How do bifidobacteria counteract environmental challenges? Mechanisms involved and physiological consequences

Genes and Nutrition

Volumn 6, Issue 3, 2011, Pages 307-318

  Ruiz, Lorena ^a   Ruas Madiedo, Patricia ^a   Gueimonde, Miguel ^a   De Los Reyes Gavilán, Clara G ^a   Margolles, Abelardo ^a   Sánchez, Borja ^a  

^a DEPARTMENT OF MICROBIOLOGY AND BIOCHEMISTRY OF DAIRY PRODUCTS   (Spain)

Author keywords

Bifidobacteria; Gastrointestinal tract; Stress; Technological processes

Indexed keywords

BACTERIAL PROTEIN; BILE SALT; OXYGEN; PROTEIN HS; UNCLASSIFIED DRUG;

BACTERIAL GENOME; BACTERIAL SURVIVAL; BACTERIAL VIABILITY; BACTERIUM COMPETENCE; BIFIDOBACTERIUM; BIFIDOBACTERIUM BREVE; BIFIDOBACTERIUM LONGUM; BIOAVAILABILITY; CARBON SOURCE; COMPETITIVE ABILITY; ENVIRONMENTAL STRESS; GASTROINTESTINAL TRACT FUNCTION; GENE ACTIVITY; HEAT SHOCK; HEAT TREATMENT; INTESTINE FLORA; MICROENVIRONMENT; NONHUMAN; OXYGENATION; PROTEIN FUNCTION; REVIEW; STOMACH PH; TEMPERATURE STRESS;

BACTERIA (MICROORGANISMS);

EID: 80054983556     PISSN: 15558932     EISSN: 18653499     Source Type: Journal    
DOI: 10.1007/s12263-010-0207-5     Document Type: Review

References (105)

