Stressors and Food Environment: Toward Strategies to Improve Robustness and Stress Tolerance in Probiotics

Probiotics, Prebiotics, and Synbiotics: Bioactive Foods in Health Promotion

Volumn , Issue , 2016, Pages 245-256

  Capozzi, Vittorio ^a   Arena, Mattia Pia ^a   Russo, Pasquale ^a   Spano, Giuseppe ^a   Fiocco, Daniela ^a  

^a UNIVERSITY OF FOGGIA   (Italy)

Author keywords

Bifidobacterium; Food; Lactic acid bacteria; Lactobacillus; Prebiotic; Probiotic; Probiotic robustness; Stress response; Stress tolerance; Stressor

Indexed keywords

EID: 84967214944     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-0-12-802189-7.00016-2     Document Type: Chapter

References (89)

1. Ananta E., Knorr D. Evidence on the role of protein biosynthesis in the induction of heat tolerance of Lactobacillus rhamnosus GG by pressure pre-treatment. Int. J. Food Microbiol. 2004, 96:307-313.
2. Ananta E., Volkert M., Knorr D. Cellular injuries and storage stability of spray-dried Lactobacillus rhamnosus GG. Int. Dairy J. 2005, 15:399-409.
3. Azcarate-Peril M.A., McAuliffe O., Altermann E., Lick S., Russell W.M., Klaenhammer T.R. Microarray analysis of a two-component regulatory system involved in acid resistance and proteolytic activity in Lactobacillus acidophilus. Appl. Environ. Microbiol. 2005, 71:5794-5804.
4. Berger B., Moine D., Mansourian R., Arigoni F. HspR mutations are naturally selected in Bifidobacterium longum when successive heat shock treatments are applied. J. Bacteriol. 2010, 192:256-263.
5. Bove P., Russo P., Capozzi V., Gallone A., Spano G., Fiocco D. Lactobacillus plantarum passage through an oro-gastro-intestinal tract simulator: carrier matrix effect and transcriptional analysis of genes associated to stress and probiosis. Microbiol. Res. 2013, 168:351-359.
6. Broadbent J.R., Larsen R.L., Deibel V., Steele J.L. Physiological and transcriptional response of Lactobacillus casei ATCC 334 to acid stress. J. Bacteriol. 2010, 192:2445-2458.
7. Bron P.A., Marco M., Hoffer S.M., Mullekom E.V., de Vos W.M., Kleerebezem M. Genetic characterization of the bile salt response in Lactobacillus plantarum and analysis of responsive promoters in vitro and in situ in the gastrointestinal tract. J. Bacteriol. 2004, 186:7829-7835.
8. Bron P.A., Grangette C., Mercenier A., de Vos W.M., Kleerebezem M. Identification of Lactobacillus plantarum genes that are induced in the gastrointestinal tract of mice. J. Bacteriol. 2004, 186:5721-5729.
9. Capozzi V., Fiocco D., Amodio M.L., Gallone A., Spano G. Bacterial stressors in minimally processed food. Int. J. Mol. Sci. 2009, 10:3076-3105.
10. Capozzi V., Arena M.P., Crisetti E., Spano G., Fiocco D. The hsp 16 gene of the probiotic Lactobacillus acidophilus is differently regulated by salt, high temperature and acidic stresses, as revealed by reverse transcription quantitative PCR (qRT-PCR) analysis. Int. J. Mol. Sci. 2011, 12:5390-5405.
11. Capozzi V., Fiocco D., Spano G. Responses of lactic acid bacteria to cold stress. Stress Responses of Lactic Acid Bacteria, Food Microbiology and Food Safety 2011, 91-110. Springer, US. E. Tsakalidou, K. Papadimitriou (Eds.).
12. Capozzi V., Weidmann S., Fiocco D., Rieu A., Hols P., Guzzo J., Spano G. Inactivation of a small heat shock protein affects cell morphology and membrane fluidity in Lactobacillus plantarum WCFS1. Res. Microbiol. 2011, 162:419-425.
13. Capozzi V., Fiocco D., Weidmann S., Guzzo J., Spano G. Increasing membrane protection in Lactobacillus plantarum cells overproducing small heat shock proteins. Ann. Microbiol. 2012, 62:517-522.
14. Chotiko A., Sathivel S. Effects of enzymatically-extracted purple rice bran fiber as a protectant of L. plantarum NRRL B-4496 during freezing, freeze drying, and storage. LWT-Food Sci. Technol. 2014, 59:59-64.
