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Beneficial Modulation of the Gut Microbiome: Probiotics and Prebiotics

  • M. Andrea Azcarate-PerilEmail author
Chapter

Abstract

The gut microbiota plays a critical role in the overall health of its host. Benefits derived from bacterial members of the gut microbiota can influence host growth, immune response, pathogen colonization, and intestinal physiology. Use of probiotics, prebiotics, and synbiotics are emerging as effective mechanisms to selectively modulate composition and function of the gut microbiota. This chapter introduces the concept of probiotics and prebiotics from a historic perspective, and attempts to answer the fundamental questions of the impact of probiotics and prebiotics on microbiome composition in health versus disease states, colonization of the human gut by probiotics (is it necessary?), and how the food or product matrix impact probiotic delivery and effect. The conclusion of this chapter focuses on the next generation of probiotics: novel species and bacterial consortia.

Keywords

Probiotics Prebiotics Microbiota modulation Bifidobacterium Lactobacillus Next generation probiotics 

References

  1. Alander, M., Satokari, R., Korpela, R., Saxelin, M., Vilpponen-Salmela, T., Mattila-Sandholm, T., & von Wright, A. (1999). Persistence of colonization of human colonic mucosa by a probiotic strain, Lactobacillus rhamnosus GG, after oral consumption. Applied and Environmental Microbiology, 65(1), 351–354.PubMedPubMedCentralGoogle Scholar
  2. Allen, S. J., Martinez, E. G., Gregorio, G. V., & Dans, L. F. (2010). Probiotics for treating acute infectious diarrhoea. Cochrane Database of Systematic Reviews, 11, CD003048.Google Scholar
  3. Ananta, E., Birkeland, S.-E., Corcoran, B. M., Fitzgerald, G., Hinz, S., Klijn, A., Matto, J., Mercenier, A., Nilsson, U., Saarela, C., Stanton, C., Stahl, U., Suomalainen, T., Vincken, J.-P., Virkajarvi, I., Voragen, F., Wesenfeld, J., Wouters, R., & Knorr, D. (2004). Processing effects on the nutritional advancement of probiotics and prebiotics. Microbial Ecology in Health and Disease, 16(2–3), 113–124.CrossRefGoogle Scholar
  4. Atlas, R. M. (1999). Probiotics—Snake oil for the new millennium? Environmental Microbiology, 1(5), 377–382.PubMedCrossRefGoogle Scholar
  5. Azcarate Peril, M. A., Savaiano, D. A., Ritter, A. J., & Klaenhammer, T. (2013). Microbiome alterations of lactose intolerant individuals in response to dietary intervention with galacto-oligosaccharides may help negate symptoms of lactose intolerance. Gastroenterology, 144(5), S-893.CrossRefGoogle Scholar
  6. Azcarate-Peril, M. A., Altermann, E., Hoover-Fitzula, R. L., Cano, R. J., & Klaenhammer, T. R. (2004). Identification and inactivation of genetic loci involved with Lactobacillus acidophilus acid tolerance. Applied and Environmental Microbiology, 70(9), 5315–5322.PubMedPubMedCentralCrossRefGoogle Scholar
  7. Azcarate-Peril, M. A., Tallon, R., & Klaenhammer, T. R. (2009). Temporal gene expression and probiotic attributes of Lactobacillus acidophilus during growth in milk. Journal of Dairy Science, 92(3), 870–886.PubMedCrossRefGoogle Scholar
  8. Azcarate-Peril, M. A., Sikes, M., & Bruno-Barcena, J. M. (2011). The intestinal microbiota, gastrointestinal environment and colorectal cancer: A putative role for probiotics in prevention of colorectal cancer? American Journal of Physiology. Gastrointestinal and Liver Physiology, 301(3), G401–G424.PubMedPubMedCentralCrossRefGoogle Scholar