1. Ahn JB, Hwang HJ, Park JH (2001) Physiological responses of oxygen-tolerant anaerobic Bifidobacterium longum under oxygen. J Microbiol Biotechnol 11:443-451 (Pubitemid 32684955)
2. Alander M, Matto J, Kneifel W, Johansson M, Kogler B, Crittenden R, Mattila-Sandholm T, Saarela M (2001) Effect of galacto-oligosaccharide supplementation on human faecal microflora and on survival and persistence of Bifidobacterium lactis Bb-12 in the gastrointestinal tract. Int Dairy J 10:817-825 (Pubitemid 33146337)
3. Alp G, Aslim B (2010) Relationship between the resistance to bile salts and low pH with exopolysaccharide (EPS) production of Bifidobacterium spp isolated from infants feces and breast milk. Anaerobe 16:101-105
4. Ananta E, Knorr D (2004) 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 96:307-313 (Pubitemid 39359154)
5. Anastasiou R, Leverrier P, Krestas I, Rouault A, Kalantzopoulos G, Boyaval P, Tsakaliodou E, Jan G (2006) Changes in protein synthesis during thermal adaptation of Propionibacterium freudenreichii subsp shermanii. Int J Food Microbiol 108: 301-314
6. Ashida H, Miyake A, Kiyohara M, Wada J, Yoshida E, Kumagai H, Katayama T, Yamamoto K (2009) Two distinct α-L-fucosidases from Bifidobacterium bifidum are essential for the utilization of fucosylated mil oligosaccharides and glycoconjugates. Glycobiology 19:1010-1017
7. Begley M, Gahan CG, Hill C (2005) The interaction between bacteria and bile. FEMS Microbiol Rev 72:1729-1738
8. Berger B, Moine D, Mansourian R, Arigoni F (2010) HspR mutations are naturally selected in Bifidobacterium longum when successive heat shock treatments are applied. J Bacteriol 192:256-263
9. Candela M, Bergmann S, Vici M, Vitali B, Turroni S, Eikmanns BJ, Hammerschnidt S, Brigidi P (2007) Binding of human plasminogen to Bifidobacterium. J Bacteriol 189:5929-5936 (Pubitemid 47236145)
10. Carvalho AS, Silva J, Ho P, Teixeira P, Malcata FX, Gibbs P (2004) Relevant factors for the preparation of freeze-dried lactic acid bacteria. Int Dairy J 14:835-847 (Pubitemid 39081551)
11. Charteris WP, Kelly PM, Morelli L, Collins JK (1998) Development and application of an in vitro methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in the upper human gastrointestinal tract. J Appl Microbiol 84:759-768 (Pubitemid 28294468)
12. Chavez BE, Ledeboer AM (2007) Drying of probiotics: optimization of formulation and process to enhance storage survival. Drying Technol 25:1193-1201 (Pubitemid 47209002)
13. Collado MC, Sanz Y (2006) Method for direct selection of potentially probiotic Bifidobacterium strains from human feces based on their acid-adaptation ability. J Microbiol Meth 66:560-563 (Pubitemid 44081814)
14. Cotter PD, Hill C (2003) Surviving the acid test: responses of gram-positive bacteria to low pH. Microbiol Mol Biol Rev 67:429-453 (Pubitemid 37122528)
15. Davis MJ, Coote PJ, O'Byme CP (1996) Acid tolerance in Listeria monocytogenes: the adaptive acid tolerance response (ATR) and growth-phase dependent acid resistance. Microbiology-SGM 142:2975-2982 (Pubitemid 26362939)
16. De Angelis M, Di Cagno R, Huet C, Crecchio C, Fox PF, Gobbetti M (2004) Heat shock response in Lactobacillus plantarum. Appl Environ Microbiol 70:1336-1346 (Pubitemid 38365111)
17. Dink WK, Shah NP (2009) Effect of various encapsulating materials on the stability of probiotic bacteria. J Food Sci 74:M1000-M1077
18. Dong X, Xin Y, Jian W, Liu X, Ling D (2000) Bifidobacterium thermacidophilum sp nov isolated from an anaerobic digester. Int J System Evol Microbiol 50:119-125 (Pubitemid 30084062)
19. FAO/WHO (2002) Guidelines for the evaluation of probiotics in food food and health. Agricultural Organization of the United Nations and World Health Organization working group report
