Advertisement

Staying alive: growth and survival of Bifidobacterium animalis subsp. animalis under in vitro and in vivo conditions

  • Muireann Egan
  • Francesca Bottacini
  • Mary O’Connell Motherway
  • Patrick G. Casey
  • Ruth Morrissey
  • Silvia Melgar
  • Jean-Michel Faurie
  • Christian Chervaux
  • Tamara Smokvina
  • Douwe van Sinderen
Genomics, transcriptomics, proteomics

Abstract

Members of the Bifidobacterium genus are widely used as probiotics in fermented milk products. Bifidobacterium animalis subsp. animalis CNCM I-4602 grows and survives poorly in reconstituted skimmed milk (RSM). Availing of genome and transcriptome information, this poor growth and survival phenotype in milk was substantially improved by the addition of certain compounds, such as yeast extract, uric acid, glutathione, cysteine, ferrous sulfate, and a combination of magnesium sulfate and manganese sulfate. Carbohydrate utilization of CNCM I-4602 was also investigated, allowing the identification of several carbohydrate utilization gene clusters, and highlighting this strain’s inability to utilize lactose, unlike the type strain of this subspecies, B. animalis subsp. animalis ATCC25527 and the B. animalis subsp. lactis subspecies. In addition, the ability of B. animalis subsp. animalis CNCM I-4602 to colonize a murine model was investigated, which showed that this strain persists in the murine gut for a period of at least 4 weeks. Associated in vivo transcriptome analysis revealed that, among other genes, a gene cluster encoding a predicted type IVb tight adherence (Tad) pilus was upregulated, indicating that this extracellular structure plays a role in the colonization/adaptation of the murine gastrointestinal tract by this strain.

Keywords

Bifidobacteria Genome sequencing Reconstituted skimmed milk Transcriptomics Probiotic Gastrointestinal tract 

Notes

Acknowledgements

The authors would like to sincerely thank Dr. Richard J. Roberts for assistance provided with the REBASE database (http://www.neb.com). We are also extremely grateful to Shandong Longlive Bio-Technology Co., Ltd. (Shandong, China) for the provision of xylo-oligosaccharides and Glycom A/S (Lyngby, Denmark) for the provision of purified Human Milk Oligosaccharides (HMOs) samples used in this study under their donation program.

Funding

This work was financially supported by Danone Research (Paris, France) and by the Science Foundation Ireland (SFI) (Wilton Place, Dublin, Ireland), through the Irish Government’s National Development Plan (grant no. SFI/12/RC/2273) and a HRB postdoctoral fellowship (Grant No. PDTM/2011/9) awarded to MOCM. FB is a recipient of a FEMS Research Grant (FEMS-RG-2016-0103) and FEMS/ESCMID Award.

Compliance with ethical standards

Experiments with mice were approved by the University College Cork Animal Experimentation Ethics Committee and experimental procedures were conducted under license from the Irish Government (license number B100/3729).

Conflict of interest

JMF, CC, and TS are employees of Danone (Paris, France). All other authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

253_2018_9413_MOESM1_ESM.pdf (163 kb)
ESM 1 (PDF 163 kb)