  9. Azcarate-Peril, M. A., Ritter, A. J., Savaiano, D., Monteagudo-Mera, A., Anderson, C., Magness, S. T., & Klaenhammer, T. R. (2017). Impact of short-chain galactooligosaccharides on the gut microbiome of lactose-intolerant individuals. Proceedings of the National Academy of Sciences of the United States of America, 114(3), E367–E375.PubMedPubMedCentralCrossRefGoogle Scholar
  10. Baharav, E., Mor, F., Halpern, M., & Weinberger, A. (2004). Lactobacillus GG bacteria ameliorate arthritis in Lewis rats. The Journal of Nutrition, 134(8), 1964–1969.PubMedCrossRefGoogle Scholar
  11. Bazanella, M., Maier, T. V., Clavel, T., Lagkouvardos, I., Lucio, M., Maldonado-Gomez, M. X., Autran, C., Walter, J., Bode, L., Schmitt-Kopplin, P., & Haller, D. (2017). Randomized controlled trial on the impact of early-life intervention with bifidobacteria on the healthy infant fecal microbiota and metabolome. The American Journal of Clinical Nutrition, 106(5), 1274–1286.PubMedGoogle Scholar
  12. Bezkorovainy, A. (2001). Probiotics: Determinants of survival and growth in the gut. The American Journal of Clinical Nutrition, 73(2 Suppl), 399S–405S.PubMedCrossRefGoogle Scholar
  13. Bindels, L. B., Delzenne, N. M., Cani, P. D., & Walter, J. (2015). Towards a more comprehensive concept for prebiotics. Nat Rev Gastroenterol Hepatol, 12(5), 303–310.PubMedCrossRefGoogle Scholar
  14. Bruno-Barcena, J. M., & Azcarate-Peril, M. A. (2015). Galacto-oligosaccharides and colorectal cancer: Feeding our intestinal probiome. Journal of Functional Foods, 12, 92–108.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bruno-Barcena, J. M., Azcarate-Peril, M. A., & Hassan, H. M. (2010). Role of antioxidant enzymes in bacterial resistance to organic acids. Applied and Environmental Microbiology, 76(9), 2747–2753.PubMedPubMedCentralCrossRefGoogle Scholar
  16. Bruzzese, E., Volpicelli, M., Squeglia, V., Bruzzese, D., Salvini, F., Bisceglia, M., Lionetti, P., Cinquetti, M., Iacono, G., Amarri, S., & Guarino, A. (2009). A formula containing galacto- and fructo-oligosaccharides prevents intestinal and extra-intestinal infections: An observational study. Clinical Nutrition, 28(2), 156–161.PubMedCrossRefGoogle Scholar
  17. Buck, B. L., Azcarate-Peril, M. A., Altermann, E., & Klaenhammer, T. Methods and compositions to modulate adhesion and stress tolerance in bacteria.Google Patents; 2006.Google Scholar
  18. Campbell, A. K., Waud, J. P., & Matthews, S. B. (2005). The molecular basis of lactose intolerance. Science Progress, 88(Pt 3), 157–202.PubMedCrossRefGoogle Scholar
  19. Cani, P. D., & de Vos, W. M. (2017). Next-generation beneficial microbes: The case of Akkermansia muciniphila. Frontiers in Microbiology, 8, 1765.PubMedPubMedCentralCrossRefGoogle Scholar
  20. Collins, M. D., & Gibson, G. R. (1999). Probiotics, prebiotics, and synbiotics: Approaches for modulating the microbial ecology of the gut. The American Journal of Clinical Nutrition, 69(5), 1052S–1057S.PubMedCrossRefGoogle Scholar
  21. Costeloe, K., Bowler, U., Brocklehurst, P., Hardy, P., Heal, P., Juszczak, E., King, A., Panton, N., Stacey, F., Whiley, A., Wilks, M., & Millar, M. R. (2016). A randomised controlled trial of the probiotic Bifidobacterium breve BBG-001 in preterm babies to prevent sepsis, necrotising enterocolitis and death: The Probiotics in Preterm infantS (PiPS) trial. Health Technology Assessment, 20(66), 1–194.PubMedCrossRefGoogle Scholar