20. Fiocco D, Capozzi V, Goffin P, Hols P, Spano G (2007) Improved adaptation to heat, cold and solvent tolerance in Lactobacillus plantarum. Appl Microbiol Biotechnol 77:909-915 (Pubitemid 350159875)
21. Garrigues C, Stuer-Lauridsen B, Johansen E (2005) Characterisation of Bifidobacterium animalis subsp lactis Bb12 and other probiotic bacteria using genomics, transcriptomics and proteomics. Aust J Dairy Tecnhol 60:84-92 (Pubitemid 41328079)
22. Gómez-Zavaglia A, Kociubinski G, Pérez P, Disalvo E, de Antoni G (2002) Effect of bile on the lipid composition and surface properties of bifidobacteria. J Appl Microbiol 93: 794-799 (Pubitemid 35340881)
23. Grill JP, Perrin S, Schneider F (2000) Bile salt toxicity to some bifidobacteria strains: role of conjugated bile salt hydrolase and pH. Can J Microbiol 46:878-884
24. Gueimonde M, Delgado S, Mayo B, Ruas-Madiedo P, Margolles A, de los Reyes-Gavilán CG (2004) Viability and diversity of probiotic Lactobacillus and Bifidobacterium populations included in commercial fermented milks. Food Res Int 37:839-850 (Pubitemid 39081560)
25. Gueimonde M, Garrigues C, van Sinderen D, de los Reyes-Gavilán CG, Margolles A (2009) Bile-inducible efflux transporter from Bifidobacterium longum NCC2705, conferring bile resistance. Appl Environ Microbiol 75:3153-3160
26. Gueimonde M, Margolles A, de los Reyes-Gavilán CG, Salminen S (2007) Competitive exclusion of enteropathogens from human intestinal mucus by Bifidobacterium strains with acquired resistance to bile-A preliminary study. Int J Food Microbiol 113:228-232 (Pubitemid 46027287)
27. Gueimonde M, Noriega L, Margolles A, de los Reyes-Gavilán CG, Salminen S (2005) Ability of Bifidobacterium strains with acquired resistance to bile to adhere to human intestinal mucus. Int J Food Microbiol 101:341-346 (Pubitemid 40733503)
28. Guillaume E, Berger B, Affolter M, Kussmann M (2009) Labelfree quantitative proteomics of two Bifidobacterium longum strains. Proteomics 72:771-784
29. Hondrop ER, Matthews RG (2004) Oxidative stress inactivates cobalamin-independent methionine synthase (MetE) in Escherichia coli LR. Plos Biol 2:1738-1753
30. Kailasapathy K, Harmstorf I, Philiphs M (2008) Survival of Lactobacillus acidophilus and Bifidobacterium animalis ssp lactis in stirred fruit yogurts. LWT-Food Sci Technol 41:1317-1322 (Pubitemid 351635921)
31. Kampinga H (2006) Chaperones in preventing protein denaturation in living cells and protecting against cellular stress. Handbook Exp Pharmacol 172:1-42
32. Kawasaki S, Mimura T, Satoh T, Takeda K, Niimura Y (2006) Response of the microaerophilic Bifidobacterium species, B boum and B thermophilum, to oxygen. Appl Environ Microbiol 72:6854-6858 (Pubitemid 44582936)
33. Kelly AL, Zeece M (2009) Application of novel technologies in processing of functional foods. Aus J Dairy Technol 64:12-15
34. Kheadr E, Dabour N, Le Lay C, Lacroix C, Fliss I (2007) Antibiotic susceptibility profile of bifidobacteria as affected by oxgall, acid, and hydrogen peroxide stress. Antimicrob Agents Chemother 51:169-174 (Pubitemid 46047702)
35. Knaust A, Weber MW, Hammerschmidt S, Bergmann S, Frosch M, Kurzai O (2007) Cytosolic proteins contribute to surface plasminogen recruitment of Neisseria meningitides. J Bacteriol 189:3246-3255 (Pubitemid 46697415)
36. Kociubinski G, Zavaglia AG, Perez PF, Disalvo EA, De Antoni GL (2002) Effect of bile components on the surface properties of bifidobacteria. J Dairy Res 69:293-302 (Pubitemid 34973544)
37. Kurdi P, Tanaka H, Van Veen HW, Asano K, Tomita F, Yokota A (2006) Mechanisms of growth inhibition by free bile acids in lactobacilli and bifidobacteria. J Bacteriol 188:1979-1986 (Pubitemid 43346878)
