Cellular and Molecular Life Sciences

, Volume 71, Issue 2, pp 183–203

Molecular dialogue between the human gut microbiota and the host: a Lactobacillus and Bifidobacterium perspective

  • Francesca Turroni
  • Marco Ventura
  • Ludovica F. Buttó
  • Sabrina Duranti
  • Paul W. O’Toole
  • Mary O’Connell Motherway
  • Douwe van Sinderen


The human gut represents a highly complex ecosystem, which is densely colonized by a myriad of microorganisms that influence the physiology, immune function and health status of the host. Among the many members of the human gut microbiota, there are microorganisms that have co-evolved with their host and that are believed to exert health-promoting or probiotic effects. Probiotic bacteria isolated from the gut and other environments are commercially exploited, and although there is a growing list of health benefits provided by the consumption of such probiotics, their precise mechanisms of action have essentially remained elusive. Genomics approaches have provided exciting new opportunities for the identification of probiotic effector molecules that elicit specific responses to influence the physiology and immune function of their human host. In this review, we describe the current understanding of the intriguing relationships that exist between the human gut and key members of the gut microbiota such as bifidobacteria and lactobacilli, discussed here as prototypical groups of probiotic microorganisms.


Probiotics Bifidobacteria Lactobacilli Gut microbiota Host–microbe cross-talk Genomics 


  1. 1.
    Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA (2005) Diversity of the human intestinal microbial flora. Science 308(5728):1635–1638PubMedCentralPubMedGoogle Scholar
  2. 2.
    Gao Z, Tseng CH, Pei Z, Blaser MJ (2007) Molecular analysis of human forearm superficial skin bacterial biota. Proc Natl Acad Sci USA 104(8):2927–2932PubMedGoogle Scholar
  3. 3.
    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(5778):1355–1359PubMedCentralPubMedGoogle Scholar
  4. 4.
    Marco ML, Pavan S, Kleerebezem M (2006) Towards understanding molecular modes of probiotic action. Curr Opin Biotechnol 17(2):204–210PubMedGoogle Scholar
  5. 5.
    Tamboli CP, Neut C, Desreumaux P, Colombel JF (2004) Dysbiosis as a prerequisite for IBD. Gut 53(7):1057PubMedGoogle Scholar
  6. 6.
    Organization FaAOotUNaWH (2001) Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. FAO/WHO, CordobaGoogle Scholar
  7. 7.
    FAO/WHO (2002) Guidelines for the evaluation of probiotics in food. Ontario, CanadaGoogle Scholar
  8. 8.
    Ventura M, O’Flaherty S, Claesson MJ, Turroni F, Klaenhammer TR, van Sinderen D, O’Toole PW (2009) Genome-scale analyses of health-promoting bacteria: probiogenomics. Nat Rev Microbiol 7(1):61–71PubMedGoogle Scholar
  9. 9.
    Ventura M, Turroni F, van Sinderen D (2012) Probiogenomics as a tool to obtain genetic insights into adaptation of probiotic bacteria to the human gut. Bioeng Bugs 3(2):73–79PubMedCentralPubMedGoogle Scholar
  10. 10.
    Joyce AR, Palsson BO (2006) The model organism as a system: integrating ‘omics’ data sets. Nat Rev Mol Cell Biol 7(3):198–210PubMedGoogle Scholar
  11. 11.
    Rajilic-Stojanovic M, Smidt H, de Vos WM (2007) Diversity of the human gastrointestinal tract microbiota revisited. Environ Microbiol 9(9):2125–2136PubMedGoogle Scholar
  12. 12.
    Turroni F, Peano C, Pass DA, Foroni E, Severgnini M, Claesson MJ, Kerr C, Hourihane J, Murray D, Fuligni F, Gueimonde M, Margolles A, De Bellis G, O’Toole PW, van Sinderen D, Marchesi JR, Ventura M (2012) Diversity of bifidobacteria within the infant gut microbiota. PLoS One 7(5):e36957PubMedCentralPubMedGoogle Scholar
  13. 13.
    Claesson MJ, Cusack S, O’Sullivan O, Greene-Diniz R, de Weerd H, Flannery E, Marchesi JR, Falush D, Dinan T, Fitzgerald G, Stanton C, van Sinderen D, O’Connor M, Harnedy N, O’Connor K, Henry C, O’Mahony D, Fitzgerald AP, Shanahan F, Twomey C, Hill C, Ross RP, O’Toole PW (2011) Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci USA 108(Suppl 1):4586–4591PubMedGoogle Scholar
  14. 14.
    Prakash S, Rodes L, Coussa-Charley M, Tomaro-Duchesneau C (2011) Gut microbiota: next frontier in understanding human health and development of biotherapeutics. Biologics 5:71–86PubMedCentralPubMedGoogle Scholar
  15. 15.
    Ventura M, Sozzi T, Turroni F, Matteuzzi D, van Sinderen D (2011) The impact of bacteriophages on probiotic bacteria and gut microbiota diversity. Genes Nutr 6(3):205–207PubMedCentralPubMedGoogle Scholar
  16. 16.
    Reyes A, Haynes M, Hanson N, Angly FE, Heath AC, Rohwer F, Gordon JI (2010) Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466(7304):334–338PubMedCentralPubMedGoogle Scholar
  17. 17.
    Vaishampayan PA, Kuehl JV, Froula JL, Morgan JL, Ochman H, Francino MP (2010) Comparative metagenomics and population dynamics of the gut microbiota in mother and infant. Genome Biol Evol 2:53–66Google Scholar
  18. 18.
    Penders J, Stobberingh EE, Thijs C, Adams H, Vink C, van Ree R, van den Brandt PA (2006) Molecular fingerprinting of the intestinal microbiota of infants in whom atopic eczema was or was not developing. Clin Exp Allergy 36(12):1602–1608PubMedGoogle Scholar
  19. 19.
    Westerbeek EA, van den Berg A, Lafeber HN, Knol J, Fetter WP, van Elburg RM (2006) The intestinal bacterial colonisation in preterm infants: a review of the literature. Clin Nutr 25(3):361–368PubMedGoogle Scholar
  20. 20.
    Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA 107(26):11971–11975PubMedGoogle Scholar
  21. 21.
    Arboleya S, Ruas-Madiedo P, Margolles A, Solis G, Salminen S, de Los Reyes-Gavilan CG, Gueimonde M (2011) Characterization and in vitro properties of potentially probiotic Bifidobacterium strains isolated from breast-milk. Int J Food Microbiol 149(1):28–36PubMedGoogle Scholar
  22. 22.
    Hyman RW, Fukushima M, Diamond L, Kumm J, Giudice LC, Davis RW (2005) Microbes on the human vaginal epithelium. Proc Natl Acad Sci USA 102(22):7952–7957PubMedGoogle Scholar
  23. 23.
    Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R (2009) Bacterial community variation in human body habitats across space and time. Science 326(5960):1694–1697PubMedCentralPubMedGoogle Scholar
  24. 24.
    Ahrne S, Lonnermark E, Wold AE, Aberg N, Hesselmar B, Saalman R, Strannegard IL, Molin G, Adlerberth I (2005) Lactobacilli in the intestinal microbiota of Swedish infants. Microbes Infect 7(11–12):1256–1262PubMedGoogle Scholar
  25. 25.
    Yoshioka H, Iseki K, Fujita K (1983) Development and differences of intestinal flora in the neonatal period in breast-fed and bottle-fed infants. Pediatrics 72(3):317–321PubMedGoogle Scholar
  26. 26.
    Gueimonde M, Laitinen K, Salminen S, Isolauri E (2007) Breast milk: a source of bifidobacteria for infant gut development and maturation? Neonatology 92(1):64–66PubMedGoogle Scholar
  27. 27.
    Zivkovic AM, German JB, Lebrilla CB, Mills DA (2011) Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proc Natl Acad Sci USA 108(Suppl 1):4653–4658PubMedGoogle Scholar
  28. 28.
    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(48):18964–18969PubMedGoogle Scholar
  29. 29.
