Abstract
Many different bifidobacterial species constitute a key component of the human gut microbiota due to their perceived health-promoting role, which they elicit at the site of their natural habitat, the large intestine. Hence, such bifidobacteria represent a growing area of interest with respect to their genetics, genomics, and molecular ecology. This chapter will present the current knowledge of the molecular players that allow bifidobacteria to cope with heat, osmotic, acid, and bile salt stress.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Alander M, Mättö J, Kneifel W, Johansson M, Kögler 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 11:817–825
Barrangou R, Briczinski EP, Traeger LL, Loquasto JR, Richards M, Horvath P, Coute-Monvoisin AC, Leyer G, Rendulic S, Steele JL, Broadbent JR, Oberg T, Dudley EG, Schuster S, Romero DA, Roberts RF (2009) Comparison of the complete genome sequences of Bifidobacterium animalis subsp. lactis DSM 10140 and Bl-04. J Bacteriol 191:4144–4151
Begley M, Gahan CG, Hill C (2002) Bile stress response in Listeria monocytogenes LO28: adaptation, cross-protection, and identification of genetic loci involved in bile resistance. Appl Environ Microbiol 68:6005–6012
Begley M, Gahan CG, Hill C (2005) The interaction between bacteria and bile. FEMS Microbiol Rev 29:625–651
Bellier A, Mazodier P (2004) ClgR, a novel regulator of clp and lon expression in Streptomyces. J Bacteriol 186:3238–3248
Bernstein C, Bernstein H, Payne CM, Beard SE, Schneider J (1999) Bile salt activation of stress response promoters in Escherichia coli. Curr Microbiol 39:68–72
Bore E, Langsrud S, Langsrud O, Rode TM, Holck A (2007) Acid-shock responses in Staphylococcus aureus investigated by global gene expression analysis. Microbiology 153:2289–2303
Bron PA, Molenaar D, de Vos WM, Kleerebezem M (2006) DNA micro-array-based identification of bile-responsive genes in Lactobacillus plantarum. J Appl Microbiol 100:728–738
Bukau B, Horwich AL (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92:351–366
Candela M, Bergmann S, Vici M, Vitali B, Turroni S, Eikmanns BJ, Hammerschmidt S, Brigidi P (2007) Binding of human plasminogen to Bifidobacterium. J Bacteriol 189:5929–5936
Chung HS, Kim YB, Chun SL, Ji GE (1999) Screening and selection of acid and bile resistant bifidobacteria. Int J Food Microbiol 47:25–32
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 Methods 66:560–563
Collado MC, Sanz Y (2007) Induction of acid resistance in Bifidobacterium: a mechanism for improving desirable traits of potentially probiotic strains. J Appl Microbiol 103:1147–1157
Collado MC, Gueimonde M, Sanz Y, Salminen S (2006) Adhesion properties and competitive pathogen exclusion ability of bifidobacteria with acquired acid resistance. J Food Prot 69:1675–1679
Comtois SL, Gidley MD, Kelly DJ (2003) Role of the thioredoxin system and the thiol-peroxidases Tpx and Bcp in mediating resistance to oxidative and nitrosative stress in Helicobacter pylori. Microbiology 149:121–129
Cotter PD, Hill C (2003) Surviving the acid test: responses of Gram-positive bacteria to low pH. Microbiol Mol Biol Rev 67:429–453
Davis MJ, Coote PJ, O’Byrne CP (1996) Acid tolerance in Listeria monocytogenes: the adaptive acid tolerance response (ATR) and growth-phase-dependent acid resistance. Microbiology 142(Pt 10):2975–2982
De Dea Lindner J, Canchaya C, Zhang Z, Neviani E, Fitzgerald GF, van Sinderen D, Ventura M (2007) Exploiting Bifidobacterium genomes: the molecular basis of stress response. Int J Food Microbiol 120:13–24