15. Cohen D.P.A., Renes J., Bouwman F.G., Zoetendal E.G., Mariman E., de Vos W.M., Vaughan E.E. Proteomic analysis of log to stationary growth phase Lactobacillus plantarum cells and a 2-DE database. Proteomics 2006, 6:6485-6493.
16. Collado M.C., Moreno Y., Cobo J.M., Hernández M. Microbiological evaluation and molecular characterization of bifidobacteria strains in commercial fermented milks. Eur. Food Res. Technol. 2006, 222:112-117.
17. Collado M.C., Gueimonde M., Sanz Y., Salminen S. Adhesion properties and competitive pathogen exclusion ability of bifidobacteria with acquired acid resistance. J. Food Prot. 2006, 69:1675-1679.
18. Collado M.C., Sanz Y. Induction of acid resistance in Bifidobacterium: a mechanism for improving desirable traits of potentially probiotic strains. J. Appl. Microbiol. 2007, 103:1147-1157.
19. Corcoran B.M., Ross R.P., Fitzgerald G.F., Stanton C. Comparative survival of probiotic lactobacilli spray-dried in the presence of prebiotic substances. J. Appl. Microbiol. 2004, 96:1024-1039.
20. Corcoran B.M., Stanton C., Fitzgerald G.F., Ross R.P. Survival of probiotic lactobacilli in acidic environments is enhanced in the presence of metabolizable sugars. Appl. Environ. Microbiol. 2005, 71:3060-3067.
21. Corcoran B.M., Ross R.P., Fitzgerald G.F., Dockery P., Stanton C. Enhanced survival of GroESL-overproducing Lactobacillus paracasei NFBC 338 under stressful conditions induced by drying. Appl. Environ. Microbiol. 2006, 72:5104-5107.
22. Corcoran B.M., Stanton C., Fitzgerald G., Ross R.P. Life under stress: the probiotic stress response and how it may be manipulated. Curr. Pharm. Des. 2008, 14:1382-1399.
23. De Angelis M., Gobbetti M. Environmental stress responses in Lactobacillus: a review. Proteomics 2004, 4:106-122.
24. De Angelis M.D., Cagno R.D., Huet C., Crecchio C., Fox P.F., Gobbetti M. Heat shock response in Lactobacillus plantarum. Appl. Environ. Microbiol. 2004, 70:1336-1346.
25. Del Piano M., Carmagnola S., Ballarè M., Sartori M., Orsello M., Balzarini M., Pagliarulo M., Tari R., Anderloni A., Strozzi G.P., Mogna L., Sforza F., Capurso L. Is microencapsulation the future of probiotic preparations? The increased efficacy of gastro-protected probiotics. Gut Microbes 2011, 2:120-123.
26. Derzelle S., Hallet B., Ferain T., Delcour J., Hols P. Improved adaptation to cold-shock, stationary-phase, and freezing stresses in Lactobacillus plantarum overproducing cold-shock proteins. Appl. Environ. Microbiol. 2003, 69:4285-4290.
27. Desmond C., Stanton C., Fitzgerald G.F., Collins K., Paul Ross R. Environmental adaptation of probiotic lactobacilli towards improvement of performance during spray drying. Int. Dairy J. 2002, 11:801-808.
28. Desmond C., Fitzgerald G.F., Stanton C., Ross R.P. Improved stress tolerance of GroESL-overproducing Lactococcus lactis and probiotic Lactobacillus paracasei NFBC 338. Appl. Environ. Microbiol. 2004, 70:5929-5936.
29. Ding W.K., Shah N.P. Acid, bile, and heat tolerance of free and microencapsulated probiotic bacteria. J. Food Sci. Technol. 2007, 72:M446-M450.
30. Doleyres Y., Fliss I., Lacroix C. Increased stress tolerance of Bifidobacterium longum and Lactococcus lactis produced during continuous mixed-strain immobilized-cell fermentation. J. Appl. Microbiol. 2004, 97:527-539.
31. du Toit E., Vesterlund S., Gueimonde M., Salminen S. Assessment of the effect of stress-tolerance acquisition on some basic characteristics of specific probiotics. Int. J. Food Microbiol. 2013, 165:51-56.
32. El Demerdash H.A., Oxmann J., Heller K.J., Geis A. Yoghurt fermentation at elevated temperatures by strains of Streptococcus thermophilus expressing a small heat-shock protein: application of a two-plasmid system for constructing food-grade strains of Streptococcus thermophilus. Biotechnol. J. 2006, 1:398-404.
33. FAO/WHO Guidelines for the Evaluation of Probiotics in Food 2002, Food and Agriculture Organization of the United Nations and World Health Organization, Ontario, Canada.