    Yoshida E, Sakurama H, Kiyohara M, Nakajima M, Kitaoka M, Ashida H, Hirose J, Katayama T, Yamamoto K, Kumagai H (2012) Bifidobacterium longum subsp. infant is uses two different beta-galactosidases for selectively degrading type-1 and type-2 human milk oligosaccharides. Glycobiology 22(3):361–368PubMedGoogle Scholar
  30. 30.
    Kaplan JL, Shi HN, Walker WA (2011) The role of microbes in developmental immunologic programming. Pediatr Res 69(6):465–472PubMedGoogle Scholar
  31. 31.
    Klaasen HLBM, Vanderheijden PJ, Stok W, Poelma FGJ, Koopman JP, Vandenbrink ME, Bakker MH, Eling WMC, Beynen AC (1993) Apathogenic, intestinal, segmented, filamentous bacteria stimulate the mucosal immune-system of mice. Infect Immun 61(1):303–306PubMedCentralPubMedGoogle Scholar
  32. 32.
    Talham GL, Jiang HQ, Bos NA, Cebra JJ (1999) Segmented filamentous bacteria are potent stimuli of a physiologically normal state of the murine gut mucosal immune system. Infect Immun 67(4):1992–2000PubMedCentralPubMedGoogle Scholar
  33. 33.
    Gaboriau-Routhiau V, Rakotobe S, Lecuyer E, Mulder I, Lan A, Bridonneau C, Rochet V, Pisi A, De Paepe M, Brandi G, Eberl G, Snel J, Kelly D, Cerf-Bensussan N (2009) The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 31(4):677–689PubMedGoogle Scholar
  34. 34.
    Smith JM (2005) Atopy and asthma: an epidemic of unknown cause. J Allergy Clin Immunol 116(1):231–232 (author reply 232)PubMedGoogle Scholar
  35. 35.
    Khazaie K, Zadeh M, Khan MW, Bere P, Gounari F, Dennis K, Blatner NR, Owen JL, Klaenhammer TR, Mohamadzadeh M (2012) Abating colon cancer polyposis by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc Natl Acad Sci USA 109(26):10462–10467PubMedGoogle Scholar
  36. 36.
    Mazmanian SK, Round JL, Kasper DL (2008) A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453(7195):620–625PubMedGoogle Scholar
  37. 37.
    Leblanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D, Ventura M (2012) Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol (in press)Google Scholar
  38. 38.
    Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, Heath AC, Warner B, Reeder J, Kuczynski J, Caporaso JG, Lozupone CA, Lauber C, Clemente JC, Knights D, Knight R, Gordon JI (2012) Human gut microbiome viewed across age and geography. Nature 486(7402):222–227PubMedCentralPubMedGoogle Scholar
  39. 39.
    Claesson MJ, Jeffery IB, Conde S, Power SE, O’Connor EM, Cusack S, Harris HM, Coakley M, Lakshminarayanan B, O’Sullivan O, Fitzgerald GF, Deane J, O’Connor M, Harnedy N, O’Connor K, O’Mahony D, van Sinderen D, Wallace M, Brennan L, Stanton C, Marchesi JR, Fitzgerald AP, Shanahan F, Hill C, Ross RP, O’Toole PW (2012) Gut microbiota composition correlates with diet and health in the elderly. Nature 488(7410):178–184PubMedGoogle Scholar
  40. 40.
    Wong JM, de Souza R, Kendall CW, Emam A, Jenkins DJ (2006) Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol 40(3):235–243PubMedGoogle Scholar
  41. 41.
    Bergman EN (1990) Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol Rev 70(2):567–590PubMedGoogle Scholar
  42. 42.
    Cryan JF, Dinan TG (2012) Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 13(10):701–712PubMedGoogle Scholar
  43. 43.
    Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, Bienenstock J, Cryan JF (2011) Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci USA 108(38):16050–16055PubMedGoogle Scholar
  44. 44.
    Mai V, Young CM, Ukhanova M, Wang X, Sun Y, Casella G, Theriaque D, Li N, Sharma R, Hudak M, Neu J (2011) Fecal microbiota in premature infants prior to necrotizing enterocolitis. PLoS One 6(6):e20647PubMedCentralPubMedGoogle Scholar
  45. 45.
    Giongo A, Gano KA, Crabb DB, Mukherjee N, Novelo LL, Casella G, Drew JC, Ilonen J, Knip M, Hyoty H, Veijola R, Simell T, Simell O, Neu J, Wasserfall CH, Schatz D, Atkinson MA, Triplett EW (2011) Toward defining the autoimmune microbiome for type 1 diabetes. ISME J 5(1):82–91PubMedGoogle Scholar
  46. 46.
    Larsen N, Vogensen FK, van den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK, Al-Soud WA, Sorensen SJ, Hansen LH, Jakobsen M (2010) Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One 5(2):e9085PubMedCentralPubMedGoogle Scholar
  47. 47.
    Carroll IM, Ringel-Kulka T, Keku TO, Chang YH, Packey CD, Sartor RB, Ringel Y (2011) Molecular analysis of the luminal- and mucosal-associated intestinal microbiota in diarrhea-predominant irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol 301(5):G799–G807PubMedGoogle Scholar
  48. 48.
    Saulnier DM, Riehle K, Mistretta TA, Diaz MA, Mandal D, Raza S, Weidler EM, Qin X, Coarfa C, Milosavljevic A, Petrosino JF, Highlander S, Gibbs R, Lynch SV, Shulman RJ, Versalovic J (2011) Gastrointestinal microbiome signatures of pediatric patients with irritable bowel syndrome. Gastroenterology 141(5):1782–1791PubMedCentralPubMedGoogle Scholar
  49. 49.
    Watanabe J, Fujiwara R, Sasajima N, Ito S, Sonoyama K (2010) Administration of antibiotics during infancy promoted the development of atopic dermatitis-like skin lesions in NC/Nga mice. Biosci Biotechnol Biochem 74(2):358–363PubMedGoogle Scholar
  50. 50.
    Sobhani I, Tap J, Roudot-Thoraval F, Roperch JP, Letulle S, Langella P, Corthier G, Tran Van Nhieu J, Furet JP (2011) Microbial dysbiosis in colorectal cancer (CRC) patients. PLoS One 6(1):e16393PubMedCentralPubMedGoogle Scholar
  51. 51.
    Hawrelak JA, Myers SP (2004) The causes of intestinal dysbiosis: a review. Altern Med Rev 9(2):180–197PubMedGoogle Scholar
  52. 52.
    De Palma G, Nadal I, Medina M, Donat E, Ribes-Koninckx C, Calabuig M, Sanz Y (2010) Intestinal dysbiosis and reduced immunoglobulin-coated bacteria associated with coeliac disease in children. BMC Microbiol 10:63PubMedCentralPubMedGoogle Scholar
  53. 53.
    Nadal I, Donat E, Ribes-Koninckx C, Calabuig M, Sanz Y (2007) Imbalance in the composition of the duodenal microbiota of children with coeliac disease. J Med Microbiol 56(Pt 12):1669–1674PubMedGoogle Scholar
  54. 54.
    Roesch LF, Lorca GL, Casella G, Giongo A, Naranjo A, Pionzio AM, Li N, Mai V, Wasserfall CH, Schatz D, Atkinson MA, Neu J, Triplett EW (2009) Culture-independent identification of gut bacteria correlated with the onset of diabetes in a rat model. ISME J 3(5):536–548PubMedCentralPubMedGoogle Scholar
  55. 55.
    Matsuzaki T, Nagata Y, Kado S, Uchida K, Kato I, Hashimoto S, Yokokura T (1997) Prevention of onset in an insulin-dependent diabetes mellitus model, NOD mice, by oral feeding of Lactobacillus casei. Acta Pathol Microbiol Immunol Scand 105(8):643–649Google Scholar
  56. 56.
    Mike A, Nagaoka N, Tagami Y, Miyashita M, Shimada S, Uchida K, Nanno M, Ohwaki M (1999) Prevention of B220+ T cell expansion and prolongation of lifespan induced by Lactobacillus casei in MRL/lpr mice. Clin Exp Immunol 117(2):368–375PubMedCentralPubMedGoogle Scholar
  57. 57.