Derré I, Rapoport G, Devine K, Rose M, Msadek T (1999a) ClpE, a novel type of HSP100 ATPase, is part of the CtsR heat shock regulon of Bacillus subtilis. Mol Microbiol 32:581–593
Derré I, Rapoport G, Msadek T (1999b) CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in Gram-positive bacteria. Mol Microbiol 31:117–131
Engels S, Schweitzer JE, Ludwig C, Bott M, Schaffer S (2004) clpC and clpP1P2 gene expression in Corynebacterium glutamicum is controlled by a regulatory network involving the transcriptional regulators ClgR and HspR as well as the ECF sigma factor sigmaH. Mol Microbiol 52:285–302
Engels S, Ludwig C, Schweitzer JE, Mack C, Bott M, Schaffer S (2005) The transcriptional activator ClgR controls transcription of genes involved in proteolysis and DNA repair in Corynebacterium glutamicum. Mol Microbiol 57:576–591
Ewalt KL, Hendrick JP, Houry WA, Hartl FU (1997) In vivo observation of polypeptide flux through the bacterial chaperonin system. Cell 90:491–500
Fanaro S, Vigi V, Chierici R, Boehm G (2003) Fecal flora measurements of breastfed infants using an integrated transport and culturing system. Acta Paediatr 92:634–635
Fedhila S, Msadek T, Nel P, Lereclus D (2002) Distinct clpP genes control specific adaptive responses in Bacillus thuringiensis. J Bacteriol 184:5554–5562
Fraser CM, Gocayne JD, White O, Adams MD, Clayton RA, Fleischmann RD, Bult CJ, Kerlavage AR, Sutton G, Kelley JM, Fritchman RD, Weidman JF, Small KV, Sandusky M, Fuhrmann J, Nguyen D, Utterback TR, Saudek DM, Phillips CA, Merrick JM, Tomb JF, Dougherty BA, Bott KF, Hu PC, Lucier TS, Peterson SN, Smith HO, Hutchison CA 3rd, Venter JC (1995) The minimal gene complement of Mycoplasma genitalium. Science 270:397–403
Fuchs M (2003) Bile acid regulation of hepatic physiology: III. Regulation of bile acid synthesis: past progress and future challenges. Am J Physiol Gastrointest Liver Physiol 284:G551–557
Garrigues C, Stuer-Lauridsen B, Johansen E (2005) Characterisation of Bifidobacterium animalis subsp. lactis BB-12 and other probiotic bacteria using genomics, transcriptomics and proteomics. Aust J Dairy Technol 60:84–92
Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, Gordon JI, Relman DA, Fraser-Liggett CM, Nelson KE (2006) Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359
Gottesman S (1996) Proteases and their targets in Escherichia coli. Annu Rev Genet 30:465–506
Gottesman S, Wickner S, Maurizi MR (1997) Protein quality control: triage by chaperones and proteases. Genes Dev 11:815–823
Grimaud R, Kessel M, Beuron F, Steven AC, Maurizi MR (1998) Enzymatic and structural similarities between the Escherichia coli ATP-dependent proteases, ClpXP and ClpAP. J Biol Chem 273:12476–12481
Gueimonde M, Garrigues C, van Sinderen D, de los Reyes-Gavilan CG, Margolles A (2009) Bile-inducible efflux transporter from Bifidobacterium longum NCC2705, conferring bile resistance. Appl Environ Microbiol 75:3153–3160
Hardison WG (1978) Hepatic taurine concentration and dietary taurine as regulators of bile acid conjugation with taurine. Gastroenterology 75:71–75
Harmsen HJ, Wildeboer-Veloo AC, Raangs GC, Wagendorp AA, Klijn N, Bindels JG, Welling GW (2000) Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J Pediatr Gastroenterol Nutr 30:61–67
Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381:571–579
Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852–1858