  22. Crovesy, L., Ostrowski, M., Ferreira, D., Rosado, E. L., & Soares-Mota, M. (2017). Effect of Lactobacillus on body weight and body fat in overweight subjects: A systematic review of randomized controlled clinical trials. International Journal of Obesity, 41(11), 1607–1614.PubMedCrossRefGoogle Scholar
  23. Dalli, S. S., Uprety, K., & Rakshit, S. K. (2017). Industrial production of active probiotics for food enrichment. In Y. H. Roos & Y. D. Livney (Eds.), Engineering foods for bioactives stability and delivery. New York: Springer.Google Scholar
  24. Davis, L. M., Martinez, I., Walter, J., Goin, C., & Hutkins, R. W. (2011). Barcoded pyrosequencing reveals that consumption of galactooligosaccharides results in a highly specific bifidogenic response in humans. PLoS One, 6(9), e25200.PubMedPubMedCentralCrossRefGoogle Scholar
  25. Derrien, M., Vaughan, E. E., Plugge, C. M., & de Vos, W. M. (2004). Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. International Journal of Systematic and Evolutionary Microbiology, 54(Pt 5), 1469–1476.PubMedCrossRefGoogle Scholar
  26. Desmond, C., Fitzgerald, G. F., Stanton, C., & Ross, R. P. (2004). Improved stress tolerance of GroESL-overproducing Lactococcus lactis and probiotic Lactobacillus paracasei NFBC 338. Applied and Environmental Microbiology, 70(10), 5929–5936.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Forssten, S. D., Korczynska, M. Z., Zwijsen, R. M., Noordman, W. H., Madetoja, M., & Ouwehand, A. C. (2013). Changes in satiety hormone concentrations and feed intake in rats in response to lactic acid bacteria. Appetite, 71, 16–21.PubMedCrossRefGoogle Scholar
  28. Frese, S. A., Hutton, A. A., Contreras, L. N., Shaw, C. A., Palumbo, M. C., Casaburi, G., Xu, G., Davis, J. C. C., Lebrilla, C. B., Henrick, B. M., Freeman, S. L., Barile, D., German, J. B., Mills, D. A., Smilowitz, J. T., & Underwood, M. A. (2017). Persistence of supplemented Bifidobacterium longum subsp. infantis EVC001 in breastfed infants. mSphere, 2(6), e00501–e00517.PubMedPubMedCentralCrossRefGoogle Scholar
  29. Fujita, K., Oura, F., Nagamine, N., Katayama, T., Hiratake, J., Sakata, K., Kumagai, H., & Yamamoto, K. (2005). Identification and molecular cloning of a novel glycoside hydrolase family of core 1 type O-glycan-specific endo-alpha-N-acetylgalactosaminidase from Bifidobacterium longum. The Journal of Biological Chemistry, 280(45), 37415–37422.PubMedCrossRefGoogle Scholar
  30. Ganji-Arjenaki, M., & Rafieian-Kopaei, M. (2018). Probiotics are a good choice in remission of inflammatory bowel diseases: A meta analysis and systematic review. Journal of Cellular Physiology, 233(3), 2091–2103.PubMedCrossRefGoogle Scholar
  31. Gibson, G. R., & Roberfroid, M. B. (1995). Dietary modulation of the human colonic microbiota—Introducing the concept of prebiotics. Journal of Nutrition, 125(6), 1401–1412.PubMedCrossRefGoogle Scholar
  32. Goldenberg, J. Z., Lytvyn, L., Steurich, J., Parkin, P., Mahant, S., & Johnston, B. C. (2015). Probiotics for the prevention of pediatric antibiotic-associated diarrhea. Cochrane Database of Systematic Reviews, 12, CD004827.Google Scholar
  33. Goldin, B., & Gorbach, S. L. (1977). Alterations in fecal microflora enzymes related to diet, age, lactobacillus supplements, and dimethylhydrazine. Cancer, 40(5 Suppl), 2421–2426.PubMedCrossRefGoogle Scholar