References

  1. Agrawal A, Houghton LA, Morris J, Reilly B, Guyonnet D, Goupil Feuillerat N, Schlumberger A, Jakob S, Whorwell PJ (2009) Clinical trial: the effects of a fermented milk product containing Bifidobacterium lactis DN-173 010 on abdominal distension and gastrointestinal transit in irritable bowel syndrome with constipation. Aliment Pharmacol Ther 29:104–114CrossRefPubMedCentralGoogle Scholar
  2. Altmann F, Kosma P, O’Callaghan A, Leahy S, Bottacini F, Molloy E, Plattner S, Schiavi E, Gleinser M, Groeger D, Grant R, Rodriguez Perez N, Healy S, Svehla E, Windwarder M, Hofinger A, O’Connell Motherway M, Akdis CA, Xu J, Roper J, van Sinderen D, O’Mahony L (2016) Genome analysis and characterisation of the exopolysaccharide produced by Bifidobacterium longum subsp. longum 35624™. PLoS One 11:e0162983CrossRefPubMedCentralGoogle Scholar
  3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefGoogle Scholar
  4. Beerens H, Gavini F, Neut C (2000) Effect of exposure to air on 84 strains of Bifidobacteria. Anaerobe 6:65–67CrossRefGoogle Scholar
  5. Bolduc MP, Raymond Y, Fustier P, Champagne C, Vuillemard JC (2006) Sensitivity of bifidobacteria to oxygen and redox potential in non-fermented pasteurized milk. Int Dairy J 16:1038–1048CrossRefGoogle Scholar
  6. Bottacini F, Medini D, Pavesi A, Turroni F, Foroni E, Riley D, Giubellini V, Tettelin H, van Sinderen D, Ventura M (2010) Comparative genomics of the genus Bifidobacterium. Microbiology 156:3243–3254CrossRefPubMedCentralGoogle Scholar
  7. Bottacini F, Milani C, Turroni F, Sánchez B, Foroni E, Duranti S, Serafini F, Viappiani A, Strati F, Ferrarini A, Delledonne M, Henrissat B, Coutinho P, Fitzgerald GF, Margolles A, van Sinderen D, Ventura M (2012) Bifidobacterium asteroides PRL2011 genome analysis reveals clues for colonization of the insect gut. PLoS One 7(9):e44229CrossRefPubMedCentralGoogle Scholar
  8. Bottacini F, O’Connell Motherway M, Kuczynski J, O’Connell KJ, Serafini F, Duranti S, Milani C, Turroni F, Lugli GA, Zomer A, Zhurina D, Riedel C, Ventura M, van Sinderen D (2014) Comparative genomics of the Bifidobacterium breve taxon. BMC Genomics 15:170CrossRefPubMedCentralGoogle Scholar
  9. Bottacini F, Morrissey R, Roberts RJ, James K, van Breen J, Egan M, Lambert J, van Limpt K, Knol J, O’Connell Motherway M, van Sinderen D (2017) Comparative genome and methylome analysis reveals restriction/modification system diversity in the gut commensal Bifidobacterium breve. Nucleic Acids Res 46:1860–1877CrossRefGoogle Scholar
  10. Boylston TD, Vinderola CG, Ghoddusi HB, Reinheimer JA (2004) Incorporation of bifidobacteria into cheeses: challenges and rewards. Int Dairy J 14:375–387CrossRefGoogle Scholar
  11. Carmel-Harel O, Storz G (2000) Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu Rev Microbiol 54:439–461CrossRefPubMedCentralGoogle Scholar
  12. Codex Alimentarius (2003) Codex-standard 243-2003: codex standard for fermented milks. Accessed 7 Apr 2013.http://www.codexalimentarius.net/input/download/standards/400/CXS_ 243e.pdf
  13. Coman MM, Verdenelli MC, Cecchini C, Silvi S, Vasile A, Bahrim GE, Orpianesi C, Cresci A (2013) Effect of buckwheat flour and oat bran on growth and cell viability of the probiotic strains Lactobacillus rhamnosus IMC 501®, Lactobacillus paracasei IMC 502® and their combination SYNBIO®, in synbiotic fermented milk. Int J Food Microbiol 167:261–268CrossRefPubMedCentralGoogle Scholar
  14. Cronin M, Sleator RD, Hill C, Fitzgerald GF, van Sinderen D (2008) Development of a luciferase-based reporter system to monitor Bifidobacterium breve UCC2003 persistence in mice. BMC Microbiol 8:161CrossRefPubMedCentralGoogle Scholar