Hlavacek O, Vachova L (2002) ATP-dependent proteinases in bacteria. Folia Microbiol (Praha) 47:203–212
Hofmann AF, Hagey LR (2008) Bile acids: chemistry, pathochemistry, biology, pathobiology, and therapeutics. Cell Mol Life Sci 65:2461–2483
Homuth G, Masuda S, Mogk A, Kobayashi Y, Schumann W (1997) The dnaK operon of Bacillus subtilis is heptacistronic. J Bacteriol 179:1153–1164
Hondorp ER, Matthews RG (2004) Oxidative stress inactivates cobalamin-independent methionine synthase (MetE) in Escherichia coli. PLoS Biol 2:e336
Houry WA, Frishman D, Eckerskorn C, Lottspeich F, Hartl FU (1999) Identification of in vivo substrates of the chaperonin GroEL. Nature 402:147–154
Jayamanne VS, Adams MR (2006) Determination of survival, identity and stress resistance of probiotic bifidobacteria in bio-yoghurts. Lett Appl Microbiol 42:189–194
Keiler KC, Waller PR, Sauer RT (1996) Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271:990–993
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
Knaust A, Weber MV, Hammerschmidt S, Bergmann S, Frosch M, Kurzai O (2007) Cytosolic proteins contribute to surface plasminogen recruitment of Neisseria meningitidis. J Bacteriol 189:3246–3255
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
Kristiansen TZ, Bunkenborg J, Gronborg M, Molina H, Thuluvath PJ, Argani P, Goggins MG, Maitra A, Pandey A (2004) A proteomic analysis of human bile. Mol Cell Proteomics 3:715–728
Kurdi P, Tanaka H, Van Veen HW, Asano K, Tomita F, Yokota A (2003) Cholic acid accumulation and its diminution by short-chain fatty acids in bifidobacteria. Microbiology 149:2031–2037
Kurdi P, Kawanishi K, Mizutani K, Yokota A (2006) Mechanism of growth inhibition by free bile acids in lactobacilli and bifidobacteria. J Bacteriol 188:1979–1986
Lamendella R, Santo Domingo JW, Kelty C, Oerther DB (2008) Bifidobacteria in feces and environmental waters. Appl Environ Microbiol 74:575–584
Langer T, Pfeifer G, Martin J, Baumeister W, Hartl FU (1992) Chaperonin-mediated protein folding: GroES binds to one end of the GroEL cylinder, which accommodates the protein substrate within its central cavity. EMBO J 11:4757–4765
Lee BH, Hibino T, Jo J, Viale AM, Takabe T (1997) Isolation and characterization of a dnaK genomic locus in a halotolerant cyanobacterium Aphanothece halophytica. Plant Mol Biol 35:763–775
Lee JH, Karamychev VN, Kozyavkin SA, Mills D, Pavlov AR, Pavlova NV, Polouchine NN, Richardson PM, Shakhova VV, Slesarev AI, Weimer B, O’Sullivan DJ (2008) Comparative genomic analysis of the gut bacterium Bifidobacterium longum reveals loci susceptible to deletion during pure culture growth. BMC Genom 9:247
Len AC, Harty DW, Jacques NA (2004) Proteome analysis of Streptococcus mutans metabolic phenotype during acid tolerance. Microbiology 150:1353–1366
Leverrier P, Dimova D, Pichereau V, Auffray Y, Boyaval P, Jan G (2003) Susceptibility and adaptive response to bile salts in Propionibacterium freudenreichii: physiological and proteomic analysis. Appl Environ Microbiol 69:3809–3818
Ley RE, Hamady M, Lozupone C, Turnbaugh 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
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
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
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
Maurizi MR, Clark WP, Kim SH, Gottesman S (1990) ClpP represents a unique family of serine proteases. J Biol Chem 265:12546–12552
Maus JE, Ingham SC (2003) Employment of stressful conditions during culture production to enhance subsequent cold- and acid-tolerance of bifidobacteria. J Appl Microbiol 95:146–154