    Matsumoto S, Hara T, Hori T, Mitsuyama K, Nagaoka M, Tomiyasu N, Suzuki A, Sata M (2005) Probiotic Lactobacillus-induced improvement in murine chronic inflammatory bowel disease is associated with the down-regulation of pro-inflammatory cytokines in lamina propria mononuclear cells. Clin Exp Immunol 140(3):417–426PubMedCentralPubMedGoogle Scholar
  58. 58.
    Gaya DR, Russell RK, Nimmo ER, Satsangi J (2006) New genes in inflammatory bowel disease: lessons for complex diseases? Lancet 367(9518):1271–1284PubMedGoogle Scholar
  59. 59.
    Bouma G, Strober W (2003) The immunological and genetic basis of inflammatory bowel disease. Nat Rev Immunol 3(7):521–533PubMedGoogle Scholar
  60. 60.
    Uronis JM, Muhlbauer M, Herfarth HH, Rubinas TC, Jones GS, Jobin C (2009) Modulation of the intestinal microbiota alters colitis-associated colorectal cancer susceptibility. PLoS One 4(6):e6026PubMedCentralPubMedGoogle Scholar
  61. 61.
    Willing B, Halfvarson J, Dicksved J, Rosenquist M, Jarnerot G, Engstrand L, Tysk C, Jansson JK (2009) Twin studies reveal specific imbalances in the mucosa-associated microbiota of patients with ileal Crohn’s disease. Inflamm Bowel Dis 15(5):653–660PubMedGoogle Scholar
  62. 62.
    Meyer AM, Ramzan NN, Loftus EV Jr, Heigh RI, Leighton JA (2004) The diagnostic yield of stool pathogen studies during relapses of inflammatory bowel disease. J Clin Gastroenterol 38(9):772–775PubMedGoogle Scholar
  63. 63.
    Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L, Nalin R, Jarrin C, Chardon P, Marteau P, Roca J, Dore J (2006) Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut 55(2):205–211PubMedGoogle Scholar
  64. 64.
    Favier C, Neut C, Mizon C, Cortot A, Colombel JF, Mizon J (1997) Fecal beta-D-galactosidase production and Bifidobacteria are decreased in Crohn’s disease. Dig Dis Sci 42(4):817–822PubMedGoogle Scholar
  65. 65.
    Mangin I, Bonnet R, Seksik P, Rigottier-Gois L, Sutren M, Bouhnik Y, Neut C, Collins MD, Colombel JF, Marteau P, Dore J (2004) Molecular inventory of faecal microflora in patients with Crohn’s disease. FEMS Microbiol Ecol 50(1):25–36PubMedGoogle Scholar
  66. 66.
    Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, Gratadoux JJ, Blugeon S, Bridonneau C, Furet JP, Corthier G, Grangette C, Vasquez N, Pochart P, Trugnan G, Thomas G, Blottiere HM, Dore J, Marteau P, Seksik P, Langella P (2008) Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 105(43):16731–16736PubMedGoogle Scholar
  67. 67.
    Segain JP, Raingeard de la Bletiere D, Bourreille A, Leray V, Gervois N, Rosales C, Ferrier L, Bonnet C, Blottiere HM, Galmiche JP (2000) Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn’s disease. Gut 47(3):397–403PubMedGoogle Scholar
  68. 68.
    Sanderson IR (2004) Short chain fatty acid regulation of signaling genes expressed by the intestinal epithelium. J Nutr 134(9):2450S–2454SPubMedGoogle Scholar
  69. 69.
    Toki S, Kagaya S, Shinohara M, Wakiguchi H, Matsumoto T, Takahata Y, Morimatsu F, Saito H, Matsumoto K (2009) Lactobacillus rhamnosus GG and Lactobacillus casei suppress Escherichia coli-induced chemokine expression in intestinal epithelial cells. Int Arch Allergy Immunol 148(1):45–58PubMedGoogle Scholar
  70. 70.
    Madsen K, Cornish A, Soper P, McKaigney C, Jijon H, Yachimec C, Doyle J, Jewell L, De Simone C (2001) Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 121(3):580–591PubMedGoogle Scholar
  71. 71.
    Pagnini C, Saeed R, Bamias G, Arseneau KO, Pizarro TT, Cominelli F (2010) Probiotics promote gut health through stimulation of epithelial innate immunity. Proc Natl Acad Sci USA 107(1):454–459PubMedGoogle Scholar
  72. 72.
    Uronis JM, Arthur JC, Keku T, Fodor A, Carroll IM, Cruz ML, Appleyard CB, Jobin C (2011) Gut microbial diversity is reduced by the probiotic VSL#3 and correlates with decreased TNBS-induced colitis. Inflamm Bowel Dis 17(1):289–297PubMedCentralPubMedGoogle Scholar
  73. 73.
    Bassaganya-Riera J, Viladomiu M, Pedragosa M, De Simone C, Hontecillas R (2012) Immunoregulatory mechanisms underlying prevention of colitis-associated colorectal cancer by probiotic bacteria. PLoS One 7(4):e34676PubMedCentralPubMedGoogle Scholar
  74. 74.
    Loguercio C, Federico A, Tuccillo C, Terracciano F, D’Auria MV, De Simone C, Del Vecchio Blanco C (2005) Beneficial effects of a probiotic VSL#3 on parameters of liver dysfunction in chronic liver diseases. J Clin Gastroenterol 39(6):540–543PubMedGoogle Scholar
  75. 75.
    Isolauri E (2004) Dietary modification of atopic disease: use of probiotics in the prevention of atopic dermatitis. Curr Allergy Asthma Rep 4(4):270–275PubMedGoogle Scholar
  76. 76.
    Rautava S, Ruuskanen O, Ouwehand A, Salminen S, Isolauri E (2004) The hygiene hypothesis of atopic disease–an extended version. J Pediatr Gastroenterol Nutr 38(4):378–388PubMedGoogle Scholar
  77. 77.
    Okada H, Kuhn C, Feillet H, Bach JF (2010) The ‘hygiene hypothesis’ for autoimmune and allergic diseases: an update. Clin Exp Immunol 160(1):1–9PubMedCentralPubMedGoogle Scholar
  78. 78.
    Noverr MC, Huffnagle GB (2005) The ‘microflora hypothesis’ of allergic diseases. Clin Exp Allergy 35(12):1511–1520PubMedGoogle Scholar
  79. 79.
    Kalliomaki M, Salminen S, Arvilommi H, Kero P, Koskinen P, Isolauri E (2001) Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet 357(9262):1076–1079PubMedGoogle Scholar
  80. 80.
    Bjorksten B, Sepp E, Julge K, Voor T, Mikelsaar M (2001) Allergy development and the intestinal microflora during the first year of life. J Allergy Clin Immunol 108(4):516–520PubMedGoogle Scholar
  81. 81.
    Penders J, Thijs C, van den Brandt PA, Kummeling I, Snijders B, Stelma F, Adams H, van Ree R, Stobberingh EE (2007) Gut microbiota composition and development of atopic manifestations in infancy: the KOALA birth cohort study. Gut 56(5):661–667PubMedGoogle Scholar
  82. 82.
    Ventura M, Canchaya C, Fitzgerald GF, Gupta RS, van Sinderen D (2007) Genomics as a means to understand bacterial phylogeny and ecological adaptation: the case of bifidobacteria. Antonie Van Leeuwenhoek 91(4):351–372PubMedGoogle Scholar
  83. 83.
    Reid G, Younes JA, Van der Mei HC, Gloor GB, Knight R, Busscher HJ (2011) Microbiota restoration: natural and supplemented recovery of human microbial communities. Nat Rev Microbiol 9(1):27–38PubMedGoogle Scholar
  84. 84.
    Velraeds MM, van de Belt-Gritter B, van der Mei HC, Reid G, Busscher HJ (1998) Interference in initial adhesion of uropathogenic bacteria and yeasts to silicone rubber by a Lactobacillus acidophilus biosurfactant. J Med Microbiol 47(12):1081–1085PubMedGoogle Scholar
  85. 85.
    Reid G, Kang YS, Lacerte M, Tieszer C, Hayes KC (1993) Bacterial biofilm formation on the bladder epithelium of spinal cord injured patients. II. Toxic outcome on cell viability. Paraplegia 31(8):494–499PubMedGoogle Scholar
  86. 86.
