Response of Lactobacillus helveticus PR4 to heat stress during propagation in cheese whey with a gradient of decreasing temperatures

Applied and Environmental Microbiology

Volumn 72, Issue 7, 2006, Pages 4503-4514

  Di Cagno, Raffaella ^a   De Angelis, Maria ^a,c   Limitone, Antonio ^a   Fox, Patrick F ^b   Gobbetti, Marco ^a  

^a UNIVERSITY OF BARI   (Italy)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c Facolta di Agraria di Bari   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELLS; DNA; ELECTROPHORESIS; ENZYMES; GROWTH KINETICS; LASER PULSES; MASS SPECTROMETRY; THERMAL EFFECTS; THERMAL STRESS;

DNA-BINDING PROTEIN; LACTOBACILLUS HELVETICUS; PEPTIDASE; PROTEINASE; STRESS PROTEIN;

BACTERIA;

ADENOSINE TRIPHOSPHATE DEPENDENT PROTEINASE; CHAPERONIN; DNA BINDING PROTEIN; ENOLASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEAT SHOCK PROTEIN; PEPTIDASE; PROTEIN DNAK; PROTEINASE; REGULATOR PROTEIN;

BACTERIUM; PROTEIN; STRESS; TEMPERATURE EFFECT; TEMPERATURE TOLERANCE;

ACIDIFICATION; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GROWTH; CELL GROWTH; CHEESEMAKING; GLYCOLYSIS; HEAT ACCLIMATIZATION; HEAT STRESS; LACTOBACILLUS HELVETICUS; LACTOBACILLUS HELVETICUS PR4; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; TEMPERATURE DEPENDENCE; TWO DIMENSIONAL ELECTROPHORESIS; WHEY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CHEESE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION REGULATION, BACTERIAL; HEAT; HEAT-SHOCK RESPONSE; KINETICS; LACTOBACILLUS HELVETICUS; MOLECULAR SEQUENCE DATA; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TEMPERATURE;

LACTOBACILLUS HELVETICUS;

EID: 33746032577     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.01829-05     Document Type: Article

References (48)