Miwa T, Esaki H, Umemori J, Hino T (1997) Activity of H(+)-ATPase in ruminal bacteria with special reference to acid tolerance. Appl Environ Microbiol 63:2155–2158
Miyake T, Watanabe K, Watanabe T, Oyaizu H (1998) Phylogenetic analysis of the genus Bifidobacterium and related genera based on 16S rDNA sequences. Microbiol Immunol 42:661–667
Mogk A, Tomoyasu T, Goloubinoff P, Rüdiger S, Röder D, Langen H, Bukau B (1999) Identification of thermolabile Escherichia coli proteins: prevention and reversion of aggregation by DnaK and ClpB. EMBO J 18:6934–6949
Muchowski PJ, Hays LG, Yates JR 3rd, Clark JI (1999) ATP and the core “alpha-crystallin” domain of the small heat-shock protein alphaB-crystallin. J Biol Chem 274:30190–30195
Nair S, Finkel SE (2004) Dps protects cells against multiple stresses during stationary phase. J Bacteriol 186:4192–4198
Narberhaus F (1999) Negative regulation of bacterial heat shock genes. Mol Microbiol 31:1–8
Narberhaus F (2002) Alpha-crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol Mol Biol Rev 66:64–93; table of contents
Noriega L, de los Reyes-Gavilan CG, Margolles A (2005) Acquisition of bile salt resistance promotes antibiotic susceptibility changes in Bifidobacterium. J Food Prot 68:1916–1919
O’Connell-Motherway M, Fitzgerald GF, Neirynck S, Ryan S, Steidler L, van Sinderen D (2008) Characterization of ApuB, an extracellular type II amylopullulanase from Bifidobacterium breve UCC2003. Appl Environ Microbiol 74:6271–6279
O’Connell-Motherway M, O’Driscoll J, Fitzgerald GF, van Sinderen D (2009) Overcoming the restriction barrier to plasmid transformation and targeted mutagenesis in Bifidobacterium breve UCC2003. Microbiol Biotechnol 2:321–332
Price CE, Reid SJ, Driessen AJ, Abratt VR (2006) The Bifidobacterium longum NCIMB 702259T ctr gene codes for a novel cholate transporter. Appl Environ Microbiol 72:923–926
Puglia AM, Vohradsky J, Thompson CJ (1995) Developmental control of the heat-shock stress regulon in Streptomyces coelicolor. Mol Microbiol 17:737–746
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
Ridlon JM, Kang DJ, Hylemon PB (2006) Bile salt biotransformations by human intestinal bacteria. J Lipid Res 47:241–259
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
Ruas-Madiedo P, Gueimonde M, Arigoni F, de los Reyes-Gavilan CG, Margolles A (2009) Bile affects the synthesis of exopolysaccharides by Bifidobacterium animalis. Appl Environ Microbiol 75:1204–1207
Ruiz L, Coute Y, Sanchez B, de los Reyes-Gavilan CG, Sanchez JC, Margolles A (2009a) The cell-envelope proteome of Bifidobacterium longum in an in vitro bile environment. Microbiology 155:957–967
Ruiz L, Sanchez B, de Los Reyes-Gavilan CG, Gueimonde M, Margolles A (2009b) Coculture of Bifidobacterium longum and Bifidobacterium breve alters their protein expression profiles and enzymatic activities. Int J Food Microbiol 133:148–153
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
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
Sanchez B, de los Reyes-Gavilan CG, Margolles A (2006) The F1F0-ATPase of Bifidobacterium animalis is involved in bile tolerance. Environ Microbiol 8:1825–1833
Sanchez B, Champomier-Verges MC, Anglade P, Baraige F, de Los Reyes-Gavilan CG, Margolles A, Zagorec M (2005) Proteomic analysis of global changes in protein expression during bile salt exposure of Bifidobacterium longum NCIMB 8809. J Bacteriol 187:5799–5808