  15. Dave RI, Shah NP (1997a) Effectiveness of ascorbic acid as an oxygen scavenger in improving viability of probiotic bacteria in yoghurts made with commercial starter cultures. Int Dairy J 7:435–443CrossRefGoogle Scholar
  16. Dave RI, Shah NP (1997b) Viability of yoghurt and probiotic bacteria in yoghurts made from commercial starter cultures. Int Dairy J 7:31–41CrossRefGoogle Scholar
  17. Dave RI, Shah NP (1998) Ingredient supplementation effects on viability of probiotic bacteria in yogurt. J Dairy Sci 81:2804–2816CrossRefPubMedCentralGoogle Scholar
  18. de Almada CN, Nunes de Almada C, Martinez RC, Sant’Ana Ade S (2015) Characterization of the intestinal microbiota and its interaction with probiotics and health impacts. Appl Microbiol Biotechnol 99:4175–4199CrossRefPubMedCentralGoogle Scholar
  19. de Jong A, Hansen ME, Kuipers OP, Kilstrup M, Kok J (2013) The transcriptional and gene regulatory network of Lactococcus lactis MG1363 during growth in milk. PLoS One 8:e53085CrossRefPubMedCentralGoogle Scholar
  20. Dianawati D, Shah NP (2011) Survival, acid and bile tolerance, and surface hydrophobicity of microencapsulated B. animalis ssp. lactis Bb12 during storage at room temperature. J Food Sci 76:M592–M599CrossRefPubMedCentralGoogle Scholar
  21. Eskesen D, Jespersen L, Michelsen B, Whorwell PJ, Müller-Lissner S, Morberg CM (2015) Effect of the probiotic strain Bifidobacterium animalis subsp. lactis, BB-12®, on defecation frequency in healthy subjects with low defecation frequency and abdominal discomfort: a randomised, double-blind, placebo-controlled, parallel-group trial. Br J Nutr 114:1638–1646CrossRefPubMedCentralGoogle Scholar
  22. Fanning S, Hall LJ, Cronin M, Zomer A, MacSharry J, Goulding D, Motherway MO, Shanahan F, Nally K, Dougan G, van Sinderen D (2012) Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. Proc Natl Acad Sci 109:2108–2113CrossRefPubMedCentralGoogle Scholar
  23. FAO/WHO (2001) Report of the joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  24. Ferdousi R, Rouhi M, Mohammadi R, Mortazavian AM, Khosravi-Darani K, Homayouni Rad A (2013) Evaluation of probiotic survivability in yogurt exposed to cold chain interruption. Iran J Pharm Res 12:139–144PubMedPubMedCentralGoogle Scholar
  25. Ferrario C, Milani C, Mancabelli L, Lugli GA, Duranti S, Mangifesta M, Viappiani A, Turroni F, Margolles A, Ruas-Madiedo P, van Sinderen D, Ventura M (2016) Modulation of the eps-ome transcription of bifidobacteria through simulation of human intestinal environment. FEMS Microbiol Ecol 92:fiw056CrossRefPubMedCentralGoogle Scholar
  26. Ferrario C, Statello R, Carnevali L, Mancabelli L, Milani C, Mangifesta M, Duranti S, Lugli GA, Jimenez B, Lodge S, Viappiani A, Alessandri G, Dall’Asta M, Del Rio D, Sgoifo A, van Sinderen D, Ventura M, Turroni F (2017) How to feed the mammalian gut microbiota: bacterial and metabolic modulation by dietary fibers. Front Microbiol 8:1749CrossRefPubMedCentralGoogle Scholar
  27. Florence ACR, de Oliveira MN, Delile A, Béal C (2016) Survival of Bifidobacterium strains in organic fermented milk is improved as a result of membrane fatty acid composition. Int Dairy J 61:1–9CrossRefGoogle Scholar
  28. Foroni E, Serafini F, Amidani D, Turroni F, He F, Bottacini F, O’Connell Motherway M, Viappiani A, Zhang Z, Rivetti C, van Sinderen D, Ventura M (2011) Genetic analysis and morphological identification of pilus-like structures in members of the genus Bifidobacterium. Microb Cell Factories 10:1CrossRefGoogle Scholar
