Growth phase-associated changes in the proteome and transcriptome of Lactobacillus rhamnosus GG in industrial-type whey medium

Microbial Biotechnology

Volumn 4, Issue 6, 2011, Pages 746-766

  Laakso, Kati ^a   Koskenniemi, Kerttu ^b   Koponen, Johanna ^c   Kankainen, Matti ^c   Surakka, Anu ^a   Salusjärvi, Tuomas ^a   Auvinen, Petri ^c   Savijoki, Kirsi ^b   Nyman, Tuula A ^c   Kalkkinen, Nisse ^c   Tynkkynen, Soile ^a   Varmanen, Pekka ^b  

^a VALIO LTD   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE KINASE; AMIDOPHOSPHORIBOSYLTRANSFERASE; ASPARTATE CARBAMOYLTRANSFERASE; CYSTATHIONINE GAMMA LYASE; CYSTEINE SYNTHASE; DIHYDROOROTASE; DIPEPTIDYL CARBOXYPEPTIDASE; ENOLASE; EXOPOLYSACCHARIDE; FORMATE TETRAHYDROFOLATE LIGASE; GALACTOKINASE; GALACTOSE; GLUCOSE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE (NADP); LACTATE DEHYDROGENASE; LIPID; LIPOTEICHOIC ACID; NICOTINATE PHOSPHORIBOSYLTRANSFERASE; NITROREDUCTASE; PHOSPHOGLUCOMUTASE; PHOSPHOGLYCERATE KINASE; PYRIDOXAL 5 PHOSPHATE; PYRUVATE KINASE; PYRUVIC ACID; TAGATOSE; TRANSCRIPTOME; TRIOSEPHOSPHATE ISOMERASE; UNINDEXED DRUG; URACIL PHOSPHORIBOSYLTRANSFERASE; CULTURE MEDIUM; PROTEOME;

AMINO ACID METABOLISM; AMINO ACID SYNTHESIS; AMINO ACID TRANSPORT; ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL SURVIVAL; BACTERIUM ADHERENCE; BIOGENESIS; BIOREACTOR; CARBOHYDRATE METABOLISM; CARBOHYDRATE TRANSPORT; CELLULAR STRESS RESPONSE; ENERGY YIELD; FERMENTATION; GENE EXPRESSION; GENE LOCUS; GLYCOLYSIS; GROWTH CURVE; HUMAN; HYDROPHOBICITY; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS RHAMNOSUS; LIPID METABOLISM; LIPID TRANSPORT; NONHUMAN; NUCLEOTIDE TRANSPORT; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEOMICS; UPREGULATION; WHEY; CHEMISTRY; CULTURE MEDIUM; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY;

BACTERIA (MICROORGANISMS); LACTOBACILLUS RHAMNOSUS;

BIOREACTORS; CULTURE MEDIA; LACTOBACILLUS RHAMNOSUS; PROTEOME; TRANSCRIPTOME;

EID: 80054119261     PISSN: 17517907     EISSN: 17517915     Source Type: Journal    
DOI: 10.1111/j.1751-7915.2011.00275.x     Document Type: Article

References (65)