38. Kurokawa K, Itoh H, Kuwahara T, Oshima K, Toh H, Toyoda A, Takami H, Morita H, Sharma VK, Srivastava TP, Taylor TD, Noguchi H, Mori H, Ogura Y, Ehrlich DS, Itoh K, Takagi T, Sakaki Y, Hayashi T, Hattori M (2007) Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res 14:169-181
39. Len AC, Harty DW, Jacques NA (2004) Proteome analysis of Streptococcus mutans metabolic phenotype during acid tolerance. Microbiology-SGM 150:1353-1366 (Pubitemid 38744737)
40. Ley RE, Hamady M, Lozupone C, Turnbauch PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI (2008) Evolution of mammals and their gut microbes. Science 320:1647-1651 (Pubitemid 351931256)
41. Li QQ, Chen QH, Hui R, Zhu DS, He GQ (2010) Isolation and characterization of an oxygen, acid and bile resistant Bifidobacterium animalis subsp lactis Qq08. J Sci Food Agric 90: 1340-1346
42. Lian WC, Hsiao HC, Chou CC (2002) Survival of bifidobacteria after spray-drying. Int J Food Microbiol 74:79-86
43. Lozupone CA, Hamady M, Cantarel BL, Coutinho PM, Henrisat B, Gordon JI, Knight R (2008) The convergence of carbohydrate active gene repertoires in human gut microbes. Proc Natl Acad Sci U S A 105:15076-15081
44. Margolles A, García L, Sánchez B, Gueimonde M, de los Reyes-Gavilán CG (2003) Characterisation of a Bifidobacterium strain with acquired resistance to cholate-a preliminary study. Int J Food Microbiol 82:191-198 (Pubitemid 36144023)
45. Masco L, Crockaert C, Van Hoorde K, Swings J, Huys G (2007) In vitro assessment of the gastrointestinal transit tolerance of taxonomic reference strains from human origin and probiotic product isolates of Bifidobacterium. J Dairy Sci 90:3572-3578 (Pubitemid 350045233)
46. Matsumoto M, Ohishi H, Benno Y (2004) H+ATPase activity in Bifidobacterium with special reference to acid tolerance. Int J Food Microbiol 93:109-113 (Pubitemid 38591630)
47. Maus JE, Ingham SC (2003) Employment of stressful conditions during culture production to enhance subsequent cold-and acidtolerance of bifidobacteria. J Appl Microbiol 95:146-154 (Pubitemid 36791877)
48. Meng XC, Stanton C, Fitzgerald GF, Daly C, Ross RP (2008) Anhydrobiotics: the challenges of drying probiotic cultures. Food Chem 106:1406-1416 (Pubitemid 47633085)
49. Modesto M, Mattarelli P, Biavati B (2004) Resistance to freezing and freeze-drying storage processes of potential probiotic bifidobacteria. Ann Microbiol 54:43-48 (Pubitemid 38485068)
50. Mokarram RR, Mortazavi SA, Najafi MBH, Shahidi F (2009) The influence of multi-stage alginate-coating on survivability of potential probiotic bacteria in simulated gastric and intestinal juice. Food Res Int 42:1040-1045
51. Niven CF, Buettner LG, Evans JB (1954) Thermal tolerance studies on the heterofermentative lactobacilli that cause greening of cured meat products. Appl Microbiol 2:26-29
52. Noriega L, de los Reyes-Gavilán CG, Margolles A (2005) Acquisition of bile salt resistance promotes antibiotic susceptibility changes in Bifidobacterium. J Food Prot 68:1916-1919 (Pubitemid 41446126)
53. Noriega L, Cuevas I, Margolles A, de los Reyes-Gavilán CG (2006) Deconjugation and bile salts hydrolase activity by Bifidobacterium strains with acquired resistance to bile. Int Dairy J 16:850-855
54. Noriega L, Gueimonde M, Sánchez B, Margolles A, de los Reyes-Gavilán CG (2004) Effect of the adaptation to high bile salts concentrations on glycosidic activity, survival at low pH and cross-resistance to bile salts in Bifidobacterium. Int J Food Microbiol 94:79-86 (Pubitemid 38681189)
55. Payne CM, Crowley C, Washo-Stultz D, Briehl M, Bernstein H, Bernstein C, Beard S, Holubec H, Warneke J (1998) The stressresponse proteins poly (ADP-ribose) polymerase and NF-kappaB protect against bile salt-induced apoptosis. Cell Death Differ 5:623-636 (Pubitemid 28356584)
