Bifidobacterium longum subspecies infantis: Champion colonizer of the infant gut

Pediatric Research

Volumn 77, Issue , 2015, Pages 229-235

  Underwood, Mark A ^a,b   German, J Bruce ^b   Lebrilla, Carlito B ^b   Mills, David A ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BCG VACCINE; GLYCAN; OLIGOSACCHARIDE; POLIOMYELITIS VACCINE; PREBIOTIC AGENT; PROBIOTIC AGENT; TETANUS TOXOID;

ANTIINFLAMMATORY ACTIVITY; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BIFIDOBACTERIUM LONGUM; BREAST MILK; CELL MEMBRANE PERMEABILITY; COEVOLUTION; ENTEROBACTERIACEAE; FECES ANALYSIS; IMMUNE RESPONSE; INTESTINE CELL; INTESTINE FLORA; NECROTIZING ENTEROCOLITIS; PREMATURITY; REVIEW; TREATMENT RESPONSE; BIFIDOBACTERIUM; CHEMISTRY; EVOLUTION; GASTROINTESTINAL TRACT; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MICROBIOLOGY; MICROFLORA; NEWBORN; SPECIES DIFFERENCE;

BIFIDOBACTERIUM; BIOLOGICAL EVOLUTION; GASTROINTESTINAL TRACT; HUMANS; INFANT, NEWBORN; MICROBIOTA; MILK, HUMAN; OLIGOSACCHARIDES; SPECIES SPECIFICITY;

EID: 84920621534     PISSN: 00313998     EISSN: 15300447     Source Type: Journal    
DOI: 10.1038/pr.2014.156     Document Type: Review

References (83)