34. Fernandez A., Ogawa J., Penaud S., Boudebbouze S., Ehrlich D., van de Guchte M., Maguin E. Rerouting of pyruvate metabolism during acid adaptation in Lactobacillus bulgaricus. Proteomics 2008, 8:3154-3163.
35. Fiocco D., Capozzi V., Goffin P., Hols P., Spano G. Improved adaptation to heat, cold, and solvent tolerance in Lactobacillus plantarum. Appl. Microbiol. Biotechnol. 2007, 77:909-915.
36. Fiocco D., Crisetti E., Capozzi V., Spano G. Validation of an internal control gene to apply reverse transcription quantitative PCR to study heat, cold and ethanol stresses in Lactobacillus plantarum. World J. Microbiol. Biotechnol. 2007, 24:899-902.
37. Fiocco D., Capozzi V., Pepe D., Crisetti E., Spano G. Sulphite stress induce small heat shock genes in wine Lactobacillus plantarum. Res. J. Microbiol. 2007, 2:838-844.
38. Fiocco D., Collins M., Muscariello L., Hols P., Kleerebezem M., Msadek T., Spano G. The Lactobacillus plantarum ftsH gene is a novel member of the CtsR stress response regulon. J. Bacteriol. 2009, 191:1688-1694.
39. Fiocco D., Capozzi V., Collins M., Gallone A., Hols P., Guzzo J., Weidmann S., Rieu A., Msadek T., Spano G. Characterization of the CtsR stress response regulon in Lactobacillus plantarum. J. Bacteriol. 2010, 192:896-900.
40. G-Alegría E., López I., Ruiz J.I., Sáenz J., Fernández E., Zarazaga M., Dizy M., Torres C., Ruiz-Larrea F. High tolerance of wild Lactobacillus plantarum and Oenococcus oeni strains to lyophilisation and stress environmental conditions of acid pH and ethanol. FEMS Microbiol. Lett. 2004, 230:53-61.
41. Gawkowski D., Chikindas M.L. Non-dairy probiotic beverages: the next step into human health. Benefic. Microbes 2013, 4:127-142.
42. Glaasker E., Tjan F.S.B., Steeg P.F.T., Konings W.N., Poolman B. Physiological response of Lactobacillus plantarum to salt and nonelectrolyte stress. J. Bacteriol. 1998, 180:4718-4723.
43. Govender M., Choonara Y.E., Kumar P., du Toit L.C., van Vuuren S., Pillay V. A review of the advancements in probiotic delivery: conventional vs. non-conventional formulations for intestinal flora supplementation. AAPS PharmSciTech 2014, 15:29-43.
44. Grześkowiak Ł., Isolauri E., Salminen S., Gueimonde M. Manufacturing process influences properties of probiotic bacteria. Br. J. Nutr. 2011, 105:887-894.
45. Gueimonde M., Margolles A., de los Reyes-Gavilán C.G., Salminen S. Competitive exclusion of enteropathogens from human intestinal mucus by Bifidobacterium strains with acquired resistance to bile-a preliminary study. Int. J. Food Microbiol. 2007, 113:228-232.
46. Guzzo J. Biotechnical applications of small heat shock proteins from bacteria. Int. J. Biochem. Cell Biol. 2012, 44:1698-1705.
47. Krasaekoopt W., Bhandari B., Deeth H. The influence of coating materials on some properties of alginate beads and survivability of microencapsulated probiotic bacteria. Int. Dairy J. 2004, 14:737-743.
48. Lee K., Rho B.-S., Pi K., Kim H.-J., Choi Y.-J. Proteomic analysis of protein expression in Lactobacillus plantarum in response to alkaline stress. J. Biotechnol. 2011, 153:1-7.
49. Li B., Tian F., Liu X., Zhao J., Zhang H., Chen W. Effects of cryoprotectants on viability of Lactobacillus reuteri CICC6226. Appl. Microbiol. Biotechnol. 2011, 92:609-616.
50. Makinen K., Berger B., Bel-Rhlid R., Ananta E. Science and technology for the mastership of probiotic applications in food products. J. Biotechnol. 2012, 162:356-365.
51. Marco M.L., Tachon S. Environmental factors influencing the efficacy of probiotic bacteria. Curr. Opin. Biotechnol. 2013, 24:207-213.
52. Marco M.L., Peters T.H.F., Bongers R.S., Molenaar D., Van Hemert S., Sonnenburg J.L., Gordon J.I., Kleerebezem M. Lifestyle of Lactobacillus plantarum in the mouse caecum. Environ. Microbiol. 2009, 11:2747-2757.