Sanchez B, Champomier-Verges MC, Collado Mdel C, Anglade P, Baraige F, Sanz Y, de los Reyes-Gavilan CG, Margolles A, Zagorec M (2007a) Low-pH adaptation and the acid tolerance response of Bifidobacterium longum biotype longum. Appl Environ Microbiol 73:6450–6459
Sanchez B, Champomier-Verges MC, Stuer-Lauridsen B, Ruas-Madiedo P, Anglade P, Baraige F, de los Reyes-Gavilan CG, Johansen E, Zagorec M, Margolles A (2007b) Adaptation and response of Bifidobacterium animalis subsp. lactis to bile: a proteomic and physiological approach. Appl Environ Microbiol 73:6757–6767
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
Schell MA, Karmirantzou M, Snel B, Vilanova D, Berger B, Pessi 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 USA 99:14422–14427
Schirmer EC, Glover JR, Singer MA, Lindquist S (1996) HSP100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem Sci 21:289–296
Sela DA, Chapman J, Adeuya A, Kim JH, Chen F, Whitehead TR, Lapidus A, Rokhsar DS, Lebrilla 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 USA 105:18964–18969
Servant P, Mazodier P (1995) Characterization of Streptomyces albus 18-kilodalton heat shock-responsive protein. J Bacteriol 177:2998–3003
Sjovall J (1959) Dietary glycine and taurine on bile acid conjugation in man; bile acids and steroids 75. Proc Soc Exp Biol Med 100:676–678
Stackebrandt E, Sproer C, Rainey FA, Burghardt J, Pauker O, Hippe H (1997) Phylogenetic analysis of the genus Desulfotomaculum: evidence for the misclassification of Desulfotomaculum guttoideum and description of Desulfotomaculum orientis as Desulfosporosinus orientis gen. nov., comb. nov. Int J Syst Bacteriol 47:1134–1139
Takahashi N, Xiao JZ, Miyaji K, Iwatsuki K (2007) H + -ATPase in the acid tolerance of Bifidobacterium longum. Milk Sci Int 62:151–153
Teter SA, Klionsky DJ (1999) How to get a folded protein across a membrane. Trends Cell Biol 9:428–431
Tharmaraj N, Shah NP (2003) Selective enumeration of Lactobacillus delbrueckii ssp. bulgaricus, Streptococcus thermophilus, Lactobacillus acidophilus, bifidobacteria, Lactobacillus casei, Lactobacillus rhamnosus, and propionibacteria. J Dairy Sci 86:2288–2296
Turroni F, Foroni E, Pizzetti P, Giubellini V, Ribbera A, Merusi P, Cagnasso P, Bizzarri B, de’Angelis GL, Shanahan F, van Sinderen D, Ventura M (2009a) Exploring the diversity of the bifidobacterial population in the human intestinal tract. Appl Environ Microbiol 75:1534–1545
Turroni F, Marchesi JR, Foroni E, Gueimonde M, Shanahan F, Margolles A, van Sinderen D, Ventura M (2009b) Microbiomic analysis of the bifidobacterial population in the human distal gut. ISME J 3:745–751
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
Ventura M, Canchaya C, van Sinderen D, Fitzgerald GF, Zink R (2004a) 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
Ventura M, Canchaya C, Zink R, Fitzgerald GF, van Sinderen D (2004b) Characterization of the groEL and groES loci in Bifidobacterium breve UCC 2003: genetic, transcriptional, and phylogenetic analyses. Appl Environ Microbiol 70:6197–6209
Ventura M, Fitzgerald GF, van Sinderen D (2005a) Genetic and transcriptional organization of the clpC locus in Bifidobacterium breve UCC 2003. Appl Environ Microbiol 71:6282–6291
Ventura M, Kenny JG, Zhang Z, Fitzgerald GF, van Sinderen D (2005b) The clpB gene of Bifidobacterium breve UCC 2003: transcriptional analysis and first insights into stress induction. Microbiology 151:2861–2872
