Abstract
Throughout the human life, the gut microbiota interacts with us in a number of different ways, thereby influencing our health status. The acquisition of such an interactive gut microbiota commences at birth. Medical and environmental factors including diet, antibiotic exposure and mode of delivery are major factors that shape the composition of the microbial communities in the infant gut. Among the most abundant members of the infant microbiota are species belonging to the Bifidobacterium genus, which are believed to confer beneficial effects upon their host. Bifidobacteria may be acquired directly from the mother by vertical transmission and their persistence in the infant gut is associated with their saccharolytic activity toward glycans that are abundant in the infant gut. Here, we discuss the establishment of the infant gut microbiota and the contribution of bifidobacteria to this early life microbial consortium.
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Adlerberth I, Wold AE (2009) Establishment of the gut microbiota in Western infants. Acta Paediatr 98:229–238
Agans R, Rigsbee L, Kenche H, Michail S, Khamis HJ, Paliy O (2011) Distal gut microbiota of adolescent children is different from that of adults. FEMS Microbiol Ecol 77:404–412
Ajslev TA, Andersen CS, Gamborg M, Sorensen TI, Jess T (2011) Childhood overweight after establishment of the gut microbiota: the role of delivery mode, pre-pregnancy weight and early administration of antibiotics. Int J Obes 35:522–529
Albrecht S, Schols HA, van den Heuvel EG, Voragen AG, Gruppen H (2011) Occurrence of oligosaccharides in feces of breast-fed babies in their first six months of life and the corresponding breast milk. Carbohydr Res 346:2540–2550
Altmann F, Kosma P, O’Callaghan A, Leahy S, Bottacini F, Molloy E, Plattner S, Schiavi E, Gleinser M, Groeger D et al (2016) Genome analysis and characterisation of the exopolysaccharide produced by Bifidobacterium longum subsp. longum 35624. PLoS One 11:e0162983
Alvarez-Martin P, O’Connell Motherway M, Turroni F, Foroni E, Ventura M, van Sinderen D (2012) A two-component regulatory system controls autoregulated serpin expression in Bifidobacterium breve UCC2003. Appl Environ Microbiol 78:7032–7041
Arboleya S, Ang L, Margolles A, Yiyuan L, Dongya Z, Liang X, Solis G, Fernandez N, de Los Reyes-Gavilan CG, Gueimonde M (2012) Deep 16S rRNA metagenomics and quantitative PCR analyses of the premature infant fecal microbiota. Anaerobe 18:378–380
Arboleya S, Sanchez B, Milani C, Duranti S, Solis G, Fernandez N, de los Reyes-Gavilan CG, Ventura M, Margolles A, Gueimonde M (2015) Intestinal microbiota development in preterm neonates and effect of perinatal antibiotics. J Pediatr 166:538–544
Ashida H, Miyake A, Kiyohara M, Wada J, Yoshida E, Kumagai H, Katayama T, Yamamoto K (2009) Two distinct alpha-l-fucosidases from Bifidobacterium bifidum are essential for the utilization of fucosylated milk oligosaccharides and glycoconjugates. Glycobiology 19:1010–1017
Backhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, Li Y, Xia Y, Xie H, Zhong H et al (2015) Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17:852
Bailey MT, Lubach GR, Coe CL (2004) Prenatal stress alters bacterial colonization of the gut in infant monkeys. J Pediatr Gastroenterol Nutr 38:414–421
Barcenilla A, Pryde SE, Martin JC, Duncan SH, Stewart CS, Henderson C, Flint HJ (2000) Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl Environ Microbiol 66:1654–1661
Belenguer A, Duncan SH, Calder AG, Holtrop G, Louis P, Lobley GE, Flint HJ (2006) Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Appl Environ Microbiol 72:3593–3599
Bienenstock J, Buck RH, Linke H, Forsythe P, Stanisz AM, Kunze WA (2013) Fucosylated but not sialylated milk oligosaccharides diminish colon motor contractions. PLoS One 8:e76236
Blustein J, Attina T, Liu M, Ryan AM, Cox LM, Blaser MJ, Trasande L (2013) Association of caesarean delivery with child adiposity from age 6 weeks to 15 years. Int J Obes 37:900–906
Bottacini F, O’Connell Motherway M, Casey E, McDonnell B, Mahony J, Ventura M, van Sinderen D (2015) Discovery of a conjugative megaplasmid in Bifidobacterium breve. Appl Environ Microbiol 81:166–176
Bottacini F, O’Connell Motherway M, Kuczynski J, O’Connell KJ, Serafini F, Duranti S, Milani C, Turroni F, Lugli GA, Zomer A et al (2014) Comparative genomics of the Bifidobacterium breve taxon. BMC Genom 15:170
Bottacini F, Ventura M, van Sinderen D, O’Connell Motherway M (2014) Diversity, ecology and intestinal function of bifidobacteria. Microb Cell Fact 13(Suppl 1):S4