56. Perrin S, Grill JP, Schneider F (2000) Effects of fructooligosaccharides and their monomeric components on bile salt resistance in three species of bifidobacteria. J Appl Microbiol 88:968-974 (Pubitemid 30409077)
57. Prasad J, McJarrow P, Gopal P (2003) Heat and osmotic stress responses of probiotic Lactobacillus rhamnosus HN001 (DR20) in relation to viability after drying. Appl Environ Microbiol 69:917-925 (Pubitemid 36204819)
58. Price CE, Reid SJ, Driessen AJ, Abratt VR (2006) The Bifidobacterium longum NCIMB702259T ctr gene codes for a novel cholate transporter. Appl Environ Microbiol 72:923-926
59. Ranadheera RDCS, Baines SK, Adams MC (2010) Importance of food in probiotic efficacy. Food Res Int 43:1-7
60. Rezzonico E, Lariani S, Barretto C, Cuanoud G, Giliberti G, Delley M, Arigoni F, Pessi G (2007) Global transcriptome analysis of the heat shock response of Bifidobacterium longum. FEMS Microbiol Lett 271:136-145 (Pubitemid 46701065)
61. Ritter P, Kohler C, von Ah U (2009) Evaluation of the passage of Lactobacillus gasseri K7 and bifidobacteria from the stomach to intestines using a single reactor model. BMC Microbiol 9:87
62. Rivera-Espinoza Y, Gallardo-Navarro Y (2010) Non-dairy probiotic products. Food Microbiol 27:1-11
63. Ruas-Madiedo P, Gueimonde M, Arigoni F, de los Reyes-Gavilán CG, Margolles A (2009) Bile affects the synthesis of exopolysaccharides by Bifidobacterium animalis. Appl Environ Microbiol 75:241-259
64. Ruas-Madiedo P, Hernández-Barranco A, Margolles A, de los Reyes-Gavilán CG (2005) A bile salt-resistant derivative of Bifidobacterium animalis has an altered fermentation pattern when grown on glucose and maltose. Appl Environ Microbiol 71:6564-6570 (Pubitemid 43194137)
65. Ruiz L, Couté Y, Sánchez B, de los Reyes-Gavilán CG, Sánchez JC, Margolles A (2009) The cell-envelope proteome of Bifidobacterium longum in an in vitro bile environment. Microbiology-SGM 274:316-322
66. Ruiz L, Sánchez B, de Los Reyes-Gavilán CG, Gueimonde M, Margolles A (2009) Coculture of Bifidobacterium longum and Bifidobacterium breve alters their protein expression profiles and enzymatic activities. Int J Food Microbiol 133:148-153
67. Ruiz L, Sánchez B, Ruas-Madiedo P, de los Reyes-Gavilán CG, Margolles A (2007) Cell envelope changes in Bifidobacterium animalis ssp lactis as a response to bile. FEMS Microbiol Lett 274:316-322 (Pubitemid 47256275)
68. Saarela M, Rantala M, Hallamaa K, Nohynek L, Virkajarvi I, Matto J (2004) Stationary-phase acid and heat-treatments for improvement of the viability of probiotic lactobacilli and bifidobacteria. J Appl Microbiol 96:1205-1214 (Pubitemid 38703599)
69. Saarela MH (2007) Probiotic technology maintaining viability and stability. Agro Food Ind Hi-Tech 18:19-21 (Pubitemid 47346071)
70. Samelis J, Ikeda JS, Sofos JN (2003) Evaluation of the pH-dependent stationary-phase acid tolerance in Listeria monocytogenes and Salmonella Typhimurium DT104 induced by culturing in media with 1% glucose: a comparative study with Escherichia coli O157:H7. J Appl Microbiol 95:563-575 (Pubitemid 37041089)
71. Sánchez B, Champomier-Vergès MC, Anglade P, Baraige F, de los Reyes-Gavilán CG, Margolles A, Zagorec M (2005) Proteomic analysis of global changes in protein expression during bile salt exposure of Bifidobacterium longum NCIMB8809. J Bacteriol 187:5799-5808 (Pubitemid 41134318)
72. Sánchez B, Champomier-Vergès MC, Collado MC, Anglade P, Baraige F, Sanz Y, de los Reyes-Gavilán CG, Margolles A, Zagorec M (2007) Low-pH adaptation and the acid tolerance response of Bifidobacterium longum biotype longum. Appl Environ Microbiol 73:6450-6459 (Pubitemid 47623703)