Ventura M, Zhang Z, Cronin M, Canchaya C, Kenny JG, Fitzgerald GF, van Sinderen D (2005c) The ClgR protein regulates transcription of the clpP operon in Bifidobacterium breve UCC 2003. J Bacteriol 187:8411–8426
Ventura M, Canchaya C, Del Casale A, Dellaglio F, Neviani E, Fitzgerald GF, van Sinderen D (2006a) Analysis of bifidobacterial evolution using a multilocus approach. Int J Syst Evol Microbiol 56:2783–2792
Ventura M, Canchaya C, Zhang Z, Bernini V, Fitzgerald GF, van Sinderen D (2006b) 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
Ventura M, Canchaya C, Fitzgerald GF, Gupta RS, van Sinderen D (2007a) Genomics as a means to understand bacterial phylogeny and ecological adaptation: the case of bifidobacteria. Antonie van Leeuwenhoek 91:351–372
Ventura M, Canchaya C, Tauch A, Chandra G, Fitzgerald GF, Chater KF, van Sinderen D (2007b) Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol Mol Biol Rev 71:495–548
Ventura M, Canchaya C, Zhang Z, Fitzgerald GF, van Sinderen D (2007c) Molecular characterization of hsp20, encoding a small heat shock protein of Bifidobacterium breve UCC2003. Appl Environ Microbiol 73:4695–4703
Ventura M, O’Flaherty S, Claesson MJ, Turroni F, Klaenhammer TR, van Sinderen D, O’Toole PW (2008) Genome-scale analyses of health-promoting bacteria: probiogenomics. Nat Rev Microbiol 7:61–71
Vernazza CL, Gibson GR, Rastall RA (2006) Carbohydrate preference, acid tolerance and bile tolerance in five strains of Bifidobacterium. J Appl Microbiol 100:846–853
Viala J, Mazodier P (2002) ClpP-dependent degradation of PopR allows tightly regulated expression of the clpP3 clpP4 operon in Streptomyces lividans. Mol Microbiol 44:633–643
Viala J, Rapoport G, Mazodier P (2000) The clpP multigenic family in Streptomyces lividans: conditional expression of the clpP3 clpP4 operon is controlled by PopR, a novel transcriptional activator. Mol Microbiol 38:602–612
Vinderola G, Prosello W, Molinari F, Ghiberto D, Reinheimer J (2009) Growth of Lactobacillus paracasei A13 in Argentinian probiotic cheese and its impact on the characteristics of the product. Int J Food Microbiol 135:171–174
Weissman JS, Kashi Y, Fenton WA, Horwich AL (1994) GroEL-mediated protein folding proceeds by multiple rounds of binding and release of nonnative forms. Cell 78:693–702
Wickner S, Maurizi MR, Gottesman S (1999) Posttranslational quality control: folding, refolding, and degrading proteins. Science 286:1888–1893
Xu Z, Horwich AL, Sigler PB (1997) The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex. Nature 388:741–750
Yasui K, Kano Y, Tanaka K, Watanabe K, Shimizu-Kadota M, Yoshikawa H, Suzuki T (2009) Improvement of bacterial transformation efficiency using plasmid artificial modification. Nucl Acids Res 37:e3
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
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer Science+Business Media, LLC
About this chapter
Cite this chapter
Ventura, M., Margolles, A., Turroni, F., Zomer, A., de los Reyes-Gavilán, C.G., van Sinderen, D. (2011). Stress Responses of Bifidobacteria. In: Tsakalidou, E., Papadimitriou, K. (eds) Stress Responses of Lactic Acid Bacteria. Food Microbiology and Food Safety. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-92771-8_14
Download citation
DOI: https://doi.org/10.1007/978-0-387-92771-8_14
Published:
Publisher Name: Springer, Boston, MA
Print ISBN: 978-0-387-92770-1
Online ISBN: 978-0-387-92771-8
eBook Packages: Chemistry and Materials ScienceChemistry and Material Science (R0)