    Asaduzzaman SM, Sonomoto K (2009) Lantibiotics: diverse activities and unique modes of action. J Biosci Bioeng 107(5):475–487PubMedGoogle Scholar
  87. 87.
    Cotter PD, Hill C, Ross RP (2005) Bacteriocins: developing innate immunity for food. Nat Rev Microbiol 3(10):777–788PubMedGoogle Scholar
  88. 88.
    Hillman JD (2002) Genetically modified Streptococcus mutans for the prevention of dental caries. Antonie Van Leeuwenhoek 82(1–4):361–366PubMedGoogle Scholar
  89. 89.
    Flynn S, van Sinderen D, Thornton GM, Holo H, Nes IF, Collins JK (2002) Characterization of the genetic locus responsible for the production of ABP-118, a novel bacteriocin produced by the probiotic bacterium Lactobacillus salivarius subsp. salivarius UCC118. Microbiology 148((Pt 4)):973–984PubMedGoogle Scholar
  90. 90.
    Corr SC, Li Y, Riedel CU, O’Toole PW, Hill C, Gahan CG (2007) Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. Proc Natl Acad Sci USA 104(18):7617–7621PubMedGoogle Scholar
  91. 91.
    Murphy EF, Clarke SF, Marques TM, Hill C, Stanton C, Ross RP, O’Doherty RM, Shanahan F, Cotter PD (2013) Antimicrobials: strategies for targeting obesity and metabolic health? Gut microbes 4(1):48–53PubMedGoogle Scholar
  92. 92.
    Liu CH, Lee SM, Vanlare JM, Kasper DL, Mazmanian SK (2008) Regulation of surface architecture by symbiotic bacteria mediates host colonization. Proc Natl Acad Sci USA 105(10):3951–3956PubMedGoogle Scholar
  93. 93.
    Aas J, Gessert CE, Bakken JS (2003) Recurrent Clostridium difficile colitis: case series involving 18 patients treated with donor stool administered via a nasogastric tube. Clin Infect Dis 36(5):580–585PubMedGoogle Scholar
  94. 94.
    Bakken JS, Borody T, Brandt LJ, Brill JV, Demarco DC, Franzos MA, Kelly C, Khoruts A, Louie T, Martinelli LP, Moore TA, Russell G, Surawicz C, Fecal Microbiota Transplantation Workgroup (2011) Treating Clostridium difficile infection with fecal microbiota transplantation. Clin Gastroenterol Hepatol 9(12):1044–1049PubMedCentralPubMedGoogle Scholar
  95. 95.
    Gough E, Shaikh H, Manges AR (2011) Systematic review of intestinal microbiota transplantation (fecal bacteriotherapy) for recurrent Clostridium difficile infection. Clin Infect Dis 53(10):994–1002PubMedGoogle Scholar
  96. 96.
    van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, Visser CE, Kuijper EJ, Bartelsman JF, Tijssen JG, Speelman P, Dijkgraaf MG, Keller JJ (2013) Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med 368(5):407–415PubMedGoogle Scholar
  97. 97.
    Hickson M, D’Souza AL, Muthu N, Rogers TR, Want S, Rajkumar C, Bulpitt CJ (2007) Use of probiotic Lactobacillus preparation to prevent diarrhoea associated with antibiotics: randomised double blind placebo controlled trial. BMJ 335(7610):80PubMedGoogle Scholar
  98. 98.
    Guglielmetti S, Mora D, Gschwender M, Popp K (2011) Randomised clinical trial: Bifidobacterium bifidum MIMBb75 significantly alleviates irritable bowel syndrome and improves quality of life–a double-blind, placebo-controlled study. Aliment Pharmacol Ther 33(10):1123–1132. xPubMedGoogle Scholar
  99. 99.
    O’Mahony L, McCarthy J, Kelly P, Hurley G, Luo F, Chen K, O’Sullivan GC, Kiely B, Collins JK, Shanahan F, Quigley EM (2005) Lactobacillus and bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles. Gastroenterology 128(3):541–551PubMedGoogle Scholar
  100. 100.
    Turroni F, van Sinderen D, Ventura M (2011) Genomics and ecological overview of the genus Bifidobacterium. Int J Food Microbiol 149(1):37–44PubMedGoogle Scholar
  101. 101.
    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(22):14422–14427PubMedGoogle Scholar
  102. 102.
    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 Genomics 9:247PubMedCentralPubMedGoogle Scholar
  103. 103.
    Turroni F, Bottacini F, Foroni E, Mulder I, Kim JH, Zomer A, Sanchez 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 USA 107(45):19514–19519PubMedGoogle Scholar
  104. 104.
    O’Connell Motherway M, Zomer A, Leahy SC, Reunanen J, Bottacini F, Claesson MJ, O’Brien F, Flynn K, Casey PG, 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 USA 108(27):11217–11222PubMedGoogle Scholar
  105. 105.
    Pokusaeva K, Fitzgerald GF, van Sinderen D (2011) Carbohydrate metabolism in Bifidobacteria. Genes Nutr 6(3):285–306PubMedCentralPubMedGoogle Scholar
  106. 106.
    Hansson GC (2012) Role of mucus layers in gut infection and inflammation. Curr Opin Microbiol 15(1):57–62PubMedCentralPubMedGoogle Scholar
  107. 107.
    Forstner JO, Oliver MG, Sylvester FA (1995) Production, structure and biologic relevance of gastrointestinal mucins. Raven, New YorkGoogle Scholar
  108. 108.
    Nagae M, Tsuchiya A, Katayama T, Yamamoto K, Wakatsuki S, Kato R (2007) Structural basis of the catalytic reaction mechanism of novel 1,2-alpha-L-fucosidase from Bifidobacterium bifidum. J Biol Chem 282(25):18497–18509PubMedGoogle Scholar
  109. 109.
    Ashida H, Maki R, Ozawa H, Tani Y, Kiyohara M, Fujita M, Imamura A, Ishida H, Kiso M, Yamamoto K (2008) Characterization of two different endo-alpha-N-acetylgalactosaminidases from probiotic and pathogenic enterobacteria, Bifidobacterium longum and Clostridium perfringens. Glycobiology 18(9):727–734PubMedGoogle Scholar
  110. 110.
    Katayama T, Fujita K, Yamamoto K (2005) Novel bifidobacterial glycosidases acting on sugar chains of mucin glycoproteins. J Biosci Bioeng 99(5):457–465PubMedGoogle Scholar
  111. 111.
    Miwa M, Horimoto T, Kiyohara M, Katayama T, Kitaoka M, Ashida H, Yamamoto K (2010) Cooperation of beta-galactosidase and beta-N-acetylhexosaminidase from bifidobacteria in assimilation of human milk oligosaccharides with type 2 structure. Glycobiology 20(11):1402–1409PubMedGoogle Scholar
  112. 112.
    Kiyohara M, Nakatomi T, Kurihara S, Fushinobu S, Suzuki H, Tanaka T, Shoda S, Kitaoka M, Katayama T, Yamamoto K, Ashida H (2012) alpha-N-acetylgalactosaminidase from infant-associated bifidobacteria belonging to novel glycoside hydrolase family 129 is implicated in alternative mucin degradation pathway. J Biol Chem 287(1):693–700PubMedGoogle Scholar
  113. 113.
    Derrien M, Collado MC, Ben-Amor K, Salminen S, de Vos WM (2008) The Mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract. Appl Environ Microbiol 74(5):1646–1648PubMedCentralPubMedGoogle Scholar
  114. 114.
    Collado MC, Derrien M, Isolauri E, de Vos WM, Salminen S (2007) Intestinal integrity and Akkermansia muciniphila, a mucin-degrading member of the intestinal microbiota present in infants, adults, and the elderly. Appl Environ Microbiol 73(23):7767–7770PubMedCentralPubMedGoogle Scholar
  115. 115.