  29. Guyonnet D, Schlumberger A, Mhamdi L, Jakob S, Chassany O (2009) Fermented milk containing Bifidobacterium lactis DN-173 010 improves gastrointestinal well-being and digestive symptoms in women reporting minor digestive symptoms: a randomised, double-blind, parallel, controlled study. Br J Nutr 102:1654–1662CrossRefPubMedCentralGoogle Scholar
  30. Hidalgo-Cantabrana C, Nikolic M, López P, Suárez A, Miljkovic M, Kojic M, Margolles A, Golic N, Ruas-Madiedo P (2014a) Exopolysaccharide-producing Bifidobacterium animalis subsp. lactis strains and their polymers elicit different responses on immune cells from blood and gut associated lymphoid tissue. Anaerobe 26:24–30CrossRefPubMedCentralGoogle Scholar
  31. Hidalgo-Cantabrana C, Sánchez B, Milani C, Ventura M, Margolles A, Ruas-Madiedo P (2014b) Genomic overview and biological functions of exopolysaccharide biosynthesis in Bifidobacterium spp. Appl Environ Microbiol 80:9–18CrossRefPubMedCentralGoogle Scholar
  32. van Hijum S, de Jong A, Baerends R, Karsens H, Kramer N, Larsen R, den Hengst C, Albers C, Kok J, Kuipers O (2005) A generally applicable validation scheme for the assessment of factors involved in reproducibility and quality of DNA-microarray data. BMC Genomics 6:77CrossRefPubMedCentralGoogle Scholar
  33. Holmes E, Li JV, Marchesi JR, Nicholson JK (2012) Gut microbiota composition and activity in relation to host metabolic phenotype and disease risk. Cell Metab 16:559–564CrossRefPubMedCentralGoogle Scholar
  34. Janer C, Peláez C, Requena T (2004) Caseinomacropeptide and whey protein concentrate enhance Bifidobacterium lactis growth in milk. Food Chem 86:263–267CrossRefGoogle Scholar
  35. Jay JM, Loessner MJ, Golden DA (2012) Modern food microbiology, seventh ed. Springer Science & Business Media, New YorkGoogle Scholar
  36. Jayamanne VS, Adams MR (2006) Determination of survival, identity and stress resistance of probiotic bifidobacteria in bio-yoghurts. Lett Appl Microbiol 42:189–194CrossRefPubMedCentralGoogle Scholar
  37. Jin J, Zhang B, Guo H, Cui J, Jiang L, Song S, Sun M, Ren F (2012) Mechanism analysis of acid tolerance response of Bifidobacterium longum subsp. longum BBMN 68 by gene expression profile using RNA-sequencing. PLoS One 7:e50777CrossRefPubMedCentralGoogle Scholar
  38. Jungersen M, Wind A, Johansen E, Christensen J, Stuer-Lauridsen B, Eskesen D (2014) The science behind the probiotic strain Bifidobacterium animalis subsp. lactis. BB-12®. Microorganisms 2:92–110CrossRefPubMedCentralGoogle Scholar
  39. Kailasapathy K (2006) Survival of free and encapsulated probiotic bacteria and their effect on the sensory properties of yoghurt. LWT-Food Sci Technol 39:1221–1227CrossRefGoogle Scholar
  40. Law J, Buist G, Haandrikman A, Kok J, Venema G, Leenhouts K (1995) A system to generate chromosomal mutations in Lactococcus lactis which allows fast analysis of targeted genes. J Bacteriol 177:7011–7018CrossRefPubMedCentralGoogle Scholar
  41. LeBlanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D, Ventura M (2013) Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol 24:160–168CrossRefPubMedCentralGoogle Scholar
  42. Li Q, Chen Q, Ruan H, Zhu D, He G (2010) Isolation and characterisation of an oxygen, acid and bile resistant Bifidobacterium animalis subsp. lactis Qq08. J Sci Food Agric 90:1340–1346CrossRefPubMedCentralGoogle Scholar