  34. Govender, M., Choonara, Y. E., Kumar, P., du Toit, L. C., van Vuuren, S., & Pillay, V. (2014). A review of the advancements in probiotic delivery: Conventional vs. non-conventional formulations for intestinal flora supplementation. AAPS PharmSciTech, 15(1), 29–43.PubMedCrossRefGoogle Scholar
  35. Hamilton-Miller, J. M., Gibson, G. R., & Bruck, W. (2003). Some insights into the derivation and early uses of the word ‘probiotic’. The British Journal of Nutrition, 90(4), 845.PubMedCrossRefGoogle Scholar
  36. Hill, C., Guarner, F., Reid, G., Gibson, G. R., Merenstein, D. J., Pot, B., Morelli, L., Canani, R. B., Flint, H. J., Salminen, S., Calder, P. C., & Sanders, M. E. (2014). Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviews. Gastroenterology & Hepatology, 11(8), 506–514.CrossRefGoogle Scholar
  37. Holscher, H. D., Faust, K. L., Czerkies, L. A., Litov, R., Ziegler, E. E., Lessin, H., Hatch, T., Sun, S., & Tappenden, K. A. (2012). Effects of prebiotic-containing infant formula on gastrointestinal tolerance and fecal microbiota in a randomized controlled trial. JPEN Journal of Parenteral and Enteral Nutrition, 36(1 Suppl), 95S–105S.PubMedCrossRefGoogle Scholar
  38. Iqbal, S., Nguyen, T. H., Nguyen, T. T., Maischberger, T., & Haltrich, D. (2010). beta-Galactosidase from Lactobacillus plantarum WCFS1: Biochemical characterization and formation of prebiotic galacto-oligosaccharides. Carbohydrate Research, 345(10), 1408–1416.PubMedCrossRefGoogle Scholar
  39. Iqbal, S., Nguyen, T. H., Nguyen, H. A., Maischberger, T., Kittl, R., & Haltrich, D. (2011). Characterization of a heterodimeric GH2 beta-galactosidase from Lactobacillus sakei Lb790 and formation of prebiotic galacto-oligosaccharides. Journal of Agricultural and Food Chemistry, 59(8), 3803–3811.PubMedCrossRefGoogle Scholar
  40. Isolauri, E., Juntunen, M., Rautanen, T., Sillanaukee, P., & Koivula, T. (1991). A human Lactobacillus strain (Lactobacillus casei sp strain GG) promotes recovery from acute diarrhea in children. Pediatrics, 88(1), 90–97.PubMedGoogle Scholar
  41. Jabr, F. Do probiotics really work? Scientific American. 2017.Google Scholar
  42. 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), 1076–1079.PubMedCrossRefGoogle Scholar
  43. Karczewski, J., Troost, F. J., Konings, I., Dekker, J., Kleerebezem, M., Brummer, R. J., & Wells, J. M. (2010). Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier. American Journal of Physiology. Gastrointestinal and Liver Physiology, 298(6), G851–G859.PubMedCrossRefGoogle Scholar
  44. Kekkonen, R. A., Lummela, N., Karjalainen, H., Latvala, S., Tynkkynen, S., Jarvenpaa, S., Kautiainen, H., Julkunen, I., Vapaatalo, H., & Korpela, R. (2008). Probiotic intervention has strain-specific anti-inflammatory effects in healthy adults. World Journal of Gastroenterology, 14(13), 2029–2036.PubMedPubMedCentralCrossRefGoogle Scholar
  45. Lee, B., Yin, X., Griffey, S. M., & Marco, M. L. (2015). Attenuation of colitis by Lactobacillus casei BL23 is dependent on the dairy delivery matrix. Applied and Environmental Microbiology, 81(18), 6425–6435.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Li, J., Lin, S., Vanhoutte, P. M., Woo, C. W., & Xu, A. (2016). Akkermansia muciniphila protects against atherosclerosis by preventing metabolic endotoxemia-induced inflammation in Apoe−/− mice. Circulation, 133(24), 2434–2446.PubMedCrossRefGoogle Scholar
  47. Lilly, D. M., & Stillwell, R. H. (1965). Probiotics: Growth-promoting factors produced by microorganisms. Science, 147(3659), 747–748.PubMedCrossRefGoogle Scholar
