 2001. BipA is required for growth of Escherichia coli K12 at low temperature. Mol. Genet. Genomics, 266, 313-317.
51. Phadtare, S., Inouye, M., 2001. Role of CspC and CspE in regulation of expression of RpoS and UspA, the stress response proteins in Escherichia coli. J. Bacteriol., 183, 1205-1214.
52. Preston, N.W., Maitland, H.B., 1952. The influence of temperature on the motility of Pasteurella pseudotuberculosis. J. Gen. Microbiol., 7, 117-128.
53. Qi, S.Y., Li, Y., Szyroki, A., Giles, I.G. et al., 1995. Salmonella typhimurium responses to a bactericidal protein from human neutrophils. Mol. Microbiol., 17, 523-531.
54. Qin, J.-H., Sheng, Y.-Y., Zhang, Z.-M., Shi, Y.-Z. et al., Date 2006. Genome-wide transcriptional analysis of temperature shift in L. interrogans serovar lai strain 56601 BMC Microbiol. 6. Available from: http://www.biomedcentral.com/1471-2180/6/51.
55. Quadling, C., Stocker, B.A.D., 1962. An environmentally induced transition from the flagellated to the non-flagellated state in Salmonella: the fate of parental flagella at cell division. J. Gen. Microbiol., 28, 257-270.
56. Raina, S., Mabey, L., Georgopoulos, C., 1991. The Escherichia coli htrP gene product is essential for bacterial growth at high temperatures: mapping, cloning, sequencing, transcriptional regulation of htrP. J. Bacteriol., 173, 5999-6008.
57. Riehle, M.M., Bennett, A.F., Lenski, R.E., Long, A.D., 2003. Evolutionary changes in heat-inducible gene expression in lines of Escherichia coli adapted to high temperature. Physiol. Genomics, 14, 47-58.
58. Sasser, M., 1990. Bacterial identification by gas chromatographic analysis of fatty acids methyl esters (GC-FAME). MIDI Technical note #101.
59. Scott, K., Diggle, M.A., Clarke, S.C., 2003. TypA is a virulence regulator and is present in many pathogenic bacteria. Braz. J. Biomed. Sci., 60, 168-170.
60. Shaw, M.K., Murr, A.C., Ingraham, J.L., 1971. Determination of the minimal temperature for growth of Escherichia coli. J. Bacteriol., 105, 683-684.
61. Sklar, J.G., Wu, T., Kahne, D., Silhavy, T.J., 2007. Defining the roles of the periplasmic chaperones SurA, Skp, DegP in Escherichia coli. Genes Dev., 21, 2473-2484.
62. 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. EMBO J., 15, 3993-4000.
63. Smirnova, G.V., Muzyka, N.G., Oktyabrsky, O.N., 2007. Enhanced resistance to peroxide stress in Escherichia coli grown outside their niche temperatures. J. Therm. Biol., 32, 321-327.
64. Smith, L.T., 1996. Role of osmolytes in adaptation of osmotically stressed and chill-stressed Listeria monocytogenes grown in liquid media and on processed meat surfaces. Appl. Environ. Microbiol., 62, 3088-3093.
65. Suutari, M., 1992. Fatty acids in temperature adaptation of mesophilic bacteria, yeasts and fungi. In: vol. Ph.D. Thesis. Helsinki University of Technology, Helsinki, Finland.
66. Suutari, M., Laakso, S., 1994. Microbial fatty acids and thermal adaptation. Crit. Rev. Microbiol., 20, 285-328.
67. Thieringer, H.A., Jones, P.G., Inouye, M., 1998. Cold shock and adaptation. Bioessays, 20, 49-57.
68. 32. EMBO J., 14, 2551-2560.
69. Verheul, A., Glaasker, E., Poolman, B., Abee, T., 1997. Betaine and L-carnitine transport by Listeria monocytogenes Scott A in response to osmotic signals. J. Bacteriol., 179, 6979-6985.
70. Vuong, P., Bennion, D., Mantei, J., Frost, D., et al., 2008. Analysis of YfgL and YaeT interactions through bioinformatics, mutagenesis, and biochemistry. J. Bacteriol., 190, 1507-1517.
71. Werner, J., Misra, R., 2005. YaeT (Omp85) affects the assembly of lipid-dependent and lipid-independent outer membrane proteins of Escherichia coli. Mol. Microbiol., 57, 1450-1459.
72. Woodcock, E., Grigg, G.C., 1972. Repair of thermally induced DNA breakage in Escherichia coli. Nat. New Biol., 237, 76-79.
73. Wouters, J.A., Kampelmacher, E.H., Hugenholtz, J., Kuipers, O.P., et al., 2000. Changes in glycolytic activity of Lactococcus lactis induced by low temperature. Appl. Environ. Microbiol., 66, 3686-3691.
74. Wu, T., Malinverni, J., Ruiz, N., Kim, S., et al., 2005. Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell, 121, 235-245.
75. Yamamori, T., Ito, K., Nakamura, Y., Yura, T., 1978. Transient regulation of protein synthesis in Escherichia coli upon shift-up of growth temperature. J. Bacteriol., 134, 1133-1140.
76. Yamanaka, K., 1999. Cold shock response in Escherichia coli. J. Mol. Microbiol. Biotechnol., 1, 193-202.
77. Yamanaka, K., Inouye, M., 2001. Selective mRNA degradation by polynucleotide phosphorylase in cold shock adaptation in Escherichia coli. J. Bacteriol., 183, 2808-2816.
78. Yamanaka, K., Ogura, T., Koonin, E.V., Niki, H., et al., 1994. Multicopy suppressors, mssA amd mssB, of an smbA mutation of Escherichia coli. Mol. Gen. Genet., 243, 9-16.
79. Yuk, H.-G., Marshall, D.L., 2003. Heat adaptation alters Escherichia coli O157:H7 membrane lipid composition and verotoxin production. Appl. Environ. Microbiol., 69, 5115-5119.
80. Yura, T., Nagai, H., Mori, H., 1993. Regulation of the heat-shock response in bacteria. Annu. Rev. Microbiol., 47, 321-350.
81. TMtargets for MALDI-MS and MS/MS and its application in the liver proteome project. Proteomics, 7, 2340-2349.