53. Maus J.E., Ingham S.C. Employment of stressful conditions during culture production to enhance subsequent cold-and acid-tolerance of bifidobacteria. J. Appl. Microbiol. 2003, 95:146-154.
54. Mills S., Stanton C., Fitzgerald G.F., Ross R.P. Enhancing the stress responses of probiotics for a lifestyle from gut to product and back again. Microb. Cell Fact. 2011, 10:S19.
55. Muller J.A., Ross R.P., Sybesma W.F.H., Fitzgerald G.F., Stanton C. Modification of the technical properties of Lactobacillus johnsonii NCC 533 by supplementing the growth medium with unsaturated fatty acids. Appl. Environ. Microbiol. 2011, 77:6889-6898.
56. Pan X., Wu T., Zhang L., Cai L., Song Z. Influence of oligosaccharides on the growth and tolerance capacity of lactobacilli to simulated stress environment. Lett. Appl. Microbiol. 2009, 48:362-367.
57. Parente E., Ciocia F., Ricciardi A., Zotta T., Felis G.E., Torriani S. Diversity of stress tolerance in Lactobacillus plantarumLactobacillus pentosus and Lactobacillus paraplantarum: a multivariate screening study. Int. J. Food Microbiol. 2010, 144:270-279.
58. Peighambardoust S.H., Golshan Tafti A., Hesari J. Application of spray drying for preservation of lactic acid starter cultures: a review. Trends Food Sci. Technol. 2011, 22:215-224.
59. Pieterse B., Leer R.J., Schuren F.H.J., van der Werf M.J. Unraveling the multiple effects of lactic acid stress on Lactobacillus plantarum by transcription profiling. Microbiology 2005, 151:3881-3894.
60. Rivera-Espinoza Y., Gallardo-Navarro Y. Non-dairy probiotic products. Food Microbiol. 2010, 27:1-11.
61. Russo P., de la Luz Mohedano M., Capozzi V., de Palencia P.F., López P., Spano G., Fiocco D. Comparative proteomic analysis of Lactobacillus plantarum WCFS1 and ΔctsR mutant strains under physiological and heat stress conditions. Int. J. Mol. Sci. 2012, 13:10680-10696.
62. Russo P., de Chiara M.L.V., Vernile A., Amodio M.L., Arena M.P., Capozzi V., Massa S., Spano G. Fresh-cut pineapple as a new carrier of probiotic lactic acid bacteria. Biomed. Res. Int. 2014, 2014:309183.
63. Saarela M., Rantala M., Hallamaa K., Nohynek L., Virkajärvi I., Mättö J. Stationary-phase acid and heat treatments for improvement of the viability of probiotic lactobacilli and bifidobacteria. J. Appl. Microbiol. 2004, 96:1205-1214.
64. Salar-Behzadi S., Wu S., Toegel S., Hofrichter M., Altenburger I., Unger F.M., Wirth M., Viernstein H. Impact of heat treatment and spray drying on cellular properties and culturability of Bifidobacterium bifidum BB-12. Food Res. Int. 2013, 54:93-101.
65. Sanders M.E., Marco M.L. Food formats for effective delivery of probiotics. Annu. Rev. Food Sci. Technol. 2010, 1:65-85.
66. Savijoki K., Suokko A., Palva A., Valmu L., Kalkkinen N., Varmanen P. Effect of heat-shock and bile salts on protein synthesis of Bifidobacterium longum revealed by [35S]methionine labelling and two-dimensional gel electrophoresis. FEMS Microbiol. Lett. 2005, 248:207-215.
67. Schwab C., Vogel R., Gänzle M.G. Influence of oligosaccharides on the viability and membrane properties of Lactobacillus reuteri TMW1.106 during freeze-drying. Cryobiology 2007, 55:108-114.
68. Sendra E., Fayos P., Lario Y., Fernández-López J., Sayas-Barberá E., Pérez-Alvarez J.A. Incorporation of citrus fibers in fermented milk containing probiotic bacteria. Food Microbiol. 2008, 25:13-21.
69. Serrano L.M., Molenaar D., Wels M., Teusink B., Bron P.A., de Vos W.M., Smid E.J. Thioredoxin reductase is a key factor in the oxidative stress response of Lactobacillus plantarum WCFS1. Microb. Cell Fact. 2007, 6:29.
70. Soukoulis C., Behboudi-Jobbehdar S., Yonekura L., Parmenter C., Fisk I.D. Stability of Lactobacillus rhamnosus GG in prebiotic edible films. Food Chem. 2014, 159:302-308.
71. Spano G., Massa S. Environmental stress response in wine lactic acid bacteria: beyond Bacillus subtilis. Crit. Rev. Microbiol. 2006, 32:77-86.