73. Sánchez B, Champomier-Vergès MC, Stuer-Lauridsen B, Ruas-Madiedo P, Anglade P, Baraige F, de los Reyes-Gavilán CG, Johansen E, Zagorec M, Margolles A (2007) Adaptation and response of Bifidobacterium animalis subsp. lactis to bile: a proteomic and physiological approach. Appl Environ Microbiol 73:6757-6767 (Pubitemid 350076794)
74. Sánchez B, de los Reyes-Gavilán CG, Margolles A (2006) The F1F0-ATPase of Bifidobacterium animalis is involved in bile tolerance. Environ Microbiol 8:1825-1833 (Pubitemid 44326474)
75. Sánchez B, de los Reyes-Gavilán CG, Margolles A, Gueimonde M (2009) Probiotic fermented milks: present and future. Int J Dairy Technol 62:472-483
76. Sánchez B, Fernández-García M, Margolles A, de los Reyes-Gavilán CG, Ruas-Madiedo P (2010) Technological and probiotic selection criteria of a bile-adapted Bifidobacterium animalis subsp lactis strain. Int Dairy J 20:800-805
77. Sánchez B, Ruiz L, de los Reyes-Gavilán CG, Margolles A (2008) Proteomics of stress response in Bifidobacterium. Front Biosci 13:6905-6919
78. Sanders ME, Marco ML (2010) Food formats for effective delivery of probiotics. Ann Rev Food Sci Technol 1:65-85
79. Sanz Y (2007) Ecological and functional implications of the acid-adaptation ability of Bifidobacterium: a way of selecting improved probiotic strains. Int Dairy J 17:1284-1289 (Pubitemid 47419315)
80. Savijoki K, Suokko A, Palva A, Valmu L, Kalkkinen N, Varmanen P (2005) 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 248:207-215 (Pubitemid 40942130)
81. Schell MA, Karmirantzou M, Snel B, Vilanova S, Berger B, Passi G, Zwahlen MC, Desiere F, Bork P, Delley M, Pridmore RD, Arigoni F (2002) The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc Natl Acad Sci U S A 99:14422-14427 (Pubitemid 35257687)
82. Schmidt G, Zink R (2000) Basic features of the stress response in three species of bifidobacteria: B longum, B adolescentis and B breve. Int J Food Microbiol 55:41-45 (Pubitemid 30160802)
83. Sela DA, Chapman J, Adeuya A, Kim JH, Chen F, Whitehead TR, Lapidus A, Rokhsar DS, Lebilla CB, German JB, Price NP, Richardson PM, Mills DA (2008) The genome sequence of Bifidobacterium longum subsp infantis reveals adaptations for milk utilization within the infant microbiome. Proc Natl Acad Sci U S A 105:18964-18969
84. Shakirova L, Auzina L, Zikmanis P, Gavare M, Grube M (2010) Influence of growth conditions on hydrophobicity of Lactobacillus acidophilus and Bifidobacterium lactis cells and characteristics by FT-IR spectra. Spectros Int J 24:251-255
85. Sheehan VM, Sleator RD, Hill C, Fitzgerald GF (2007) Improving gastric transit, gastrointestinal persistence and therapeutic efficacy of the probiotic strain Bifidobacterium breve UCC2003. Microbiology-SGM 153:3563-3571 (Pubitemid 47629559)
86. Shin SY, Park JH (1997) Activities of oxidative enzymes related with oxygen tolerance in Bifidobacterium sp. J Microbiol Biotechnol 7:356-359
87. Simpson PJ, Ross RP, Filzgerald GF, Stanton C (2004) Bifidobacterium psychraerophilum sp nov and Aeriscardovia aeriphila gen nov, sp nov, isolated from a porcine caecum. Int J Syst Evol Microbiol 54:401-406 (Pubitemid 38443733)
88. Simpson PJ, Stanton C, Fitzgerald GF, Ross RP (2005) Intrinsic tolerance of Bifidobacterium species to heat and oxygen and survival following spray drying and storage. J Appl Microbiol 99:493-501 (Pubitemid 41215826)
89. Su P, Henriksson A, Mitchell H (2007) Prebiotics enhance survival and prolong the retention period of specific probiotic inocula in an in vivo murine model. J Appl Microbiol 103: 2392-2400 (Pubitemid 350191166)