  43. Loquasto JR, Barrangou R, Dudley EG, Roberts RF (2011) Short communication: the complete genome sequence of Bifidobacterium animalis subspecies animalis ATCC 25527T and comparative analysis of growth in milk with B animalis subspecies lactis DSM 10140T. J Dairy Sci 94:5864–5870CrossRefPubMedCentralGoogle Scholar
  44. Marteau P, Guyonnet D, Lafaye de Micheaux P, Gelu S (2013) A randomized, double-blind, controlled study and pooled analysis of two identical trials of fermented milk containing probiotic Bifidobacterium lactis CNCM I-2494 in healthy women reporting minor digestive symptoms. Neurogastroenterol Motil 25:331–e252CrossRefPubMedCentralGoogle Scholar
  45. Martin R, Laval L, Chain F, Miquel S, Natividad J, Cherbuy C, Sokol H, Verdu EF, van Hylckama Vlieg J, Bermudez-Humaran LG, Smokvina T, Langella P (2016) Bifidobacterium animalis ssp. lactis CNCM-I2494 restores gut barrier permeability in chronically low-grade inflamed mice. Front Microbiol 7:608Google Scholar
  46. Masco L, Ventura M, Zink R, Huys G, Swings J (2004) Polyphasic taxonomic analysis of Bifidobacterium animalis and Bifidobacterium lactis reveals relatedness at the subspecies level: reclassification of Bifidobacterium animalis as Bifidobacterium animalis subsp. animalis subsp. nov. and Bifidobacterium lactis as Bifidobacterium animalis subsp. lactis subsp. nov. Int J Syst Evol Microbiol 54:1137–1143Google Scholar
  47. Matsumoto M, Ohishi H, Benno Y (2004) H+-ATPase activity in Bifidobacterium with special reference to acid tolerance. Int J Food Microbiol 93:109–113CrossRefPubMedCentralGoogle Scholar
  48. Meile L, Ludwig W, Rueger U, Gut C, Kaufmann P, Dasen G, Wenger S, Teuber M (1997) Bifidobacterium lactis sp. nov., a moderately oxygen tolerant species isolated from fermented milk. Syst Appl Microbiol 20:57–64CrossRefGoogle Scholar
  49. Micanel N, Haynes I, Playne M (1997) Viability of probiotic cultures in commercial Australian yogurts. Aust J Dairy Technol 52:24Google Scholar
  50. Milani C, Duranti S, Lugli GA, Bottacini F, Strati F, Arioli S, Foroni E, Turroni F, van Sinderen D, Ventura M (2013) Comparative genomics of Bifidobacterium animalis subsp. lactis reveals a strict monophyletic bifidobacterial taxon. Appl Environ Microbiol 79:4304–4315CrossRefPubMedCentralGoogle Scholar
  51. Milani C, Lugli GA, Duranti S, Turroni F, Bottacini F, Mangifesta M, Sanchez B, Viappiani A, Mancabelli L, Taminiau B, Delcenserie V, Barrangou R, Margolles A, van Sinderen D, Ventura M (2014) Genome encyclopaedia of type strains of the genus Bifidobacterium. Appl Environ Microbiol 80:6290–6302CrossRefPubMedCentralGoogle Scholar
  52. Milani C, Duranti S, Bottacini F, Casey E, Turroni F, Mahony J, Belzer C, Delgado Palacio S, Arboleya Montes S, Mancabelli L, Lugli GA, Rodriguez JM, Bode L, de Vos W, Gueimonde M, Margolles A, van Sinderen D, Ventura M (2017) The first microbial colonizers of the human gut: composition, activities, and health implications of the infant gut microbiota. Microbiol Mol Biol Rev 81:e00036–e00017CrossRefPubMedCentralGoogle Scholar
  53. Mistou MY, Sutcliffe IC, van Sorge NM, Bitter W (2016) Bacterial glycobiology: rhamnose-containing cell wall polysaccharides in gram-positive bacteria. FEMS Microbiol Rev 40:464–479CrossRefPubMedCentralGoogle Scholar
  54. Mortazavian AM, Ehsani MR, Mousavi SM, Rezaei K, Sohrabvandi S, Reinheimer JA (2007) Effect of refrigerated storage temperature on the viability of probiotic micro-organisms in yogurt. Int J Dairy Technol 60:123–127CrossRefGoogle Scholar
  55. Mortazavian A, Ehsani M, Azizi A, Razavi S, Mousavi S, Sohrabvandi S, Reinheimer J (2008) Viability of calcium-alginate-microencapsulated probiotic bacteria in Iranian yogurt drink (Doogh) during refrigerated storage and under simulated gastrointestinal conditions. Aust J Dairy Technol 63:25Google Scholar