  48. Liu, S., Hu, P., Du, X., Zhou, T., & Pei, X. (2013). Lactobacillus rhamnosus GG supplementation for preventing respiratory infections in children: A meta-analysis of randomized, placebo-controlled trials. Indian Pediatrics, 50(4), 377–381.PubMedCrossRefGoogle Scholar
  49. LoCascio, R. G., Desai, P., Sela, D. A., Weimer, B., & Mills, D. A. (2010). Broad conservation of milk utilization genes in Bifidobacterium longum subsp. infantis as revealed by comparative genomic hybridization. Applied and Environmental Microbiology, 76(22), 7373–7381.PubMedPubMedCentralCrossRefGoogle Scholar
  50. Maischberger, T., Leitner, E., Nitisinprasert, S., Juajun, O., Yamabhai, M., Nguyen, T. H., & Haltrich, D. (2010). Beta-galactosidase from Lactobacillus pentosus: Purification, characterization and formation of galacto-oligosaccharides. Biotechnology Journal, 5(8), 838–847.PubMedCrossRefGoogle Scholar
  51. Metchnikoff, I. I., & Mitchell, P. (2004). Prolongation of life: Optimistic studies. New York: Springer.Google Scholar
  52. Monteagudo-Mera, A., Arthur, J. C., Jobin, C., Keku, T. O., Bruno Barcena, J. M., & Azcarate-Peril, M. A. (2016). High purity galacto-oligosaccharides enhance specific Bifidobacterium species and their metabolic activity in the mouse gut microbiome. Beneficial Microbes, 3, 1–18.Google Scholar
  53. Nguyen, T. H., Splechtna, B., Steinbock, M., Kneifel, W., Lettner, H. P., Kulbe, K. D., & Haltrich, D. (2006). Purification and characterization of two novel beta-galactosidases from Lactobacillus reuteri. Journal of Agricultural and Food Chemistry, 54(14), 4989–4998.PubMedCrossRefGoogle Scholar
  54. Nguyen, T. H., Splechtna, B., Krasteva, S., Kneifel, W., Kulbe, K. D., Divne, C., & Haltrich, D. (2007). Characterization and molecular cloning of a heterodimeric beta-galactosidase from the probiotic strain Lactobacillus acidophilus R22. FEMS Microbiology Letters, 269(1), 136–144.PubMedCrossRefGoogle Scholar
  55. Nguyen, T. T., Nguyen, H. A., Arreola, S. L., Mlynek, G., Djinovic-Carugo, K., Mathiesen, G., Nguyen, T. H., & Haltrich, D. (2012). Homodimeric beta-galactosidase from Lactobacillus delbrueckii subsp. bulgaricus DSM 20081: Expression in Lactobacillus plantarum and biochemical characterization. Journal of Agricultural and Food Chemistry, 60(7), 1713–1721.PubMedPubMedCentralCrossRefGoogle Scholar
  56. Nishimoto, M., & Kitaoka, M. (2007). Identification of N-acetylhexosamine 1-kinase in the complete lacto-N-biose I/galacto-N-biose metabolic pathway in Bifidobacterium longum. Applied and Environmental Microbiology, 73(20), 6444–6449.PubMedPubMedCentralCrossRefGoogle Scholar
  57. O’Toole, P. W., Marchesi, J. R., & Hill, C. (2017). Next-generation probiotics: The spectrum from probiotics to live biotherapeutics. Nature Microbiology, 2, 17057.PubMedCrossRefGoogle Scholar
  58. Oozeer, R., Leplingard, A., Mater, D. D., Mogenet, A., Michelin, R., Seksek, I., Marteau, P., Dore, J., Bresson, J. L., & Corthier, G. (2006). Survival of Lactobacillus casei in the human digestive tract after consumption of fermented milk. Applied and Environmental Microbiology, 72(8), 5615–5617.PubMedPubMedCentralCrossRefGoogle Scholar
  59. Petrof, E. O., Gloor, G. B., Vanner, S. J., Weese, S. J., Carter, D., Daigneault, M. C., Brown, E. M., Schroeter, K., & Allen-Vercoe, E. (2013). Stool substitute transplant therapy for the eradication of Clostridium difficile infection: ‘RePOOPulating’ the gut. Microbiome, 1(1), 3.PubMedPubMedCentralCrossRefGoogle Scholar