1. Alander, M., Korpela, R., Saxelin, M., Vilpponen-Salmela, T., Mattila-Sandholm, T., and von Wright, A. (1997) Recovery of Lactobacillus rhamnosus GG from human colonic biopsies. Lett Appl Microbiol 24: 361-364.
2. Alander, M., Satokari, R., Korpela, R., Saxelin, M., Vilpponen-Salmela, T., Mattila-Sandholm, T., and von Wright, A. (1999) Persistence of colonization of human colonic mucosa by a probiotic strain, Lactobacillus rhamnosus GG, after oral consumption. Appl Environ Microbiol 65: 351-354.
3. Alcántara, C., Sarmiento-Rubiano, L.A., Monedero, V., Deutscher, J., Pérez-Martínez, G., and Yebra, M.J. (2008) Regulation of Lactobacillus casei sorbitol utilization genes requires DNA-binding transcriptional activator GutR and the conserved protein GutM. Appl Environ Microbiol 74: 5731-5740.
4. Axelsson, L. (2004) Lactic acid bacteria: classification and physiology. In Lactic Acid Bacteria: Microbiological and Functional Aspects. Salminen, S., von Wright, A., and Ouwehand, A. (eds). New York, USA: Marcel Dekker, pp. 1-66.
5. Azcarate-Peril, M.A., Tallon, R., and Klaenhammer, T.R. (2009) Temporal gene expression and probiotic attributes of Lactobacillus acidophilus during growth in milk. J Dairy Sci 92: 870-886.
6. van Baarlen, P., Troost, F.J., van Hemert, S., van der Meer, C., de Vos, W.M., de Groot, P.J., etal. (2009) Differential NF-κB pathways induction by Lactobacillus plantarum in the duodenum of healthy humans correlating with immune tolerance. Proc Natl Acad Sci USA 106: 2371-2376.
7. Baldi, P., and Long, A.D. (2001) A Bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics 17: 509-519.
8. Bandow, J.E., Becher, D., Büttner, K., Hochgräfe, F., Freiberg, C., Brötz, H., and Hecker, M. (2003) The role of peptide deformylase in protein biosynthesis: a proteomic study. Proteomics 3: 299-306.
9. Claes, I.J.J., Lebeer, S., Shen, C., Verhoeven, T.L.A., Dilissen, E., De Hertogh, G., etal. (2010) Impact of lipoteichoic acid modification on the performance of the probiotic Lactobacillus rhamnosus GG in experimental cholitis. Clin Exp Immunol 162: 306-314.
10. Cohen, D.P.A., Renes, J., Bouwman, F.G., Zoetendal, E.G., Mariman, E., de Vos, W.M., and Vaughan, E.E. (2006) Proteomic analysis of log to stationary growth phase Lactobacillus plantarum cells and a 2-DE database. Proteomics 6: 6485-6493.
11. Cozzone, A.J. (1998) Post-translational modification of proteins by reversible phosphorylation in prokaryotes. Biochimie 80: 43-48.
12. De Angelis, M., and Gobbetti, M. (2004) Environmental stress responses in Lactobacillus: a review. Proteomics 4: 106-122.
13. Deepika, G., Green, R.J., Frazier, R.A., and Charalampopoulos, D. (2009) Effect of growth time on the surface and adhesion properties of Lactobacillus rhamnosus GG. J Appl Microbiol 107: 1230-1240.
14. Eymann, C., Becher, D., Bernhardt, J., Gronau, K., Klutzny, A., and Hecker, M. (2007) Dynamics of protein phosphorylation on Ser/Thr/Tyr in Bacillus subtilis. Proteomics 7: 3509-3526.
15. Francl, A.L., Thongaram, T., and Miller, M.J. (2010) The PTS transporters of Lactobacillus gasseri ATCC 33323. BMC Microbiol 10: 77.
16. Gentleman, R.C., Carey, V.J., Bates, D.M., Bolstad, B., Dettling, M., Dudoit, S., etal. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
17. Goldin, B.R., Gorbach, S.L., Saxelin, M., Barakat, S., Gualtieri, L., and Salminen, S. (1992) Survival of Lactobacillus species (strain GG) in human gastrointestinal tract. Dig Dis Sci 37: 121-128.
18. Guarino, A., Lo Vecchio, A., and Canani, R.B. (2009) Probiotics as prevention and treatment for diarrhea. Curr Opin Gastroenterol 25: 18-23.
19. Habimana, O., Le Goff, C., Juillard, V., Bellon-Fontaine, M.-N., Buist, G., Kulakauskas, S., and Briandet, R. (2007) Positive role of cell wall anchored proteinase PrtP in adhesion of lactococci. BMC Microbiol 7: 36.
20. Hatakka, K., Savilahti, E., Pönkä, A., Meurman, J.H., Poussa, T., Näse, L., etal. (2001) Effect of long term consumption of probiotic milk on infections in children attending day care centres: double blind, randomised trial. BMJ 322: 1-5.
21. Hojsak, I., Snovak, N., Abdović, S., Szajewska, H., Mišak, Z., and Kolaček, S. (2010) Lactobacillus GG in the prevention of gastrointestinal and respiratory tract infections in children who attend day care centers: a randomized, double-blind, placebo-controlled trial. Clin Nutr 29: 312-316.
22. Isolauri, E., Arvola, T., Sütas, Y., Moilanen, E., and Salminen, S. (2000) Probiotics in the management of atopic eczema. Clin Exp Allergy 30: 1604-1610.