  56. O’Callaghan A, Bottacini F, O’Connell Motherway M, van Sinderen D (2015) Pangenome analysis of Bifidobacterium longum and site-directed mutagenesis through by-pass of restriction-modification systems. BMC Genomics 16:832CrossRefPubMedCentralGoogle Scholar
  57. O’Connell Motherway M, Zomer A, Leahy SC, Reunanen J, Bottacini F, Claesson MJ, O’Brien F, Flynn K, Casey PG, Moreno Munoz JA, Kearney B, Houston AM, O’Mahony C, Higgins DG, Shanahan F, Palva A, de Vos WM, Fitzgerald GF, Ventura M, O’Toole PW, van Sinderen D (2011) Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. Proc Natl Acad Sci 108:11217–11222CrossRefPubMedCentralGoogle Scholar
  58. O’Connell Motherway M, Kinsella M, Fitzgerald GF, van Sinderen D (2013) Transcriptional and functional characterization of genetic elements involved in galacto-oligosaccharide utilization by Bifidobacterium breve UCC2003. Microb Biotechnol 6:67–79CrossRefPubMedCentralGoogle Scholar
  59. O’Connell Motherway M, Watson D, Bottacini F, Clark TA, Roberts RJ, Korlach J, Garault P, Chervaux C, van Hylckama Vlieg JET, Smokvina T, van Sinderen D (2014) Identification of restriction-modification systems of Bifidobacterium animalis subsp. lactis CNCM I-2494 by SMRT sequencing and associated methylome analysis. PLoS One 9:e94875CrossRefGoogle Scholar
  60. O’Connell KJ, O’Connell Motherway M, O’Callaghan J, Fitzgerald GF, RossRP VM, Stanton C, van Sinderen D (2013) Metabolism of four α-glycosidic linkage-containing oligosaccharides by Bifidobacterium breve UCC2003. Appl Environ Microbiol 79:6280–6292CrossRefPubMedCentralGoogle Scholar
  61. Odamaki T, Horigome A, Sugahara H, Hashikura N, Minami J, Xiao J-z, Abe F (2015) Comparative genomics revealed genetic diversity and species/strain-level differences in carbohydrate metabolism of three probiotic bifidobacterial species. Int J Genomics 567809Google Scholar
  62. Ouwehand AC, Salminen SJ (1998) The health effects of cultured milk products with viable and non-viable bacteria. Int Dairy J 8:749–758CrossRefGoogle Scholar
  63. Patrignani F, Serrazanetti DI, Mathara JM, Siroli L, Gardini F, Holzapfel WH, Lanciotti R (2015) Use of homogenisation pressure to improve quality and functionality of probiotic fermented milks containing Lactobacillus rhamnosus BFE 5264. Int J Dairy Technol 69:262–271CrossRefGoogle Scholar
  64. Phillips M, Kailasapathy K, Tran L (2006) Viability of commercial probiotic cultures (L. acidophilus, Bifidobacterium sp, L. casei, L. paracasei and L. rhamnosus) in cheddar cheese. Int J Food Microbiol 108:276–280CrossRefPubMedCentralGoogle Scholar
  65. Pokusaeva K, Neves AR, Zomer A, O'Connell-Motherway M, MacSharry J, Curley P, Fitzgerald GF, van Sinderen D (2010) Ribose utilization by the human commensal Bifidobacterium breve UCC2003. Microb Biotechnol 3:311–23CrossRefPubMedCentralGoogle Scholar
  66. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J (2011) The Pfam protein families database. Nucleic Acids Res 40:290–301CrossRefGoogle Scholar
  67. Raeisi SN, Ouoba LII, Farahmand N, Sutherland J, Ghoddusi HB (2013) Variation, viability and validity of bifidobacteria in fermented milk products. Food Control 34:691–697CrossRefGoogle Scholar
  68. Ranadheera RDCS, Baines SK, Adams MC (2010) Importance of food in probiotic efficacy. Food Res Int 43:1–7CrossRefGoogle Scholar