1. Moro E. Morphologische und biologische Untersuchung über die Darmbakterien des Säuglings [Morphological and biological study of the intestinal bacteria of infants]. Jahrb F Kinderh 1905;61:687-734.
2. Tao N, Wu S, Kim J, et al. Evolutionary glycomics: characterization of milk oligosaccharides in primates. J Proteome Res 2011;10:1548-57.
3. Ruhaak LR, Lebrilla CB. Analysis and role of oligosaccharides in milk. BMB Rep 2012;45:442-51.
4. Aldredge DL, Geronimo MR, Hua S, Nwosu CC, Lebrilla CB, Barile D. Annotation and structural elucidation of bovine milk oligosaccharides and determination of novel fucosylated structures. Glycobiology 2013;23: 664-76.
5. Totten SM, Zivkovic AM, Wu S, et al. Comprehensive profiles of human milk oligosaccharides yield highly sensitive and specific markers for determining secretor status in lactating mothers. J Proteome Res 2012;11:6124-33.
6. Sela DA, Mills DA. Nursing our microbiota: molecular linkages between bifidobacteria and milk oligosaccharides. Trends Microbiol 2010;18: 298-307.
7. Garrido D, Dallas DC, Mills DA. Consumption of human milk glycoconjugates by infant-associated bifidobacteria: mechanisms and implications. Microbiology 2013;159(Pt 4):649-64.
8. Yu ZT, Chen C, Newburg DS. Utilization of major fucosylated and sialylated human milk oligosaccharides by isolated human gut microbes. Glycobiology 2013;23:1281-92.
9. Marcobal A, Barboza M, Froehlich JW, et al. Consumption of human milk oligosaccharides by gut-related microbes. J Agric Food Chem 2010;58:5334-40.
10. Dominguez-Bello MG, Costello EK, Contreras M, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA 2010;107:11971-5.
11. Boesten R, Schuren F, Ben Amor K, Haarman M, Knol J, de Vos WM. Bifidobacterium population analysis in the infant gut by direct mapping of genomic hybridization patterns: potential for monitoring temporal development and effects of dietary regimens. Microb Biotechnol 2011;4:417-27.
12. Harmsen HJ, Wildeboer-Veloo AC, Raangs GC, et al. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J Pediatr Gastroenterol Nutr 2000;30:61-7.
13. Jost T, Lacroix C, Braegger CP, Chassard C. New insights in gut microbiota establishment in healthy breast fed neonates. PLoS One 2012;7:e44595.
14. Jost T, Lacroix C, Braegger CP, Rochat F, Chassard C. Vertical mother-neonate transfer of maternal gut bacteria via breastfeeding. Environ Microbiol [online], 2013 (doi:10.1111/1462-2920.12238).
15. Marcobal A, Sonnenburg JL. Human milk oligosaccharide consumption by intestinal microbiota. Clin Microbiol Infect 2012;18:Suppl 4:12-5.
16. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. Development of the human infant intestinal microbiota. PLoS Biol 2007;5:e177.
17. Underwood MA, Arriola J, Gerber CW, et al. Bifidobacterium longum subsp. infantis in experimental necrotizing enterocolitis: alterations in inflammation, innate immune response, and the microbiota. Pediatr Res 2014;76:326-33.
18. Sakata S, Tonooka T, Ishizeki S, et al. Culture-independent analysis of fecal microbiota in infants, with special reference to Bifidobacterium species. FEMS Microbiol Lett 2005;243:417-23.
19. Roger LC, Costabile A, Holland DT, Hoyles L, McCartney AL. Examination of faecal Bifidobacterium populations in breast- and formula-fed infants during the first 18 months of life. Microbiology 2010;156(Pt 11):3329-41.
20. Turroni F, Foroni E, Pizzetti P, et al. Exploring the diversity of the bifidobacterial population in the human intestinal tract. Appl Environ Microbiol 2009;75:1534-45.
21. Belkaid Y, Hand TW. Role of the microbiota in immunity and inflammation. Cell 2014;157:121-41.
22. Huda MN, Lewis ZT, Kalanetra KM, et al. Stool microbiota and vaccine responses of infants. Pediatrics 2014;134:e362-72.
23. Ward RE, Niñonuevo M, Mills DA, Lebrilla CB, German JB. In vitro fermentability of human milk oligosaccharides by several strains of bifidobacteria. Mol Nutr Food Res 2007;51:1398-405.
24. Locascio RG, Niñonuevo MR, Kronewitter SR, et al. A versatile and scalable strategy for glycoprofiling bifidobacterial consumption of human milk oligosaccharides. Microb Biotechnol 2009;2:333-42.
25. Sela DA, Chapman J, Adeuya A, et al. The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc Natl Acad Sci USA 2008;105:18964-9.
26. LoCascio RG, Desai P, Sela DA, Weimer B, Mills DA. Broad conservation of milk utilization genes in Bifidobacterium longum subsp. infantis as revealed by comparative genomic hybridization. Appl Environ Microbiol 2010;76:7373-81.
27. Zivkovic AM, German JB, Lebrilla CB, Mills DA. Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proc Natl Acad Sci USA 2011;108:Suppl 1:4653-8.
28. Sela DA, Mills DA. The marriage of nutrigenomics with the microbiome: the case of infant-associated bifidobacteria and milk. Am J Clin Nutr 2014;99:697S-703S.
29. Garrido D, Kim JH, German JB, Raybould HE, Mills DA. Oligosaccharide binding proteins from Bifidobacterium longum subsp. infantis reveal a preference for host glycans. PLoS One 2011;6:e17315.