  60. Pfeiler, E. A., Azcarate-Peril, M. A., & Klaenhammer, T. R. (2006). Characterization of a two-component regulatory system implicated in the bile tolerance of Lactobacillus acidophilus NCFM. Journal of Animal Science, 84, 181–181.Google Scholar
  61. Pfeiler, E. A., Azcarate-Peril, M. A., & Klaenhammer, T. R. (2007). Characterization of a novel bile-inducible operon encoding a two-component regulatory system in Lactobacillus acidophilus. Journal of Bacteriology, 189(13), 4624–4634.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 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. International Journal of Food Microbiology, 108(2), 276–280.PubMedCrossRefGoogle Scholar
  63. Plovier, H., Everard, A., Druart, C., Depommier, C., Van Hul, M., Geurts, L., Chilloux, J., Ottman, N., Duparc, T., Lichtenstein, L., Myridakis, A., Delzenne, N. M., Klievink, J., Bhattacharjee, A., van der Ark, K. C., Aalvink, S., Martinez, L. O., Dumas, M. E., Maiter, D., Loumaye, A., Hermans, M. P., Thissen, J. P., Belzer, C., de Vos, W. M., & Cani, P. D. (2017). A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nature Medicine, 23(1), 107–113.PubMedCrossRefGoogle Scholar
  64. Puebla-Barragan, S., & Reid, G. (2019). Forty-five-year evolution of probiotic therapy. Microbial Cell, 6(4), 184–196.PubMedPubMedCentralCrossRefGoogle Scholar
  65. Reid, G., Sanders, M. E., Gaskins, H. R., Gibson, G. R., Mercenier, A., Rastall, R., Roberfroid, M., Rowland, I., Cherbut, C., & Klaenhammer, T. R. (2003). New scientific paradigms for probiotics and prebiotics. Journal of Clinical Gastroenterology, 37(2), 105–118.PubMedCrossRefGoogle Scholar
  66. Rettger, L. F., & Cheplin, H. A. (1921). Treatise on the transformation of the intestinal flora: With special reference to the implantation of Bacillus acidophilus (Vol. 13). Yale University Press.Google Scholar
  67. Robert, S., & Steidler, L. (2014). Recombinant Lactococcus lactis can make the difference in antigen-specific immune tolerance induction, the Type 1 Diabetes case. Microbial Cell Factories, 13(Suppl 1), S11.PubMedPubMedCentralCrossRefGoogle Scholar
  68. Salvini, F., Riva, E., Salvatici, E., Boehm, G., Jelinek, J., Banderali, G., & Giovannini, M. (2011). A specific prebiotic mixture added to starting infant formula has long-lasting bifidogenic effects. The Journal of Nutrition, 141(7), 1335–1339.PubMedPubMedCentralCrossRefGoogle Scholar
  69. Sanders, M. E., & Marco, M. L. (2010). Food formats for effective delivery of probiotics. Annual Review of Food Science and Technology, 1, 65–85.PubMedCrossRefGoogle Scholar
  70. Scalabrin, D. M., Mitmesser, S. H., Welling, G. W., Harris, C. L., Marunycz, J. D., Walker, D. C., Bos, N. A., Tolkko, S., Salminen, S., & Vanderhoof, J. A. (2012). New prebiotic blend of polydextrose and galacto-oligosaccharides has a bifidogenic effect in young infants. Journal of Pediatric Gastroenterology and Nutrition, 54(3), 343–352.PubMedCrossRefGoogle Scholar
  71. Seo, M., Heo, J., Yoon, J., Kim, S. Y., Kang, Y. M., Yu, J., Cho, S., & Kim, H. (2017). Methanobrevibacter attenuation via probiotic intervention reduces flatulence in adult human: A non-randomised paired-design clinical trial of efficacy. PLoS One, 12(9), e0184547.PubMedPubMedCentralCrossRefGoogle Scholar
  72. Seregin, S. S., Golovchenko, N., Schaf, B., Chen, J., Eaton, K. A., & Chen, G. Y. (2017a). NLRP6 function in inflammatory monocytes reduces susceptibility to chemically induced intestinal injury. Mucosal Immunology, 10(2), 434–445.PubMedCrossRefGoogle Scholar