    Derrien M, van Passel MW, van de Bovenkamp JH, Schipper RG, de Vos WM, Dekker J (2010) Mucin-bacterial interactions in the human oral cavity and digestive tract. Gut microbes 1(4):254–268PubMedGoogle Scholar
  116. 116.
    van Passel MW, Kant R, Zoetendal EG, Plugge CM, Derrien M, Malfatti SA, Chain PS, Woyke T, Palva A, de Vos WM, Smidt H (2011) The genome of Akkermansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagenomes. PLoS One 6(3):e16876PubMedCentralPubMedGoogle Scholar
  117. 117.
    Turroni F, Milani C, van Sinderen D, Ventura M (2011) Genetic strategies for mucin metabolism in Bifidobacterium bifidum PRL2010: an example of possible human-microbe co-evolution. Gut Microbes 2(3):183–189PubMedGoogle Scholar
  118. 118.
    van den Broek LA, Hinz SW, Beldman G, Vincken JP, Voragen AG (2008) Bifidobacterium carbohydrases-their role in breakdown and synthesis of (potential) prebiotics. Mol Nutr Food Res 52(1):146–163PubMedGoogle Scholar
  119. 119.
    Turroni F, Strati F, Foroni E, Serafini F, Duranti S, van Sinderen D, Ventura M (2012) Analysis of predicted carbohydrate transport systems encoded by Bifidobacterium bifidum PRL2010. Appl Environ Microbiol 78(14):5002–5012PubMedCentralPubMedGoogle Scholar
  120. 120.
    Parche S, Amon J, Jankovic I, Rezzonico E, Beleut M, Barutcu H, Schendel I, Eddy MP, Burkovski A, Arigoni F, Titgemeyer F (2007) Sugar transport systems of Bifidobacterium longum NCC2705. J Mol Microbiol Biotechnol 12(1–2):9–19PubMedGoogle Scholar
  121. 121.
    Asakuma S, Hatakeyama E, Urashima T, Yoshida E, Katayama T, Yamamoto K, Kumagai H, Ashida H, Hirose J, Kitaoka M (2011) Physiology of consumption of human milk oligosaccharides by infant gut-associated bifidobacteria. J Biol Chem 286(40):34583–34592PubMedGoogle Scholar
  122. 122.
    Sela DA (2011) Bifidobacterial utilization of human milk oligosaccharides. Int J Food Microbiol 149(1):58–64PubMedGoogle Scholar
  123. 123.
    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(5):734–759PubMedGoogle Scholar
  124. 124.
    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(22):7039–7049PubMedCentralPubMedGoogle Scholar
  125. 125.
    Claesson MJ, van Sinderen D, O’Toole PW (2008) Lactobacillus phylogenomics–towards a reclassification of the genus. Int J Syst Evol Microbiol 58(Pt 12):2945–2954PubMedGoogle Scholar
  126. 126.
    Stiles ME, Holzapfel WH (1997) Lactic acid bacteria of foods and their current taxonomy. Int J Food Microbiol 36(1):1–29PubMedGoogle Scholar
  127. 127.
    Makarova KS, Koonin EV (2007) Evolutionary genomics of lactic acid bacteria. J Bacteriol 189(4):1199–1208PubMedCentralPubMedGoogle Scholar
  128. 128.
    Heilig HG, Zoetendal EG, Vaughan EE, Marteau P, Akkermans AD, de Vos WM (2002) Molecular diversity of Lactobacillus spp. and other lactic acid bacteria in the human intestine as determined by specific amplification of 16S ribosomal DNA. Appl Environ Microbiol 68(1):114–123PubMedCentralPubMedGoogle Scholar
  129. 129.
    Reuter G (2001) The Lactobacillus and Bifidobacterium microflora of the human intestine: composition and succession. Curr Issues Intest Microbiol 2(2):43–53PubMedGoogle Scholar
  130. 130.
    Walter J, Hertel C, Tannock GW, Lis CM, Munro K, Hammes WP (2001) Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl Environ Microbiol 67(6):2578–2585PubMedCentralPubMedGoogle Scholar
  131. 131.
    Satokari RM, Vaughan EE, Akkermans AD, Saarela M, de Vos WM (2001) Bifidobacterial diversity in human feces detected by genus-specific PCR and denaturing gradient gel electrophoresis. Appl Environ Microbiol 67(2):504–513PubMedCentralPubMedGoogle Scholar
  132. 132.
    Zoetendal EG, Raes J, van den Bogert B, Arumugam M, Booijink CC, Troost FJ, Bork P, Wels M, de Vos WM, Kleerebezem M (2012) The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J 6(7):1415–1426PubMedGoogle Scholar
  133. 133.
    Booijink CC, El-Aidy S, Rajilic-Stojanovic M, Heilig HG, Troost FJ, Smidt H, Kleerebezem M, De Vos WM, Zoetendal EG (2010) High temporal and inter-individual variation detected in the human ileal microbiota. Environ Microbiol 12(12):3213–3227PubMedGoogle Scholar
  134. 134.
    Kleerebezem M, Vaughan EE (2009) Probiotic and gut lactobacilli and bifidobacteria: molecular approaches to study diversity and activity. Annu Rev Microbiol 63:269–290PubMedGoogle Scholar
  135. 135.
    Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B, Koonin E, Pavlov A, Pavlova N, Karamychev V, Polouchine N, Shakhova V, Grigoriev I, Lou Y, Rohksar D, Lucas S, Huang K, Goodstein DM, Hawkins T, Plengvidhya V, Welker D, Hughes J, Goh Y, Benson A, Baldwin K, Lee JH, Diaz-Muniz I, Dosti B, Smeianov V, Wechter W, Barabote R, Lorca G, Altermann E, Barrangou R, Ganesan B, Xie Y, Rawsthorne H, Tamir D, Parker C, Breidt F, Broadbent J, Hutkins R, O’Sullivan D, Steele J, Unlu G, Saier M, Klaenhammer T, Richardson P, Kozyavkin S, Weimer B, Mills D (2006) Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci USA 103(42):15611–15616PubMedGoogle Scholar
  136. 136.
    Kleerebezem M, Boekhorst J, van Kranenburg R, Molenaar D, Kuipers OP, Leer R, Tarchini R, Peters SA, Sandbrink HM, Fiers MW, Stiekema W, Lankhorst RM, Bron PA, Hoffer SM, Groot MN, Kerkhoven R, de Vries M, Ursing B, de Vos WM, Siezen RJ (2003) Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci USA 100(4):1990–1995PubMedGoogle Scholar
  137. 137.
    Siezen R, Boekhorst J, Muscariello L, Molenaar D, Renckens B, Kleerebezem M (2006) Lactobacillus plantarum gene clusters encoding putative cell-surface protein complexes for carbohydrate utilization are conserved in specific gram-positive bacteria. BMC Genomics 7:126PubMedCentralPubMedGoogle Scholar
  138. 138.
    Lambert JM, Siezen RJ, de Vos WM, Kleerebezem M (2008) Improved annotation of conjugated bile acid hydrolase superfamily members in Gram-positive bacteria. Microbiology 154(Pt 8):2492–2500PubMedGoogle Scholar
  139. 139.
    Claesson MJ, Li Y, Leahy S, Canchaya C, van Pijkeren JP, Cerdeno-Tarraga AM, Parkhill J, Flynn S, O’Sullivan GC, Collins JK, Higgins D, Shanahan F, Fitzgerald GF, van Sinderen D, O’Toole PW (2006) Multireplicon genome architecture of Lactobacillus salivarius. Proc Natl Acad Sci USA 103(17):6718–6723PubMedGoogle Scholar
  140. 140.
    Pridmore RD, Berger B, Desiere F, Vilanova D, Barretto C, Pittet AC, Zwahlen MC, Rouvet M, Altermann E, Barrangou R, Mollet B, Mercenier A, Klaenhammer T, Arigoni F, Schell MA (2004) The genome sequence of the probiotic intestinal bacterium Lactobacillus johnsonii NCC 533. Proc Natl Acad Sci USA 101(8):2512–2517PubMedGoogle Scholar
  141. 141.
    Boekhorst J, Wels M, Kleerebezem M, Siezen RJ (2006) The predicted secretome of Lactobacillus plantarum WCFS1 sheds light on interactions with its environment. Microbiology 152(Pt 11):3175–3183PubMedGoogle Scholar
  142. 142.