72. Spano G., Capozzi V., Vernile A., Massa S. Cloning, molecular characterization and expression analysis of two small heat shock genes isolated from wine Lactobacillus plantarum. J. Appl. Microbiol. 2004, 97:774-782.
73. Spano G., Beneduce L., Perrotta C., Massa S. Cloning and characterization of the hsp 18.55 gene, a new member of the small heat shock gene family isolated from wine Lactobacillus plantarum. Res. Microbiol. 2005, 156:219-224.
74. Stack H.M., Kearney N., Stanton C., Fitzgerald G.F., Ross R.P. Association of beta-glucan endogenous production with increased stress tolerance of intestinal lactobacilli. Appl. Environ. Microbiol. 2010, 76:500-507.
75. Suokko A., Poutanen M., Savijoki K., Kalkkinen N., Varmanen P. ClpL is essential for induction of thermotolerance and is potentially part of the HrcA regulon in Lactobacillus gasseri. Proteomics 2008, 8:1029-1041.
76. Tsakalidou E., Papadimitriou K. Stress Responses of Lactic Acid Bacteria 2011, Springer Science & Business Media, New York.
77. Tymczyszyn E.E., Gerbino E., Illanes A., Gómez-Zavaglia A. Galacto-oligosaccharides as protective molecules in the preservation of Lactobacillus delbrueckii subsp. bulgaricus. Cryobiology 2011, 62:123-129.
78. van Baarlen P., Troost F.J., van Hemert S., van der Meer C., de Vos W.M., de Groot P.J., Hooiveld G.J.E.J., Brummer R.-J.M., Kleerebezem M. Differential NF-κB pathways induction by Lactobacillus plantarum in the duodenum of healthy humans correlating with immune tolerance. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:2371-2376.
79. van Bokhorst-van de Veen H., Abee T., Tempelaars M., Bron P.A., Kleerebezem M., Marco M.L. Short-and long-term adaptation to ethanol stress and its cross-protective consequences in Lactobacillus plantarum. Appl. Environ. Microbiol. 2011, 77:5247-5256.
80. van de Guchte M., Serror P., Chervaux C., Smokvina T., Ehrlich S.D., Maguin E. Stress responses in lactic acid bacteria. Antonie Van Leeuwenhoek 2002, 82:187-216.
81. Ventura M., Canchaya C., van Sinderen D., Fitzgerald G.F., Zink R. Bifidobacterium lactis DSM 10140: identification of the atp (atpBEFHAGDC) operon and analysis of its genetic structure, characteristics, and phylogeny. Appl. Environ. Microbiol. 2004, 70:3110-3121.
82. Ventura M., Zhang Z., Cronin M., Canchaya C., Kenny J.G., Fitzgerald G.F., van Sinderen D. The ClgR protein regulates transcription of the clpP operon in Bifidobacterium breve UCC 2003. J. Bacteriol. 2005, 187:8411-8426.
83. Wu V.C.H. A review of microbial injury and recovery methods in food. Food Microbiol. 2008, 25:735-744.
84. Wu C., Zhang J., Du G., Chen J. Aspartate protects Lactobacillus casei against acid stress. Appl. Microbiol. Biotechnol. 2013, 97:4083-4093.
85. Wu C., Huang J., Zhou R. Progress in engineering acid stress resistance of lactic acid bacteria. Appl. Microbiol. Biotechnol. 2014, 98:1055-1063.
86. Zhai Z., Douillard F.P., An H., Wang G., Guo X., Luo Y., Hao Y. Proteomic characterization of the acid tolerance response in Lactobacillus delbrueckii subsp. bulgaricus CAUH1 and functional identification of a novel acid stress-related transcriptional regulator Ldb0677. Environ. Microbiol. 2014, 16:1524-1537.
87. Zhang J., Wu C., Du G., Chen J. Enhanced acid tolerance in Lactobacillus casei by adaptive evolution and compared stress response during acid stress. Biotechnol. Bioprocess Eng. 2012, 17:283-289.
88. Zuo F., Yu R., Khaskheli G.B., Ma H., Chen L., Zeng Z., Mao A., Chen S. Homologous overexpression of alkyl hydroperoxide reductase subunit C (ahpC) protects Bifidobacterium longum strain NCC2705 from oxidative stress. Res. Microbiol. 2014, 165:581-589.
89. Zuo F., Yu R., Feng X., Khaskheli G.B., Chen L., Ma H., Chen S. Combination of heterogeneous catalase and superoxide dismutase protects Bifidobacterium longum strain NCC2705 from oxidative stress. Appl. Microbiol. Biotechnol. 2014, 98:7523-7534.