  73. Seregin, S. S., Golovchenko, N., Schaf, B., Chen, J., Pudlo, N. A., Mitchell, J., Baxter, N. T., Zhao, L., Schloss, P. D., Martens, E. C., Eaton, K. A., & Chen, G. Y. (2017b). NLRP6 protects Il10(-/-) mice from colitis by limiting colonization of Akkermansia muciniphila. Cell Reports, 19(4), 733–745.PubMedPubMedCentralCrossRefGoogle Scholar
  74. Sheehan, V. M., Sleator, R. D., Hill, C., & Fitzgerald, G. F. (2007). Improving gastric transit, gastrointestinal persistence and therapeutic efficacy of the probiotic strain Bifidobacterium breve UCC2003. Microbiology, 153(Pt 10), 3563–3571.PubMedCrossRefGoogle Scholar
  75. Simon, M. C., Strassburger, K., Nowotny, B., Kolb, H., Nowotny, P., Burkart, V., Zivehe, F., Hwang, J. H., Stehle, P., Pacini, G., Hartmann, B., Holst, J. J., MacKenzie, C., Bindels, L. B., Martinez, I., Walter, J., Henrich, B., Schloot, N. C., & Roden, M. (2015). Intake of Lactobacillus reuteri improves incretin and insulin secretion in glucose-tolerant humans: A proof of concept. Diabetes Care, 38(10), 1827–1834.PubMedCrossRefGoogle Scholar
  76. Sipailiene, A., & Petraityte, S. (2017). Encapsulation of probiotics: Proper selection of the probiotic strain and the influence of encapsulation technology and materials on the viability of encapsulated microorganisms. Probiotics Antimicrob Proteins, 10(1), 1–10.CrossRefGoogle Scholar
  77. Staudacher, H. M., Lomer, M. C. E., Farquharson, F. M., Louis, P., Fava, F., Franciosi, E., Scholz, M., Tuohy, K. M., Lindsay, J. O., Irving, P. M., & Whelan, K. (2017). A diet low in FODMAPs reduces symptoms in patients with irritable bowel syndrome and a probiotic restores bifidobacterium species: A randomized controlled trial. Gastroenterology, 153(4), 936–947.PubMedCrossRefGoogle Scholar
  78. Takahashi, S., Anzawa, D., Takami, K., Ishizuka, A., Mawatari, T., Kamikado, K., Sugimura, H., & Nishijima, T. (2016). Effect of Bifidobacterium animalis ssp. lactis GCL2505 on visceral fat accumulation in healthy Japanese adults: A randomized controlled trial. Bioscience of Microbiota, Food and Health, 35(4), 163–171.PubMedPubMedCentralCrossRefGoogle Scholar
  79. Tannock, G. W., Lawley, B., Munro, K., Gowri Pathmanathan, S., Zhou, S. J., Makrides, M., Gibson, R. A., Sullivan, T., Prosser, C. G., Lowry, D., & Hodgkinson, A. J. (2013). Comparison of the compositions of the stool microbiotas of infants fed goat milk formula, cow milk-based formula, or breast milk. Applied and Environmental Microbiology, 79(9), 3040–3048.PubMedPubMedCentralCrossRefGoogle Scholar
  80. Thompson, A. L., Monteagudo-Mera, A., Cadenas, M. B., Lampl, M. L., & Azcarate-Peril, M. A. (2015). Milk- and solid-feeding practices and daycare attendance are associated with differences in bacterial diversity, predominant communities, and metabolic and immune function of the infant gut microbiome. Frontiers in Cellular and Infection Microbiology, 5, 3.PubMedPubMedCentralCrossRefGoogle Scholar
  81. Toscano, M., De Grandi, R., Miniello, V. L., Mattina, R., & Drago, L. (2017a). Ability of Lactobacillus kefiri LKF01 (DSM32079) to colonize the intestinal environment and modify the gut microbiota composition of healthy individuals. Digestive and Liver Disease, 49(3), 261–267.PubMedCrossRefGoogle Scholar