    Barrangou R, Altermann E, Hutkins R, Cano R, Klaenhammer TR (2003) Functional and comparative genomic analyses of an operon involved in fructooligosaccharide utilization by Lactobacillus acidophilus. Proc Natl Acad Sci USA 100(15):8957–8962PubMedGoogle Scholar
  143. 143.
    Buck BL, Altermann E, Svingerud T, Klaenhammer TR (2005) Functional analysis of putative adhesion factors in Lactobacillus acidophilus NCFM. Appl Environ Microbiol 71(12):8344–8351PubMedCentralPubMedGoogle Scholar
  144. 144.
    Ventura M, Turroni F, Motherway MO, MacSharry J, van Sinderen D (2012) Host-microbe interactions that facilitate gut colonization by commensal bifidobacteria. Trends Microbiol 20(10):467–476PubMedGoogle Scholar
  145. 145.
    McCracken VJ, Lorenz RG (2001) The gastrointestinal ecosystem: a precarious alliance among epithelium, immunity and microbiota. Cell Microbiol 3(1):1–11PubMedGoogle Scholar
  146. 146.
    Bevins CL, Salzman NH (2011) Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat Rev Microbiol 9(5):356–368PubMedGoogle Scholar
  147. 147.
    Salzman NH (2011) Microbiota-immune system interaction: an uneasy alliance. Curr Opin Microbiol 14(1):99–105PubMedCentralPubMedGoogle Scholar
  148. 148.
    Wells JM, Rossi O, Meijerink M, van Baarlen P (2011) Epithelial crosstalk at the microbiota-mucosal interface. Proc Natl Acad Sci USA 108(Suppl 1):4607–4614PubMedGoogle Scholar
  149. 149.
    Liew FY (2002) T(H)1 and T(H)2 cells: a historical perspective. Nat Rev Immunol 2(1):55–60PubMedGoogle Scholar
  150. 150.
    Kelsall BL (2008) A focus on dendritic cells and macrophages as key regulators of mucosal immunity. Mucosal Immunol 1(6):423–424PubMedGoogle Scholar
  151. 151.
    Rescigno M (2010) Intestinal dendritic cells. Adv Immunol 107:109–138PubMedGoogle Scholar
  152. 152.
    Sansonetti PJ, Medzhitov R (2009) Learning tolerance while fighting ignorance. Cell 138(3):416–420PubMedGoogle Scholar
  153. 153.
    Chung H, Kasper DL (2010) Microbiota-stimulated immune mechanisms to maintain gut homeostasis. Curr Opin Immunol 22(4):455–460PubMedGoogle Scholar
  154. 154.
    Artis D (2008) Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat Rev Immunol 8(6):411–420PubMedGoogle Scholar
  155. 155.
    Asong J, Wolfert MA, Maiti KK, Miller D, Boons GJ (2009) Binding and cellular activation studies reveal that Toll-like receptor 2 can differentially recognize peptidoglycan from Gram-positive and Gram-negative bacteria. J Biol Chem 284(13):8643–8653PubMedGoogle Scholar
  156. 156.
    Takeda K, Kaisho T, Akira S (2003) Toll-like receptors. Annu Rev Immunol 21:335–376PubMedGoogle Scholar
  157. 157.
    Volz T, Nega M, Buschmann J, Kaesler S, Guenova E, Peschel A, Rocken M, Gotz F, Biedermann T (2010) Natural Staphylococcus aureus-derived peptidoglycan fragments activate NOD2 and act as potent costimulators of the innate immune system exclusively in the presence of TLR signals. FASEB J 24(10):4089–4102PubMedGoogle Scholar
  158. 158.
    Zeuthen LH, Fink LN, Frokiaer H (2008) Epithelial cells prime the immune response to an array of gut-derived commensals towards a tolerogenic phenotype through distinct actions of thymic stromal lymphopoietin and transforming growth factor-beta. Immunology 123(2):197–208PubMedGoogle Scholar
  159. 159.
    Chamaillard M, Hashimoto M, Horie Y, Masumoto J, Qiu S, Saab L, Ogura Y, Kawasaki A, Fukase K, Kusumoto S, Valvano MA, Foster SJ, Mak TW, Nunez G, Inohara N (2003) An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat Immunol 4(7):702–707PubMedGoogle Scholar
  160. 160.
    Macho Fernandez E, Valenti V, Rockel C, Hermann C, Pot B, Boneca IG, Grangette C (2011) Anti-inflammatory capacity of selected lactobacilli in experimental colitis is driven by NOD2-mediated recognition of a specific peptidoglycan-derived muropeptide. Gut 60(8):1050–1059PubMedGoogle Scholar
  161. 161.
    Shida K, Kiyoshima-Shibata J, Kaji R, Nagaoka M, Nanno M (2009) Peptidoglycan from lactobacilli inhibits interleukin-12 production by macrophages induced by Lactobacillus casei through Toll-like receptor 2-dependent and independent mechanisms. Immunology 128(1 Suppl):e858–e869PubMedGoogle Scholar
  162. 162.
    Matsumoto S, Hara T, Nagaoka M, Mike A, Mitsuyama K, Sako T, Yamamoto M, Kado S, Takada T (2009) A component of polysaccharide peptidoglycan complex on Lactobacillus induced an improvement of murine model of inflammatory bowel disease and colitis-associated cancer. Immunology 128(1 Suppl):e170–e180PubMedGoogle Scholar
  163. 163.
    Xia G, Kohler T, Peschel A (2010) The wall teichoic acid and lipoteichoic acid polymers of Staphylococcus aureus. Intern J Med Microbiol 300(2–3):148–154Google Scholar
  164. 164.
    Grangette C, Nutten S, Palumbo E, Morath S, Hermann C, Dewulf J, Pot B, Hartung T, Hols P, Mercenier A (2005) Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids. Proc Natl Acad Sci USA 102(29):10321–10326PubMedGoogle Scholar
  165. 165.
    Mohamadzadeh M, Pfeiler EA, Brown JB, Zadeh M, Gramarossa M, Managlia E, Bere P, Sarraj B, Khan MW, Pakanati KC, Ansari MJ, O’Flaherty S, Barrett T, Klaenhammer TR (2011) Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc Natl Acad Sci USA 108(Suppl 1):4623–4630PubMedGoogle Scholar
  166. 166.
    Saber R, Zadeh M, Pakanati KC, Bere P, Klaenhammer T, Mohamadzadeh M (2011) Lipoteichoic acid-deficient Lactobacillus acidophilus regulates downstream signals. Immunotherapy 3(3):337–347PubMedGoogle Scholar
  167. 167.
    Ryu YH, Baik JE, Yang JS, Kang SS, Im J, Yun CH, Kim DW, Lee K, Chung DK, Ju HR, Han SH (2009) Differential immunostimulatory effects of Gram-positive bacteria due to their lipoteichoic acids. Int Immunopharmacol 9(1):127–133PubMedGoogle Scholar
  168. 168.
    Deininger S, Stadelmaier A, von Aulock S, Morath S, Schmidt RR, Hartung T (2003) Definition of structural prerequisites for lipoteichoic acid-inducible cytokine induction by synthetic derivatives. J Immunol 170(8):4134–4138PubMedGoogle Scholar
  169. 169.
    Lebeer S, Verhoeven TL, Perea Velez M, Vanderleyden J, De Keersmaecker SC (2007) Impact of environmental and genetic factors on biofilm formation by the probiotic strain Lactobacillus rhamnosus GG. Appl Environ Microbiol 73(21):6768–6775PubMedCentralPubMedGoogle Scholar
  170. 170.
    Walter J, Loach DM, Alqumber M, Rockel C, Hermann C, Pfitzenmaier M, Tannock GW (2007) D-alanyl ester depletion of teichoic acids in Lactobacillus reuteri 100–23 results in impaired colonization of the mouse gastrointestinal tract. Environ Microbiol 9(7):1750–1760PubMedGoogle Scholar
  171. 171.