  69. Rizzardini G, Eskesen D, Calder PC, Capetti A, Jespersen L, Clerici M (2012) Evaluation of the immune benefits of two probiotic strains Bifidobacterium animalis ssp. lactis, BB-12® and Lactobacillus paracasei ssp. paracasei, L. casei 431® in an influenza vaccination model: a randomised, double-blind, placebo-controlled study. Br J Nutr 107:876–884CrossRefPubMedCentralGoogle Scholar
  70. Rodrigues D, Sousa S, Rocha-Santos T, Silva JP, Sousa Lobo JM, Costa P, Amaral MH, Pintado MM, Gomes AM, Malcata FX, Freitas AC (2011) Influence of L-cysteine, oxygen and relative humidity upon survival throughout storage of probiotic bacteria in whey protein-based microcapsules. Int Dairy J 21:869–876CrossRefGoogle Scholar
  71. Round JL, Mazmanian SK (2009) The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9:313–323CrossRefPubMedCentralGoogle Scholar
  72. Ruiz L, Gueimonde M, Ruas-Madiedo P, Ribbera A, de Los Reyes-Gavilán CG, Ventura M, Margolles A, Sánchez B (2012) Molecular clues to understand the aerotolerance phenotype of Bifidobacterium animalis subsp. lactis. Appl Environ Microbiol 78:644–650CrossRefPubMedCentralGoogle Scholar
  73. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream M-A, Barrell B (2000) Artemis: sequence visualization and annotation. Bioinformatics 16:944–945CrossRefPubMedCentralGoogle Scholar
  74. Salazar N, Ruas-Madiedo P, Kolida S, Collins M, Rastall R, Gibson G, de los Reyes-Gavilán CG (2009) Exopolysaccharides produced by Bifidobacterium longum IPLA E44 and Bifidobacterium animalis subsp. lactis IPLA R1 modify the composition and metabolic activity of human faecal microbiota in pH-controlled batch cultures. Int J Food Microbiol 135:260–267Google Scholar
  75. Sánchez B, de los Reyes-Gavilán CG, Margolles A, Gueimonde M (2009) Probiotic fermented milks: present and future. Int J Dairy Technol 62:472–483CrossRefGoogle Scholar
  76. Sanders ME, in’t Veld JH (1999) Bringing a probiotic-containing functional food to the market: microbiological, product, regulatory and labeling issues. Antonie Van Leeuwenhoek 76:293–315CrossRefPubMedCentralGoogle Scholar
  77. Schiavi E, Gleinser M, Molloy E, Groeger D, Frei R, Ferstl R, Rodriguez-Perez N, Ziegler M, Grant R, Moriarty TF, Plattner S, Healy S, O’Connell Motherway M, Akdis CA, Roper J, Altmann F, van Sinderen D, O’Mahony L (2016) The surface associated exopolysaccharide of Bifidobacterium longum 35624 plays an essential role in dampening host pro-inflammatory responses and in repressing local TH17 responses. Appl Environ Microbiol 82:7185–7196CrossRefPubMedCentralGoogle Scholar
  78. Scott JR, Zähner D (2006) Pili with strong attachments: gram-positive bacteria do it differently. Mol Microbiol 62:320–330CrossRefPubMedCentralGoogle Scholar
  79. Settachaimongkon S, van Valenberg HJF, Winata V, Wang X, Nout MJR, van Hooijdonk TCM, Zwietering MH, Smid EJ (2015) Effect of sublethal preculturing on the survival of probiotics and metabolite formation in set-yoghurt. Food Microbiol 49:104–115CrossRefPubMedCentralGoogle Scholar
  80. Shah N, Ravula R (2000) Influence of water activity on fermentation, organic acids production and viability of yogurt and probiotic bacteria. Aust J Dairy Tech 55:127Google Scholar
  81. Shah NP, Ali JF, Ravula RR (2000) Populations of Lactobacillus acidophilus, Bifidobacterium spp., and Lactobacillus casei in commercial fermented milk products. Biosci Microflora 19:35–39CrossRefGoogle Scholar
  82. 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 99:493–501CrossRefPubMedCentralGoogle Scholar
  83. Sun W, Griffiths MW (2000) Survival of bifidobacteria in yogurt and simulated gastric juice following immobilization in gellan–xanthan beads. Int J Food Microbiol 61:17–25CrossRefPubMedCentralGoogle Scholar