  82. Toscano, M., De Grandi, R., Stronati, L., De Vecchi, E., & Drago, L. (2017b). Effect of Lactobacillus rhamnosus HN001 and Bifidobacterium longum BB536 on the healthy gut microbiota composition at phyla and species level: A preliminary study. World Journal of Gastroenterology, 23(15), 2696–2704.PubMedPubMedCentralCrossRefGoogle Scholar
  83. Tripathi, M. K., & Giri, S. K. (2014). Probiotic functional foods: Survival of probiotics during processing and storage. Journal of Functional Foods, 9, 225–241.CrossRefGoogle Scholar
  84. Ulsemer, P., Toutounian, K., Kressel, G., Goletz, C., Schmidt, J., Karsten, U., Hahn, A., & Goletz, S. (2016). Impact of oral consumption of heat-treated Bacteroides xylanisolvens DSM 23964 on the level of natural TFalpha-specific antibodies in human adults. Beneficial Microbes, 7(4), 485–500.PubMedCrossRefGoogle Scholar
  85. Urbanska, A. M., Bhathena, J., Martoni, C., & Prakash, S. (2009). Estimation of the potential antitumor activity of microencapsulated Lactobacillus acidophilus yogurt formulation in the attenuation of tumorigenesis in Apc(Min/+) mice. Digestive Diseases and Sciences, 54(2), 264–273.PubMedCrossRefGoogle Scholar
  86. Wada, J., Ando, T., Kiyohara, M., Ashida, H., Kitaoka, M., Yamaguchi, M., Kumagai, H., Katayama, T., & Yamamoto, K. (2008). Bifidobacterium bifidum lacto-N-biosidase, a critical enzyme for the degradation of human milk oligosaccharides with a type 1 structure. Applied and Environmental Microbiology, 74(13), 3996–4004.PubMedPubMedCentralCrossRefGoogle Scholar
  87. Watson, D., Sleator, R. D., Hill, C., & Gahan, C. G. (2008). Enhancing bile tolerance improves survival and persistence of Bifidobacterium and Lactococcus in the murine gastrointestinal tract. BMC Microbiology, 8, 176.PubMedPubMedCentralCrossRefGoogle Scholar
  88. Westfall, S., Lomis, N., Kahouli, I., Dia, S. Y., Singh, S. P., & Prakash, S. (2017). Microbiome, probiotics and neurodegenerative diseases: Deciphering the gut brain axis. Cellular and Molecular Life Sciences, 74(20), 3769–3787.PubMedCrossRefGoogle Scholar
  89. Yan, F., & Polk, D. B. (2002). Probiotic bacterium prevents cytokine-induced apoptosis in intestinal epithelial cells. The Journal of Biological Chemistry, 277(52), 50959–50965.PubMedPubMedCentralCrossRefGoogle Scholar
  90. Yan, F., Cao, H., Cover, T. L., Whitehead, R., Washington, M. K., & Polk, D. B. (2007). Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology, 132(2), 562–575.PubMedCrossRefGoogle Scholar
  91. Yan, F., Liu, L., Dempsey, P. J., Tsai, Y. H., Raines, E. W., Wilson, C. L., Cao, H., Cao, Z., Liu, L., & Polk, D. B. (2013). A Lactobacillus rhamnosus GG-derived soluble protein, p40, stimulates ligand release from intestinal epithelial cells to transactivate epidermal growth factor receptor. The Journal of Biological Chemistry, 288(42), 30742–30751.PubMedPubMedCentralCrossRefGoogle Scholar
  92. Yoshida, E., Sakurama, H., Kiyohara, M., Nakajima, M., Kitaoka, M., Ashida, H., Hirose, J., Katayama, T., Yamamoto, K., & Kumagai, H. (2012). Bifidobacterium longum subsp. infantis uses two different beta-galactosidases for selectively degrading type-1 and type-2 human milk oligosaccharides. Glycobiology, 22(3), 361–368.PubMedCrossRefGoogle Scholar
  93. Zimmermann, P., & Curtis, N. (2018). The influence of probiotics on vaccine responses—A systematic review. Vaccine, 36(2), 207–213.PubMedCrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Division of Gastroenterology and Hepatology, Department of MedicineUniversity of North Carolina at Chapel HillChapel HillUSA

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