    Claes IJ, Lebeer S, Shen C, Verhoeven TL, Dilissen E, De Hertogh G, Bullens DM, Ceuppens JL, Van Assche G, Vermeire S, Rutgeerts P, Vanderleyden J, De Keersmaecker SC (2010) Impact of lipoteichoic acid modification on the performance of the probiotic Lactobacillus rhamnosus GG in experimental colitis. Clin Exp Immunol 162(2):306–314PubMedCentralPubMedGoogle Scholar
  172. 172.
    Duncker SC, Wang L, Hols P, Bienenstock J (2008) The d-alanine content of lipoteichoic acid is crucial for Lactobacillus plantarum-mediated protection from visceral pain perception in a rat colorectal distension model. Neurogastroenterol Motil 20(7):843–850PubMedGoogle Scholar
  173. 173.
    Kim HG, Kim NR, Gim MG, Lee JM, Lee SY, Ko MY, Kim JY, Han SH, Chung DK (2008) Lipoteichoic acid isolated from Lactobacillus plantarum inhibits lipopolysaccharide-induced TNF-alpha production in THP-1 cells and endotoxin shock in mice. J Immunol 180(4):2553–2561PubMedGoogle Scholar
  174. 174.
    Kaji R, Kiyoshima-Shibata J, Nagaoka M, Nanno M, Shida K (2010) Bacterial teichoic acids reverse predominant IL-12 production induced by certain lactobacillus strains into predominant IL-10 production via TLR2-dependent ERK activation in macrophages. J Immunol 184(7):3505–3513PubMedGoogle Scholar
  175. 175.
    Krinos CM, Coyne MJ, Weinacht KG, Tzianabos AO, Kasper DL, Comstock LE (2001) Extensive surface diversity of a commensal microorganism by multiple DNA inversions. Nature 414(6863):555–558PubMedGoogle Scholar
  176. 176.
    Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL (2005) An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122(1):107–118PubMedGoogle Scholar
  177. 177.
    Mazmanian SK, Kasper DL (2006) The love-hate relationship between bacterial polysaccharides and the host immune system. Nat Rev Immunol 6(11):849–858PubMedGoogle Scholar
  178. 178.
    Kuwahara T, Yamashita A, Hirakawa H, Nakayama H, Toh H, Okada N, Kuhara S, Hattori M, Hayashi T, Ohnishi Y (2004) Genomic analysis of Bacteroides fragilis reveals extensive DNA inversions regulating cell surface adaptation. Proc Natl Acad Sci USA 101(41):14919–14924PubMedGoogle Scholar
  179. 179.
    Cerdeno-Tarraga AM, Patrick S, Crossman LC, Blakely G, Abratt V, Lennard N, Poxton I, Duerden B, Harris B, Quail MA, Barron A, Clark L, Corton C, Doggett J, Holden MT, Larke N, Line A, Lord A, Norbertczak H, Ormond D, Price C, Rabbinowitsch E, Woodward J, Barrell B, Parkhill J (2005) Extensive DNA inversions in the B. fragilis genome control variable gene expression. Science 307((5714)):1463–1465PubMedGoogle Scholar
  180. 180.
    Shen Y, Torchia ML, Lawson GW, Karp CL, Ashwell JD, Mazmanian SK (2012) Outer membrane vesicles of a human commensal mediate immune regulation and disease protection. Cell Host Microbe 12(4):509–520PubMedGoogle Scholar
  181. 181.
    Round JL, Mazmanian SK (2010) Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci USA 107(27):12204–12209PubMedGoogle Scholar
  182. 182.
    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 USA 109(6):2108–2113PubMedGoogle Scholar
  183. 183.
    Lebeer S, Verhoeven TL, Francius G, Schoofs G, Lambrichts I, Dufrene Y, Vanderleyden J, De Keersmaecker SC (2009) Identification of a gene cluster for the biosynthesis of a long, Galactose-Rich Exopolysaccharide in Lactobacillus rhamnosus GG and functional analysis of the priming glycosyltransferase. Appl Environ Microbiol 75(11):3554–3563PubMedCentralPubMedGoogle Scholar
  184. 184.
    Lebeer S, Claes IJ, Verhoeven TL, Vanderleyden J, De Keersmaecker SC (2011) Exopolysaccharides of Lactobacillus rhamnosus GG form a protective shield against innate immune factors in the intestine. Microb Biotechnol 4(3):368–374PubMedGoogle Scholar
  185. 185.
    Hafez M, Hayes K, Goldrick M, Warhurst G, Grencis R, Roberts IS (2009) The K5 capsule of Escherichia coli strain Nissle 1917 is important in mediating interactions with intestinal epithelial cells and chemokine induction. Infect Immun 77(7):2995–3003PubMedCentralPubMedGoogle Scholar
  186. 186.
    Lebeer S, Vanderleyden J, De Keersmaecker SC (2008) Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 72(4):728–764PubMedCentralPubMedGoogle Scholar
  187. 187.
    Sims IM, Frese SA, Walter J, Loach D, Wilson M, Appleyard K, Eason J, Livingston M, Baird M, Cook G, Tannock GW (2011) Structure and functions of exopolysaccharide produced by gut commensal Lactobacillus reuteri 100–23. ISME J 5(7):1115–1124PubMedGoogle Scholar
  188. 188.
    Telford JL, Barocchi MA, Margarit I, Rappuoli R, Grandi G (2006) Pili in gram-positive pathogens. Nat Rev Microbiol 4(7):509–519PubMedGoogle Scholar
  189. 189.
    Kankainen M, Paulin L, Tynkkynen S, von Ossowski I, Reunanen J, Partanen P, Satokari R, Vesterlund S, Hendrickx AP, Lebeer S, De Keersmaecker SC, Vanderleyden J, Hamalainen T, Laukkanen S, Salovuori N, Ritari J, Alatalo E, Korpela R, Mattila-Sandholm T, Lassig A, Hatakka K, Kinnunen KT, Karjalainen H, Saxelin M, Laakso K, Surakka A, Palva A, Salusjarvi T, Auvinen P, de Vos WM (2009) Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human- mucus binding protein. Proc Natl Acad Sci USA 106(40):17193–17198PubMedGoogle Scholar
  190. 190.
    von Ossowski I, Reunanen J, Satokari R, Vesterlund S, Kankainen M, Huhtinen H, Tynkkynen S, Salminen S, de Vos WM, Palva A (2010) Mucosal adhesion properties of the probiotic Lactobacillus rhamnosus GG SpaCBA and SpaFED pilin subunits. Appl Environ Microbiol 76(7):2049–2057Google Scholar
  191. 191.
    Lebeer S, Claes I, Tytgat HL, Verhoeven TL, Marien E, von Ossowski I, Reunanen J, Palva A, Vos WM, Keersmaecker SC, Vanderleyden J (2012) Functional analysis of Lactobacillus rhamnosus GG pili in relation to adhesion and immunomodulatory interactions with intestinal epithelial cells. Appl Environ Microbiol 78(1):185–193PubMedCentralPubMedGoogle Scholar
  192. 192.
    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 Fact 10(Suppl 1):S16PubMedCentralPubMedGoogle Scholar
  193. 193.
    Avall-Jaaskelainen S, Palva A (2005) Lactobacillus surface layers and their applications. FEMS Microbiol Rev 29(3):511–529PubMedGoogle Scholar
  194. 194.
    Schneitz C, Nuotio L, Lounatma K (1993) Adhesion of Lactobacillus acidophilus to avian intestinal epithelial cells mediated by the crystalline bacterial cell surface layer (S-layer). J Appl Bact 74(3):290–294Google Scholar
  195. 195.
    Toba T, Virkola R, Westerlund B, Bjorkman Y, Sillanpaa J, Vartio T, Kalkkinen N, Korhonen TK (1995) A Collagen-Binding S-Layer Protein in Lactobacillus crispatus. Appl Environ Microbiol 61(7):2467–2471PubMedCentralPubMedGoogle Scholar
  196. 196.
    Konstantinov SR, Smidt H, de Vos WM, Bruijns SC, Singh SK, Valence F, Molle D, Lortal S, Altermann E, Klaenhammer TR, van Kooyk Y (2008) S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. Proc Natl Acad Sci USA 105(49):19474–19479PubMedGoogle Scholar
  197. 197.