90. Teixeira P, Castro H, Kirby R (1994) Inducible thermotolerance in Lactobacillus bulgaricus. Lett Appl Microbiol 18:218-221 (Pubitemid 24210509)
91. Turroni F, Bottacini F, Foroni E, Mulder I, Kim JH, Zomer A, Sánchez B, Bidossi A, Ferrarini A, Giubellini V, Delledonne M, Henrissat B, Coutinho P, Oggioni M, Fitzgerald GF, Mills D, Margolles A, Kelly D, van Sinderen D, Ventura M (2010) Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proc Natl Acad Sci U S A (in press)
92. Van de Guchte M, Serror P, Chervaux C, Smokvina T, Ehrlich SD, Maguin E (2002) Stress responses in lactic acid bacteria. Antonie van Leeuwenhoek 82:187-216
93. Ventura M, Canchaya C, Van Sinderen D, Fitzgerald GF, Zink R (2004) Bifidobacterium lactis DSM 10140: identification of the atp (atpBEFHAGDC) operon and analysis of its genetic structure, characteristics, and phylogeny. Appl Environ Microbiol 70:3110-3121 (Pubitemid 38657831)
94. Ventura M, Canchaya C, Zhang Z, Bernini V, Fitzgerald GF, van Sinderen D (2006) How high G + C Gram-positive bacteria and in particular bifidobacteria cope with heat stress: protein players and regulators. FEMS Microbiol Rev 30:734-759 (Pubitemid 44199348)
95. Ventura M, Canchaya C, Zhang Z, Fitzgerald GF, van Sinderen D (2007) Molecular characterization of hsp20, encoding a small heat shock protein of Bifidobacterium breve UCC2003. Appl Environ Microbiol 73:4695-4703 (Pubitemid 47122618)
96. Ventura M, Canchaya C, Zink R, Fitzgerald GF, van Sinderen D (2004) Characterization of the groEL and groES loci in Bifidobacterium breve UCC2003: genetic, transcriptional, and phylogenetic analyses. Appl Environ Microbiol 70:6197-6209 (Pubitemid 39471870)
97. Ventura M, Canchaya C, Bernini V, Del Casale A, Dellaglio F, Neviani E, Fitzgerald GF, van Sinderen D (2005) Genetic characterization of the Bifidobacterium breve UCC2003 hrcA locus. Appl Environ Microbiol 71:8998-9007 (Pubitemid 41804049)
98. Ventura M, Fitzgerald GF, van Sinderen D (2005) Genetic and transcriptional organization of the clpC locus in Bifidobacterium breve UCC2003. Appl Environ Microbiol 71:6282-6291 (Pubitemid 41456930)
99. Ventura M, Kenny JG, Zhang ZD, Fitzgerald GF, van Sinderen D (2005) The clpB gene of Bifidobacterium breve UCC2003: transcriptional analysis and first insights into stress induction. Microbiology-SGM 151:2861-2872 (Pubitemid 41309561)
100. Ventura M, Zhang ZD, Cronin M, Canchaya C, Kenny JG, Fitzgerald GF, van Sinderen D (2005) The ClgR protein regulates transcription of the clpP operon in Bifidobacterium breve UCC2003. J Bacteriol 187:8411-8426 (Pubitemid 41780506)
101. Von Ah U, Mozzetti V, Lacroix C, Kheadr EE, Fliss I, Meile L (2007) Classification of a moderately oxygen-tolerant isolate from baby faeces as Bifidobacterium thermophilum. BMC Microbiol 7:79
102. Watson D, Sleator RD, Hill C, Gahan CGM (2008) Enhancing bile tolerance improves survival and persistence of Bifidobacterium and Lactococcus in the murine gastrointestinal tract. BMC Microbiol 8:176
103. Yang Y, Chen M, Liao C (2001) New isolated Bifidobacterium mutant strains tolerant to oxygen, bile salts and gastric acid, which can pass through the stomach with increased survivability, useful in foods. Patent number US6306638-B1
104. Yuan J, Wang B, Sun Z, Bo X, Yuan X, Zhao H, Du X, Wang F, Jiang Z, Zhang L, Jia L, Wang Y, Wei K, Wang J, Zhang X, Sun Y, Huan L, Zeng M (2008) Analysis of host-inducing proteome changes in Bifidobacterium longum NCC2705 grown in vivo. J Proteome Res 7:375-385 (Pubitemid 351171152)
105. Zomer A, Fernandez M, Kearney B, Fitzgerald GF, Ventura M, van Sinderen D (2009) An interactive regulatory network controls stress response in Bifidobacterium breve UCC2003. J Bacteriol 191:7039-7049