30. Kim JH, An HJ, Garrido D, German JB, Lebrilla CB, Mills DA. Proteomic analysis of Bifidobacterium longum subsp. infantis reveals the metabolic insight on consumption of prebiotics and host glycans. PLoS One 2013;8:e57535.
31. Sela DA, Li Y, Lerno L, et al. An infant-associated bacterial commensal utilizes breast milk sialyloligosaccharides. J Biol Chem 2011;286:11909-18.
32. Sela DA, Garrido D, Lerno L, et al. Bifidobacterium longum subsp. infantis ATCC 15697 α-fucosidases are active on fucosylated human milk oligosaccharides. Appl Environ Microbiol 2012;78:795-803.
33. Yoshida E, Sakurama H, Kiyohara M, et al. Bifidobacterium longum subsp. infantis uses two different β-galactosidases for selectively degrading type-1 and type-2 human milk oligosaccharides. Glycobiology 2012;22:361-8.
34. Garrido D, Ruiz-Moyano S, Mills DA. Release and utilization of N-acetyl-d-glucosamine from human milk oligosaccharides by Bifidobacterium longum subsp. infantis. Anaerobe 2012;18:430-5.
35. Marcobal A, Barboza M, Sonnenburg ED, et al. Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host Microbe 2011;10:507-14.
36. Ng KM, Ferreyra JA, Higginbottom SK, et al. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 2013;502:96-9.
37. Park EJ, Suh M, Ramanujam K, Steiner K, Begg D, Clandinin MT. Dietinduced changes in membrane gangliosides in rat intestinal mucosa, plasma and brain. J Pediatr Gastroenterol Nutr 2005;40:487-95.
38. Rueda R. The role of dietary gangliosides on immunity and the prevention of infection. Br J Nutr 2007;98:Suppl 1:S68-73.
39. Lee H, Garrido D, Mills DA, Barile D. Hydrolysis of milk gangliosides by infant-gut associated bifidobacteria determined by microfluidic chips and high-resolution mass spectrometry. Electrophoresis 2014;35:1742-50.
40. Garrido D, Nwosu C, Ruiz-Moyano S, et al. Endo-β-N-acetylglucosaminidases from infant gut-associated bifidobacteria release complex N-glycans from human milk glycoproteins. Mol Cell Proteomics 2012;11: 775-85.
41. Westerbeek EA, van den Berg A, Lafeber HN, Knol J, Fetter WP, van Elburg RM. The intestinal bacterial colonisation in preterm infants: a review of the literature. Clin Nutr 2006;25:361-8.
42. Morrow AL, Lagomarcino AJ, Schibler KR, et al. Early microbial and metabolomic signatures predict later onset of necrotizing enterocolitis in preterm infants. Microbiome 2013;1:13.
43. Cotten CM, Taylor S, Stoll B, et al. Prolonged duration of initial empirical antibiotic treatment is associated with increased rates of necrotizing enterocolitis and death for extremely low birth weight infants. Pediatrics 2009;123:58-66.
44. Guillet R, Stoll BJ, Cotten CM, et al. Association of H2-blocker therapy and higher incidence of necrotizing enterocolitis in very low birth weight infants. Pediatrics 2006;117:e137-142.
45. Mai V, Young CM, Ukhanova M, et al. Fecal microbiota in premature infants prior to necrotizing enterocolitis. PLoS One 2011;6:e20647.
46. Meinzen-Derr J, Poindexter B, Wrage L, Morrow AL, Stoll B, Donovan EF. Role of human milk in extremely low birth weight infants' risk of necrotizing enterocolitis or death. J Perinatol 2009;29:57-62.
47. De Leoz ML, Gaerlan SC, Strum JS, et al. Lacto-N-tetraose, fucosylation, and secretor status are highly variable in human milk oligosaccharides from women delivering preterm. J Proteome Res 2012;11:4662-72.
48. Underwood MA, Kalanetra KM, Bokulich NA, et al. Prebiotic oligosaccharides in premature infants. J Pediatr Gastroenterol Nutr 2014;58:352-60.
49. Westerbeek EA, Slump RA, Lafeber HN, et al. The effect of enteral supplementation of specific neutral and acidic oligosaccharides on the faecal microbiota and intestinal microenvironment in preterm infants. Eur J Clin Microbiol Infect Dis 2013;32:269-76.
50. Westerbeek EA, van den Berg JP, Lafeber HN, et al. Neutral and acidic oligosaccharides in preterm infants: a randomized, double-blind, placebocontrolled trial. Am J Clin Nutr 2010;91:679-86.
51. LeCouffe NE, Westerbeek EA, van Schie PE, Schaaf VA, Lafeber HN, van Elburg RM. Neurodevelopmental outcome during the first year of life in preterm infants after supplementation of a prebiotic mixture in the neonatal period: a follow-up study. Neuropediatrics 2014;45:22-9.
52. AlFaleh K, Anabrees J. Probiotics for prevention of necrotizing enterocolitis in preterm infants. Cochrane Database Syst Rev 2014;4:CD005496.
53. Jacobs SE, Tobin JM, Opie GF, et al. Probiotic effects on late-onset sepsis in very preterm infants: a randomized controlled trial. Pediatrics 2013;132:1055-62.
54. Janvier A, Malo J, Barrington KJ. Cohort study of probiotics in a North American neonatal intensive care unit. J Pediatr 2014;164:980-5.
55. Ofek Shlomai N, Deshpande G, Rao S, Patole S. Probiotics for preterm neonates: what will it take to change clinical practice? Neonatology 2014;105:64-70.
56. Marcobal A, Underwood MA, Mills DA. Rapid determination of the bacterial composition of commercial probiotic products by terminal restriction fragment length polymorphism analysis. J Pediatr Gastroenterol Nutr 2008;46:608-11.