    Johnson-Henry KC, Hagen KE, Gordonpour M, Tompkins TA, Sherman PM (2007) Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157:h7 adhesion to epithelial cells. Cell Microbiol 9(2):356–367PubMedGoogle Scholar
  198. 198.
    Taverniti VSM, Minuzzo M, Arioli S, De Noni I, Scabiosi C, Cordova ZM, Junttila I, Hämäläinen S, Turpeinen H, Mora D, Karp M, Pesu M, Guglielmetti S (2013) S-Layer Protein Mediates the Stimulatory Effect of Lactobacillus helveticus MIMLh5 on Innate Immunity. Appl Environ Microbiol 79(4):1221–1231PubMedCentralPubMedGoogle Scholar
  199. 199.
    O’Callaghan J, Butto LF, MacSharry J, Nally K, O’Toole PW (2012) Influence of adhesion and bacteriocin production by Lactobacillus salivarius on the intestinal epithelial cell transcriptional response. Appl Environ Microbiol 78(15):5196–5203PubMedCentralPubMedGoogle Scholar
  200. 200.
    Murphy EF, Cotter PD, Hogan A, O’Sullivan O, Joyce A, Fouhy F, Clarke SF, Marques TM, O’Toole PW, Stanton C, Quigley EM, Daly C, Ross PR, O’Doherty RM, Shanahan F (2012) Divergent metabolic outcomes arising from targeted manipulation of the gut microbiota in diet-induced obesity. Gut 62:220–226Google Scholar
  201. 201.
    Riboulet-Bisson E, Sturme MH, Jeffery IB, O’Donnell MM, Neville BA, Forde BM, Claesson MJ, Harris H, Gardiner GE, Casey PG, Lawlor PG, O’Toole PW, Ross RP (2012) Effect of Lactobacillus salivarius bacteriocin Abp118 on the mouse and pig intestinal microbiota. PLoS One 7(2):e31113PubMedCentralPubMedGoogle Scholar
  202. 202.
    Meijerink M, van Hemert S, Taverne N, Wels M, de Vos P, Bron PA, Savelkoul HF, van Bilsen J, Kleerebezem M, Wells JM (2010) Identification of genetic loci in Lactobacillus plantarum that modulate the immune response of dendritic cells using comparative genome hybridization. PLoS One 5(5):e10632PubMedCentralPubMedGoogle Scholar
  203. 203.
    Walsh MC, Gardiner GE, Hart OM, Lawlor PG, Daly M, Lynch B, Richert BT, Radcliffe S, Giblin L, Hill C, Fitzgerald GF, Stanton C, Ross P (2008) Predominance of a bacteriocin-producing Lactobacillus salivarius component of a five-strain probiotic in the porcine ileum and effects on host immune phenotype. FEMS Microbiol Ecol 64(2):317–327PubMedGoogle Scholar
  204. 204.
    Marco ML, Bongers RS, de Vos WM, Kleerebezem M (2007) Spatial and temporal expression of Lactobacillus plantarum genes in the gastrointestinal tracts of mice. Appl Environ Microbiol 73(1):124–132PubMedCentralPubMedGoogle Scholar
  205. 205.
    Miyauchi E, O’Callaghan J, Butto LF, Hurley G, Melgar S, Tanabe S, Shanahan F, Nally K, O’Toole PW (2012) Mechanism of protection of transepithelial barrier function by Lactobacillus salivarius: strain dependence and attenuation by bacteriocin production. Am J Physiol Gastrointest Liver Physiol 303(9):G1029–G1041PubMedGoogle Scholar
  206. 206.
    van Pijkeren JP, Canchaya C, Ryan KA, Li Y, Claesson MJ, Sheil B, Steidler L, O’Mahony L, Fitzgerald GF, van Sinderen D, O’Toole PW (2006) Comparative and functional analysis of sortase-dependent proteins in the predicted secretome of Lactobacillus salivarius UCC118. Appl Environ Microbiol 72(6):4143–4153PubMedCentralPubMedGoogle Scholar
  207. 207.
    Munoz-Provencio D, Rodriguez-Diaz J, Collado MC, Langella P, Bermudez-Humaran LG, Monedero V (2012) Functional analysis of the Lactobacillus casei BL23 sortases. Appl Environ Microbiol 78(24):8684–8693Google Scholar
  208. 208.
    Boekhorst J, de Been MW, Kleerebezem M, Siezen RJ (2005) Genome-wide detection and analysis of cell wall-bound proteins with LPxTG-like sorting motifs. J Bacteriol 187(14):4928–4934PubMedCentralPubMedGoogle Scholar
  209. 209.
    Boekhorst J, Helmer Q, Kleerebezem M, Siezen RJ (2006) Comparative analysis of proteins with a mucus-binding domain found exclusively in lactic acid bacteria. Microbiology 152(Pt 1):273–280PubMedGoogle Scholar
  210. 210.
    Juge N, Muroyama A, Hiasa M, Omote H, Moriyama Y (2009) Vesicular inhibitory amino acid transporter is a Cl-/gamma-aminobutyrate Co-transporter. J Biol Chem 284(50):35073–35078PubMedGoogle Scholar
  211. 211.
    Troost FJ, van Baarlen P, Lindsey P, Kodde A, de Vos WM, Kleerebezem M, Brummer RJ (2008) Identification of the transcriptional response of human intestinal mucosa to Lactobacillus plantarum WCFS1 in vivo. BMC Genomics 9:374PubMedCentralPubMedGoogle Scholar
  212. 212.
    van Baarlen P, Troost FJ, van Hemert S, van der Meer C, de Vos WM, de Groot PJ, Hooiveld GJ, Brummer RJ, Kleerebezem M (2009) Differential NF-kappaB pathways induction by Lactobacillus plantarum in the duodenum of healthy humans correlating with immune tolerance. Proc Natl Acad Sci USA 106(7):2371–2376PubMedGoogle Scholar
  213. 213.
    Wang M, Ahrne S, Jeppsson B, Molin G (2005) Comparison of bacterial diversity along the human intestinal tract by direct cloning and sequencing of 16S rRNA genes. FEMS Microbiol Ecol 54(2):219–231PubMedGoogle Scholar
  214. 214.
    Sonnenburg JL, Xu J, Leip DD, Chen CH, Westover BP, Weatherford J, Buhler JD, Gordon JI (2005) Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307(5717):1955–1959PubMedGoogle Scholar
  215. 215.
    Tannock GW, Wilson CM, Loach D, Cook GM, Eason J, O’Toole PW, Holtrop G, Lawley B (2012) Resource partitioning in relation to cohabitation of Lactobacillus species in the mouse forestomach. ISME J 6(5):927–938PubMedGoogle Scholar
  216. 216.
    Paton AW, Morona R, Paton JC (2006) Designer probiotics for prevention of enteric infections. Nat Rev Microbiol 4(3):193–200PubMedGoogle Scholar
  217. 217.
    Sleator RD (2010) Probiotics—a viable therapeutic alternative for enteric infections especially in the developing world. Discov Med 10(51):119–124PubMedGoogle Scholar
  218. 218.
    Chang TL, Chang CH, Simpson DA, Xu Q, Martin PK, Lagenaur LA, Schoolnik GK, Ho DD, Hillier SL, Holodniy M, Lewicki JA, Lee PP (2003) Inhibition of HIV infectivity by a natural human isolate of Lactobacillus jensenii engineered to express functional two-domain CD4. Proc Natl Acad Sci USA 100(20):11672–11677PubMedGoogle Scholar

Copyright information

© Springer Basel 2013

Authors and Affiliations

  • Francesca Turroni
    • 1
  • Marco Ventura
    • 2
  • Ludovica F. Buttó
    • 1
  • Sabrina Duranti
    • 2
  • Paul W. O’Toole
    • 1
  • Mary O’Connell Motherway
    • 1
  • Douwe van Sinderen
    • 1
  1. 1.Alimentary Pharmabiotic Centre, Department of Microbiology Biosciences InstituteUniversity College Cork, National University of IrelandCorkIreland
  2. 2.Laboratory of Probiogenomics, Department of Genetics, Biology of Microorganisms, Anthropology and EvolutionUniversity of ParmaParmaItaly

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