  84. Takahashi N, Xiao J-Z, Miyaji K, Yaeshiima T, Hiramatsu A, Iwatsuki K, Kokubo S, Hosono A (2004) Selection of acid tolerant bifidobacteria and evidence for a low-pH-inducible acid tolerance response in Bifidobacterium longum. J Dairy Res 71:340–345CrossRefPubMedCentralGoogle Scholar
  85. Talwalkar A, Miller CW, Kailasapathy K, Nguyen MH (2004) Effect of packaging materials and dissolved oxygen on the survival of probiotic bacteria in yoghurt. Int J Food Sci Technol 39:605–611CrossRefGoogle Scholar
  86. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4:1CrossRefPubMedCentralGoogle Scholar
  87. Tillisch K, Labus J, Kilpatrick L, Jiang Z, Stains J, Ebrat B, Guyonnet D, Legrain-Raspaud S, Trotin B, Naliboff B, Mayer EA (2013) Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology 144:1394–1401CrossRefPubMedCentralGoogle Scholar
  88. Turroni F, Serafini F, Foroni E, Duranti S, O’Connell Motherway M, Taverniti V, Mangifesta M, Milani C, Viappiani A, Roversi T, Sánchez B, Santoni A, Gioiosa L, Ferrarini A, Delledonne M, Margolles A, Piazza L, Palanza P, Bolchi A, Guglielmetti S, van Sinderen D, Ventura M (2013) Role of sortase-dependent pili of Bifidobacterium bifidum PRL2010 in modulating bacterium–host interactions. Proc Natl Acad Sci 110:11151–11156CrossRefPubMedCentralGoogle Scholar
  89. Van der Meulen R, Avonts L, De Vuyst L (2004) Short fractions of oligofructose are preferentially metabolized by Bifidobacterium animalis DN-173 010. Appl Environ Microbiol 70:1923–1930CrossRefPubMedCentralGoogle Scholar
  90. Vaughan E, Heilig H, Ben-Amor K, De Vos W (2005) Diversity, vitality and activities of intestinal lactic acid bacteria and bifidobacteria assessed by molecular approaches. FEMS Microbiol Rev 29:477–490CrossRefPubMedCentralGoogle Scholar
  91. Ventura M, Zink R, Fitzgerald GF, van Sinderen D (2005) Gene structure and transcriptional organization of the dnaK operon of Bifidobacterium breve UCC2003 and application of the operon in bifidobacterial tracing. Appl Environ Microbiol 71:487–500CrossRefPubMedCentralGoogle Scholar
  92. Ventura M, Turroni F, O’Connell Motherway M, MacSharry J, van Sinderen D (2012) Host–microbe interactions that facilitate gut colonization by commensal bifidobacteria. Trends Microbiol 20:467–476CrossRefPubMedCentralGoogle Scholar
  93. Ventura M, O’Toole PW, de Vos WM, van Sinderen D (2018) Selected aspects of the human gut microbiota. Cell Mol Life Sci 75:81–82CrossRefPubMedCentralGoogle Scholar
  94. Vernazza CL, Gibson GR, Rastall RA (2006) Carbohydrate preference, acid tolerance and bile tolerance in five strains of Bifidobacterium. J Appl Microbiol 100:846–853CrossRefPubMedCentralGoogle Scholar
  95. Vinderola CG, Reinheimer JA (2003) Lactic acid starter and probiotic bacteria: a comparative “in vitro” study of probiotic characteristics and biological barrier resistance. Food Res Int 36:895–904CrossRefGoogle Scholar
  96. 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 191:7039–7049CrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Muireann Egan
    • 1
  • Francesca Bottacini
    • 1
  • Mary O’Connell Motherway
    • 1
  • Patrick G. Casey
    • 1
  • Ruth Morrissey
    • 1
  • Silvia Melgar
    • 1
  • Jean-Michel Faurie
    • 2
  • Christian Chervaux
    • 2
  • Tamara Smokvina
    • 2
  • Douwe van Sinderen
    • 1
  1. 1.APC Microbiome Ireland and School of MicrobiologyUniversity College CorkCorkIreland
  2. 2.Danone Nutricia ResearchPalaiseauFrance

Personalised recommendations