23. Jacobsen, C.N., Rosenfeldt Nielsen, V., Hayford, A.E., Møller, P.L., Michaelsen, K.F., Pærregaard, A., etal. (1999) Screening of probiotic activities of forty-seven strains of Lactobacillus spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans. Appl Environ Microbiol 65: 4949-4956.
24. Kalliomäki, M., Salminen, S., Arvilommi, H., Kero, P., Koskinen, P., and Isolauri, E. (2001) Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet 357: 1076-1079.
25. Kalliomäki, M., Salminen, S., Poussa, T., Arvilommi, H., and Isolauri, E. (2003) Probiotics and prevention of atopic disease: 4-year follow-up of a randomised placebo-controlled trial. Lancet 361: 1869-1871.
26. Kalliomäki, M., Salminen, S., Poussa, T., and Isolauri, E. (2007) Probiotics during the first 7 years of life: a cumulative risk reduction of eczema in a randomized, placebo-controlled trial. J Allergy Clin Immunol 119: 1019-1021.
27. Kankainen, M., Paulin, L., Tynkkynen, S., von Ossowski, I., Reunanen, J., Partanen, P., etal. (2009) Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human-mucus binding protein. Proc Natl Acad Sci USA 106: 17193-17198.
28. Koistinen, K.M., Plumed-Ferrer, C., Lehesranta, S.J., Kärenlampi, S.O., and von Wright, A. (2007) Comparison of growth-phase-dependent cytosolic proteomes of two Lactobacillus plantarum strains used in food and feed fermentations. FEMS Microbiol Lett 273: 12-21.
29. Koskenniemi, K., Koponen, J., Kankainen, M., Savijoki, K., Tynkkynen, S., de Vos, W.M., etal. (2009) Proteome analysis of Lactobacillus rhamnosus GG using 2-D DIGE and mass spectrometry shows differential protein production in laboratory and industrial-type growth media. J Proteome Res 8: 4993-5007.
30. Koskenniemi, K., Laakso, K., Koponen, J., Kankainen, M., Greco, D., Auvinen, P., etal. (2011) Proteomics and transcriptomics characterization of bile stress response in probiotic Lactobacillus rhamnosus GG. Mol Cell Proteomics 10: M110.002741.
31. Laparra, J.M., and Sanz, Y. (2009) Comparison of in vitro models to study bacterial adhesion to the intestinal epithelium. Lett Appl Microbiol 49: 695-701.
32. Lebeer, S., Verhoeven, T.L.A., Perea Vélez, M., Vanderleyden, J., and De Keersmaecker, S.C.J. (2007) Impact of environmental and genetic factors on biofilm formation by the probiotic strain Lactobacillus rhamnosus GG. Appl Environ Microbiol 73: 6768-6775.
33. Lebeer, S., Vanderleyden, J., and De Keersmaecker, S.C.J. (2008) Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 72: 728-764.
34. Lebeer, S., Verhoeven, T.L.A., Francius, G., Schoofs, G., Lambrichts, I., Dufrêne, Y., etal. (2009) Identification of a gene cluster for the biosynthesis of a long, galactose-rich exopolysaccharide in Lactobacillus rhamnosus GG and functional analysis of the priming glycosyltransferase. Appl Environ Microbiol 75: 3554-3563.
35. Lebeer, S., Vanderleyden, J., and De Keersmaecker, S.C.J. (2010) Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat Rev Microbiol 8: 171-184.
36. Lebeer, S., Claes, I.J.J., Verhoeven, T.L.A., Vanderleyden, J., and De Keersmaecker, S.C.J. (2011) Exopolysaccharides of Lactobacillus rhamnosus GG form a protective shield against innate immune factors in the intestine. Microb Biotechnol 4: 368-374.
37. Macek, B., Mijakovic, I., Olsen, J.V., Gnad, F., Kumar, C., Jensen, P.R., and Mann, M. (2007) The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis. Mol Cell Proteomics 6: 697-707.
38. Macek, B., Gnad, F., Soufi, B., Kumar, C., Olsen, J.V., Mijakovic, I., and Mann, M. (2008) Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation. Mol Cell Proteomics 7: 299-307.
39. Majamaa, H., and Isolauri, E. (1997) Probiotics: a novel approach in the management of food allergy. J Allergy Clin Immunol 99: 179-185.
40. Mandlik, A., Swierczynski, A., Das, A., and Ton-That, H. (2008) Pili in Gram-positive bacteria: assembly, involvement in colonization and biofilm development. Trends Microbiol 16: 33-40.
41. Näse, L., Hatakka, K., Savilahti, E., Saxelin, M., Pönkä, A., Poussa, T., etal. (2001) Effect of long-term consumption of a probiotic bacterium, Lactobacillus rhamnosus GG, in milk on dental caries and caries risk in children. Caries Res 35: 412-420.
42. Neuhaus, F.C., and Baddiley, J. (2003) A continuum of anionic charge: structures and functions of d-alanyl-teichoic acids in gram-positive bacteria. Microbiol Mol Biol Rev 67: 686-723.