1. Appel, R. D., and D. F. Hochstrasser. 1999. Computer analysis of 2-D images. Methods Mol. Biol. 112:383-391.
2. Bini, L., B. Magi, B. Marzocchi, F. Arcuri, S. Tripodi, M. Cintorino, J. C. Sanchez, S. Frutiger, G. Hughes, V. Pallini, D. F. Hochstrasser, and P. Tosi. 1997. Protein expression profiles in human breast ductal carcinoma and histologically normal tissue. Electrophoresis 18:2832-2841.
3. Bjellqvist, B., G. J. Hughes, C. Pasquali, N. Paquet, F. Ravier, J. C. Sanchez, S. Fructiger, and D. F. Hochstrasser. 1993. The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences. Electrophoresis 14:1023-1031.
4. 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.
5. Broadbent, J. R., J. C. Oberg, and L. Wie. 1998. Characterization of the Lactobacillus helveticus groESL operon. Res. Microbiol. 149:247-253.
6. Broadbent, J. R., J. C. Oberg, H. Wang, and L. Wie. 1997. Attributes of the heat shock response in three species of dairy Lactobacillus. Syst. Appl. Microbiol. 20:12-19.
7. Bukau, B, and A. L. Horwich. 1998. The Hsp70 and Hsp60 chaperone machines. Cells 92:351-366.
8. Callanan, M. J., T. P. Beresford, and R. P. Ross. 2005. Genetic diversity in the lactose operons of Lactobacillus helveticus strains and its relationship to the role of these strains as commercial starter cultures. Appl. Environ. Microbiol. 71:1655-1658.
9. Champoux, J. J. 2001. DNA topoisomerases: structure, function and mechanism. Annu. Rev. Biochem. 70:369-413.
10. De Angelis, M., and M. Gobbetti. 2004. Environmental stress response in Lactobacillus: a review. Proteomics 4:106-122.
11. De Angelis, M., R. Di Cagno, C. Huet, C. Crecchio, P. F. Fox, and M. Gobbetti. 2004. Heat shock response in Lactobacillus plantarum. Appl. Environ. Microbiol. 70:1336-1346.
12. Desmond, C., G. F. Fitzgerald, C. Stanton, and R. P. Ross. 2004. Improved stress tolerance of GroESL-overproducing Lactococcus lactis and probiotic Lactobacillus paracasei NFBC 338. Appl. Environ. Microbiol. 70:5929-5936.
13. Elli, M., L. Morelli, and R. Zink. 2002. Evidence of a role of thioredoxin reductase in oxidative stress resistance in Lactobacillus johnsonii, abstr. G9. Proceedings of the Seventh Symposium on Lactic Acid Bacteria: Genetics, Metabolism and Applications, 1 to 5 September, 2002. Kluwer Academic Publishers, Dordrecht, The Netherlands.
14. Fountoulakis, M., and H. Langen. 1997. Identification of proteins by matrix-assisted laser desorption ionization-mass spectrometry following in-gel digestion in low-salt, nonvolatile buffer and simplified peptide recovery. Anal. Biochem. 250:153-156.
15. Gagnaire, V., M. Piot, B. Camier, J. P. C. Vissers, G. Jan, and J. Léonil. 2004. Survey of bacterial proteins released in cheese: a proteomic approach. Int. J. Food Microbiol. 94:185-201.
16. Gatti, M., C. Lazzi, L. Rossetti, G. Mucchetti, and E. Neviani. 2003. Biodiversity in Lactobacillus helveticus strains present in natural whey starter used for Parmigiano Reggiano cheese. J. Appl. Microbiol. 95:463-470.
17. Gatti, M., C. Travisano, E. Fabrizi, E. Neviani, and F. Gardini. 2004. Biodiversity among Lactobacillus helveticus strain isolated from different natural whey starter cultures as revealed by classification trees. Appl. Environ. Microbial. 70:182-190.
18. Gobbetti, M. 2004. Extra-hard varieties, p. 51-70. In P. F. Fox, P. L. H. McSweeney, T. M. Cogan, and T. P. Guinee (ed.), Cheese: chemistry, physics and microbiology. Elsevier Academic Press, San Diego, Calif.
19. Gobbetti, M., B. Folkertsma, P. F. Fox, A. Corsetti, E. Smacchi, M. De Angelis, J. Rossi, K. Kilcawley, and M. Cortini. 1999. Microbiology and biochemistry of Fossa (pit) cheese. Intern. Dairy J. 9:763-773.
20. Gorg, A., W. Postel, and S. Gunther. 1988. The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 9:531-546.
21. Guerzoni, M. E., R. Lanciotti, and P. S. Cocconcelli. 2001. Alteration in cellular fatty acid composition as a response to salt, acid, oxidative and thermal stresses in Lactobacillus helveticus. Microbiology 147:2255-2264.
22. Guimont, C., M. A. Chopard, J. L. Gaillard, and J. F. Chamba. 2002. Comparative study of the protein composition of three strains of Streptococcus thermophilus grown either in M17 medium or milk. Lait 82:645-656.
23. Hamdan, H., and P. G. Righetti. 2002. Modern strategies for protein quantification in proteome analysis: advantages and limitations. Mass. Spectrom. Rev. 21:287-302.
24. Hochstrasser, D. F., M. G. Harrington, A. C. Hochstrasser, M. J. Miller, and C. R. Merril. 1988. Methods for increasing the resolution of two dimensional protein electrophoresis. Anal. Biochem. 173:424-435.
25. Kunji, E. R. S., I. Mierau, A. Hagting, B. Poolman, and N. Konings. 1996. The proteolytic system of lactic acid bacteria. Antonie Leeuwenhoek 70:187-221.