57. Aureli P, Fiore A, Scalfaro C, Casale M, Franciosa G. National survey outcomes on commercial probiotic food supplements in Italy. Int J Food Microbiol 2010;137:265-73.
58. Underwood MA, Kalanetra KM, Bokulich NA, et al. A comparison of two probiotic strains of bifidobacteria in premature infants. J Pediatr 2013;163:1585-91.e9.
59. Underwood MA, Salzman NH, Bennett SH, et al. A randomized placebocontrolled comparison of 2 prebiotic/probiotic combinations in preterm infants: impact on weight gain, intestinal microbiota, and fecal short-chain fatty acids. J Pediatr Gastroenterol Nutr 2009;48:216-25.
60. Samanta M, Sarkar M, Ghosh P, Ghosh Jk, Sinha Mk, Chatterjee S. Prophylactic probiotics for prevention of necrotizing enterocolitis in very low birth weight newborns. J Trop Pediatr 2009;55:128-31.
61. Lin HC, Su BH, Chen AC, et al. Oral probiotics reduce the incidence and severity of necrotizing enterocolitis in very low birth weight infants. Pediatrics 2005;115:1-4.
62. Fernández-Carrocera LA, Solis-Herrera A, Cabanillas-Ayón M, et al. Double-blind, randomised clinical assay to evaluate the efficacy of probiotics in preterm newborns weighing less than 1500 g in the prevention of necrotising enterocolitis. Arch Dis Child Fetal Neonatal Ed 2013;98:F5-9.
63. Bin-Nun A, Bromiker R, Wilschanski M, et al. Oral probiotics prevent necrotizing enterocolitis in very low birth weight neonates. J Pediatr 2005;147:192-6.
64. Szajewska H, Guandalini S, Morelli L, Van Goudoever JB, Walker A. Effect of Bifidobacterium animalis subsp lactis supplementation in preterm infants: a systematic review of randomized controlled trials. J Pediatr Gastroenterol Nutr 2010;51:203-9.
65. Chichlowski M, De Lartigue G, German JB, Raybould HE, Mills DA. Bifidobacteria isolated from infants and cultured on human milk oligosaccharides affect intestinal epithelial function. J Pediatr Gastroenterol Nutr 2012;55:321-7.
66. Kavanaugh DW, O'Callaghan J, Butto LF, et al. Exposure of subsp. to milk oligosaccharides increases adhesion to epithelial cells and induces a substantial transcriptional response. PLoS One 2013;8:e67224.
67. Neu J, Walker WA. Necrotizing enterocolitis. N Engl J Med 2011;364: 255-64.
68. Ganguli K, Meng D, Rautava S, Lu L, Walker WA, Nanthakumar N. Probiotics prevent necrotizing enterocolitis by modulating enterocyte genes that regulate innate immune-mediated inflammation. Am J Physiol Gastrointest Liver Physiol 2013;304:G132-41.
69. Weng M, Ganguli K, Zhu W, Shi HN, Walker WA. Conditioned medium from Bifidobacteria infantis protects against Cronobacter sakazakiiinduced intestinal inflammation in newborn mice. Am J Physiol Gastrointest Liver Physiol 2014;306:G779-87.
70. Romond MB, Colavizza M, Mullié C, et al. Does the intestinal bifidobacterial colonisation affect bacterial translocation? Anaerobe 2008;14:43-8.
71. Bergmann KR, Liu SX, Tian R, et al. Bifidobacteria stabilize claudins at tight junctions and prevent intestinal barrier dysfunction in mouse necrotizing enterocolitis. Am J Pathol 2013;182:1595-606.
72. Puertollano E, Kolida S, Yaqoob P. Biological significance of short-chain fatty acid metabolism by the intestinal microbiome. Curr Opin Clin Nutr Metab Care 2014;17:139-44.
73. Waligora-Dupriet AJ, Dugay A, Auzeil N, et al. Short-chain fatty acids and polyamines in the pathogenesis of necrotizing enterocolitis: kinetics aspects in gnotobiotic quails. Anaerobe 2009;15:138-44.
74. Nafday SM, Chen W, Peng L, Babyatsky MW, Holzman IR, Lin J. Shortchain fatty acids induce colonic mucosal injury in rats with various postnatal ages. Pediatr Res 2005;57:201-4.
75. Wang C, Shoji H, Sato H, et al. Effects of oral administration of Bifidobacterium breve on fecal lactic acid and short-chain fatty acids in low birth weight infants. J Pediatr Gastroenterol Nutr 2007;44:252-7.
76. Mohan R, Koebnick C, Schildt J, Mueller M, Radke M, Blaut M. Effects of Bifidobacterium lactis Bb12 supplementation on body weight, fecal pH, acetate, lactate, calprotectin, and IgA in preterm infants. Pediatr Res 2008;64:418-22.
77. de Vrese M, Rautenberg P, Laue C, Koopmans M, Herremans T, Schrezenmeir J. Probiotic bacteria stimulate virus-specific neutralizing antibodies following a booster polio vaccination. Eur J Nutr 2005;44:406-13.
78. Maidens C, Childs C, Przemska A, Dayel IB, Yaqoob P. Modulation of vaccine response by concomitant probiotic administration. Br J Clin Pharmacol 2013;75:663-70.
79. Wu S, Tao N, German JB, Grimm R, Lebrilla CB. Development of an annotated library of neutral human milk oligosaccharides. J Proteome Res 2010;9:4138-51.
80. Wu S, Grimm R, German JB, Lebrilla CB. Annotation and structural analysis of sialylated human milk oligosaccharides. J Proteome Res 2011;10: 856-68.
81. Urashima T, Saito T, Nakamura T, Messer M. Oligosaccharides of milk and colostrum in non-human mammals. Glycoconj J 2001;18:357-71.
82. Boehm G, Stahl B. Oligosaccharides. In: Mattila-Sandholm T, Saarela M, eds. Functional Dairy Products. Cambridge, England: CRC Press, 2003:203-243.
83. Tao N, DePeters EJ, Freeman S, German JB, Grimm R, Lebrilla CB. Bovine milk glycome. J Dairy Sci 2008;91:3768-78.