43. Neves, A.R., Wietske, A.P., Kok, J., Kuipers, O.P., and Santos, H. (2005) Overview on sugar metabolism and its control in Lactococcus lactis - the input from in vivo NMR. FEMS Microbiol Rev 29: 531-554.
44. O'Connell, K.L., and Stults, J.T. (1997) Identification of mouse liver proteins on two-dimensional electrophoresis gels by matrix-assisted laser desorption/ionization mass spectrometry of in situ enzymatic digests. Electrophoresis 18: 349-359.
45. Ouwehand, A.C., Tuomola, E.M., Tölkkö, S., and Salminen, S. (2001) Assessment of adhesion properties of novel probiotic strains to human intestinal mucus. Int J Food Microbiol 64: 119-126.
46. Ritchie, M.E., Silver, J., Oshlack, A., Holmes, M., Diyagama, D., Holloway, A., and Smyth, G.K. (2007) A comparison of background correction methods for two-colour microarrays. Bioinformatics 23: 2700-2707.
47. Saeed, A.I., Bhagabati, N.K., Braisted, J.C., Liang, W., Sharov, V., Howe, E.A., etal. (2006) TM4 microarray software suite. Methods Enzymol 411: 134-193.
48. Sánchez, B., Bressollier, P., Chaignepain, S., Schmitter, J.-M., and Urdaci, M.C. (2009) Identification of surface-associated proteins in the probiotic bacterium Lactobacillus rhamnosus GG. Int Dairy J 19: 85-88.
49. Savijoki, K., Ingmer, H., and Varmanen, P. (2006) Proteolytic systems of lactic acid bacteria. Appl Microbiol Biotechnol 71: 394-406.
50. Seth, A., Yan, F., Polk, D.B., and Rao, R.K. (2008) Probiotics ameliorate the hydrogen peroxide-induced epithelial barrier disruption by a PKC- and MAP kinase-dependent mechanism. Am J Physiol Gastrointest Liver Physiol 294: G1060-G1069.
51. Smyth, G.K. (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article 3.
52. Smyth, G.K., and Speed, T. (2003) Normalization of cDNA microarray data. Methods 31: 265-273.
53. Song, X.-M., Connor, W., Hokamp, K., Babiuk, L.A., and Potter, A.A. (2009) The growth phase-dependent regulation of the pilus locus genes by two-component system TCS08 in Streptococcus pneumoniae. Microb Pathog 46: 28-35.
54. Soufi, B., Gnad, F., Jensen, P.R., Petranovic, D., Mann, M., Mijakovic, I., and Macek, B. (2008) The Ser/Thr/Tyr phosphoproteome of Lactococcus lactis IL1403 reveals multiply phosphorylated proteins. Proteomics 8: 3486-3493.
55. Szajewska, H., Kotowska, M., Mrukowicz, J.Z., Armańska, M., and Mikolajczyk, W. (2001) Efficacy of Lactobacillus GG in prevention of nosocomial diarrhea in infants. J Pediatr 138: 361-365.
56. Szajewska, H., Skórka, A., Ruszczyński, M., and Gieruszczak-Białek, D. (2007) Meta-analysis: Lactobacillus rhamnosus GG for treating acute diarrhoea in children. Aliment Pharmacol Ther 25: 871-881.
57. Tao, Y., Drabik, K.A., Waypa, T.S., Musch, M.W., Alverdy, J.C., Schneewind, O., etal. (2006) Soluble factors from Lactobacillus GG activate MAPKs and induce cytoprotective heat shock proteins in intestinal epithelial cells. Am J Physiol Cell Physiol 290: C1018-C1030.
58. Tuomola, E.M., Ouwehand, A.C., and Salminen, S.J. (2000) Chemical, physical and enzymatic pre-treatments of probiotic lactobacilli alter their adhesion to human intestinal mucus glycoproteins. Int J Food Microbiol 60: 75-81.
59. Vélez, M.P., Petrova, M.I., Lebeer, S., Verhoeven, T.L., Claes, I., Lambrichts, I., etal. (2010) Characterization of MabA, a modulator of Lactobacillus rhamnosus GG adhesion and biofilm formation. FEMS Immunol Med Microbiol 59: 386-398.
60. Welman, A., Maddox, I., and Archer, R. (2003) Exopolysaccharide and extracellular metabolite production by Lactobacillus delbrueckii subsp. bulgaricus, grown on lactose in continuous culture. Biotechnol Lett 25: 1515-1520.
61. Welman, A.D., Maddox, I.S., and Archer, R.H. (2006) Metabolism associated with raised metabolic flux to sugar nucleotide precursors of exopolysaccharides in Lactobacillus delbrueckii subsp. bulgaricus. J Ind Microbiol Biotechnol 33: 391-400.
62. Yan, F., and Polk, D.B. (2002) Probiotic bacterium prevents cytokine-induced apoptosis in intestinal epithelial cells. J Biol Chem 277: 50959-50965.
63. Yan, F., Cao, H., Cover, T.L., Whitehead, R., Washington, M.K., and Polk, D.B. (2007) Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology 132: 562-575.
64. Yang, Y.H., and Thorne, N.P. (2003) Normalization for two-color cDNA microarray data. In Science and Statistics: A Festschrift for Terry Speed. Goldstein, D.R. (ed.). Beachwood, OH, USA: Institute of Mathematical Statistics, pp. 403-418.
65. Zhang, Y.-M., and Rock, C.O. (2009) Transcriptional regulation in bacterial membrane lipid synthesis. J Lipid Res 50: S115-S119.