26. Messer, M., M. Griffiths, P. D. Rismiller, and D. C. Shaw. 1997. Lactose synthesis in a monoestreme, the echidna (Tachyglossus acueatus): isolation and amino acid sequence of echidna α-lactalbumin. Comp. Biochem. Physiol. B 118:403-410.
27. Miyakawa, H., K. Anjitsu, N. Ishibashi, and S. Shimamura. 1994. Effects of pressure on enzyme-activities of Lactobacillus helveticus LHE-511. Biosci. Biotechnol. Biochem. 58:606-607.
28. Munchbach, M., P. Dainese, W. Staudenmann, F. Narberhaus, and P. James. 1999. Proteome analysis of heat shock protein expression in Bradyrhizobium japonicum. Eur. J. Biochem. 263:39-48.
29. Oakley, B. R., D. R. Kirsch, and R. Morris. 1980. A simplified ultrasensitive silver stain for detecting proteins in polyacrylamide gels. Anal. Biochem. 105:361-363.
30. Okamoto, S., and K. Ochi. 1998. An essential GTP-binding protein functions as a regulator for differentiation in Streptomyces coelicolor. Mol. Microbiol. 30:107-119.
31. Parente, E., and T. M. Cogan. 2004. Starter cultures: general aspects, p. 122-147. In P. F. Fox, P. L. H. McSweeney, T. M. Cogan, and T. P. Guinee (ed.), Cheese: chemistry, physics and microbiology. Elsevier Academic Press, San Diego, Calif.
32. Pontiggia, A., A. Negri, M. Beltrame, and M. E. Bianchi. 1993. Protein HU binds specifically to kinked DNA. Mol. Microbiol. 7:343-350.
33. Pooley, H. M., and D. Karamata. 1994. Teichoic acid synthesis in Bacillus subtilis: genetic organization and biological roles, p. 187-198. In J. M. Ghuysen, and R. Hakenbeck (ed.), Bacterial cell wall. Elsevier Science Publishers, Amsterdam, The Netherlands.
34. Prasad, J., P. McJarrow, and P. Gopal. 2003. Heat and osmotic stress responses of probiotic Lactobacillus rhamnosus HN001 (DR20) in relation to viability after drying. Appl. Environ. Microbiol. 69:917-925.
35. B stress response transcription factor cofractionate with ribosomes. J. Bacteriol. 182:2771-2777.
36. Smeds, A., P. Varmanen, and A. Palva. 1998. Molecular characterization of a stress-inducible gene from Laaobacillus helveticus. J. Bacteriol. 180:6148-6153.
37. Sridhar, V. R., J. E. Hughes, D. L. Welker, J. R. Broadbent, and J. L. Steele. 2005. Identification of endopeptidase genes from the genomic sequence of Lactobacillus helveticus CNRZ32 and the role of these genes in hydrolysis of model bitter peptides. Appl. Environ. Microbiol. 71:3025-3032.
38. Stillman, T. J., M. Upadhyay, V. A. Norte, S. E. Sedelnikova, M. Carradus, S. Tzokov, P. A. Bullough, C. A. Shearman, M. J. Gasson, C. H. Williams, P. J. Artymiuk, and J. Green. 2005. The crystal structures of Lactococcus lactis MG1363 Dps proteins reveal the presence of an N-terminal helix that is required for DNA binding. Mol. Microbiol. 57:1101-1112.
39. Tango, M. S. A., and A. E. Ghaly. 1999. Effect of temperature on lactic acid production from cheese whey using Lactobacillus helveticus under batch conditions. Biomass Bioenerg. 16:61-78.
40. Twinning, S. 1984. Fluorescein isothiocyanate-labeled casein assay for proteolytic enzyme. Anal. Biochem. 143:30-34.
41. Ueno, K., S. Mizuno, and N. Yamanoto. 2004. Purification and characterization of an endopeptidase that has an important role in the carboxyl terminal processing of antihypertensive peptides in Lactobacillus helveticus CM4. Lett. Appl. Microbiol. 39:313-318.
42. VanBogelen, R. A., and F. C. Neidhardt. 1990. Ribosomes as sensors of heat and cold shock in Escherichia coli. Proc. Natl. Acad. Sci. USA 87:5589-5593.
43. Veinger, L., S. Diamant, J. Buchner, and P. Goloubinoff. 1998. The small heat shock protein IbpB from Escherichia coli stabilises stress-denatured proteins for subsequent refolding by a multichaperone network. J. Biol. Chem. 273:11032-11037.
44. Wang, J., and L. Chen. 2003. Domain motions in GroEL upon binding of an oligopeptide. J. Mol. Biol. 334:489-499.
45. Wang, J. L., J. H. Wan, L., L. Luo, S. X. Xiong, G. H. Wang, F. C. He, and X. H. Qian. 2000. Development and preliminary application of a peptide mass fingerprinting technique in proteome research. Acta Biochem. Biophys. Sin. 32:373-378
46. Wilkins, J. C., K. A. Homer, and D. Beighton. 2002. Analysis of Streptococcus mutants proteins modulated by culture under acidic conditions. Appl. Environ. Microbiol. 68:2382-2390.
47. Wouters, J. A., H. H. Kamphuis, J. Hugenholtz, O. P. Kuipers, W. M. De Vos, and T. Abee. Changes in glycolytic activity of Lactococcus lactis induced by low temperature. Appl. Environ. Microbiol. 66:3686-3691.
48. Zwietering, M. H., I. Jongeberger, F. M. Roumbouts, and K. van't Riet. 1990. Modeling of the bacterial growth curve. Appl. Environ. Microbiol. 56:1875-1881.