Castanys-Munoz E, Martin MJ, Prieto PA (2013) 2′-Fucosyllactose: an abundant, genetically determined soluble glycan present in human milk. Nutr Rev 71:773–789
Cerdeno-Tarraga AM, Patrick S, Crossman LC, Blakely G, Abratt V, Lennard N, Poxton I, Duerden B, Harris B, Quail MA et al (2005) Extensive DNA inversions in the B. fragilis genome control variable gene expression. Science 307:1463–1465
Chaplin AV, Efimov BA, Smeianov VV, Kafarskaia LI, Pikina AP, Shkoporov AN (2015) Intraspecies genomic diversity and long-term persistence of Bifidobacterium longum. PLoS One 10:e0135658
Christiaen SE, O’Connell Motherway M, Bottacini F, Lanigan N, Casey PG, Huys G, Nelis HJ, van Sinderen D, Coenye T (2014) Autoinducer-2 plays a crucial role in gut colonization and probiotic functionality of Bifidobacterium breve UCC2003. PLoS One 9:e98111
Clarke G, O’Mahony SM, Dinan TG, Cryan JF (2014) Priming for health: gut microbiota acquired in early life regulates physiology, brain and behaviour. Acta Paediatr 103:812–819
Colagiorgi A, Turroni F, Mancabelli L, Serafini F, Secchi A, van Sinderen D, Ventura M (2015) Insights into teichoic acid biosynthesis by Bifidobacterium bifidum PRL2010. FEMS Microbiol Lett 362:fnv141
Cox LM, Yamanishi S, Sohn J, Alekseyenko AV, Leung JM, Cho I, Kim SG, Li H, Gao Z, Mahana D et al (2014) Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell 158:705–721
D’Elia JN, Salyers AA (1996) Effect of regulatory protein levels on utilization of starch by Bacteroides thetaiotaomicron. J Bacteriol 178:7180–7186
De Boever P, Wouters R, Verschaeve L, Berckmans P, Schoeters G, Verstraete W (2000) Protective effect of the bile salt hydrolase-active Lactobacillus reuteri against bile salt cytotoxicity. Appl Microbiol Biotechnol 53:709–714
De Leoz ML, Kalanetra KM, Bokulich NA, Strum JS, Underwood MA, German JB, Mills DA, Lebrilla CB (2015) Human milk glycomics and gut microbial genomics in infant feces show a correlation between human milk oligosaccharides and gut microbiota: a proof-of-concept study. J Proteome Res 14:491–502
De Vuyst L, Leroy F (2011) Cross-feeding between bifidobacteria and butyrate-producing colon bacteria explains bifidobacterial competitiveness, butyrate production, and gas production. Int J Food Microbiol 149:73–80
Dethlefsen L, Huse S, Sogin ML, Relman DA (2008) The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol 6:e280
DiGiulio DB, Romero R, Amogan HP, Kusanovic JP, Bik EM, Gotsch F, Kim CJ, Erez O, Edwin S, Relman DA (2008) Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS One 3:e3056
Dogra S, Sakwinska O, Soh SE, Ngom-Bru C, Bruck WM, Berger B, Brussow H, Lee YS, Yap F, Chong YS et al. (2015) Dynamics of infant gut microbiota are influenced by delivery mode and gestational duration and are associated with subsequent adiposity. mBio 6:1–9
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 107:11971–11975
Duncan SH, Flint HJ (2008) Proposal of a neotype strain (A1-86) for Eubacterium rectale. Request for an opinion. Int J Syst Evol Microbiol 58:1735–1736
Duranti S, Milani C, Lugli GA, Turroni F, Mancabelli L, Sanchez B, Ferrario C, Viappiani A, Mangifesta M, Mancino W et al (2015) Insights from genomes of representatives of the human gut commensal Bifidobacterium bifidum. Environ Microbiol 17(7):2515–2531
Duranti S, Turroni F, Lugli GA, Milani C, Viappiani A, Mangifesta M, Gioiosa L, Palanza P, van Sinderen D, Ventura M (2014) Genomic characterization and transcriptional studies of the starch-utilizing strain Bifidobacterium adolescentis 22L. Appl Environ Microbiol 80:6080–6090
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 308:1635–1638
Egan M, Jiang H, O’Connell Motherway M, Oscarson S, van Sinderen D (2016) Glycosulfatase-encoding gene cluster in Bifidobacterium breve UCC2003. Appl Environ Microbiol 82:6611–6623
Egan M, Motherway MO, Kilcoyne M, Kane M, Joshi L, Ventura M, van Sinderen D (2014) Cross-feeding by Bifidobacterium breve UCC2003 during co-cultivation with Bifidobacterium bifidum PRL2010 in a mucin-based medium. BMC Microbiol 14:282
Egan M, O’Connell Motherway M, Ventura M, van Sinderen D (2014) Metabolism of sialic acid by Bifidobacterium breve UCC2003. Appl Environ Microbiol 80:4414–4426
Fallani M, Amarri S, Uusijarvi A, Adam R, Khanna S, Aguilera M, Gil A, Vieites JM, Norin E, Young D et al (2011) Determinants of the human infant intestinal microbiota after the introduction of first complementary foods in infant samples from five European centres. Microbiology 157:1385–1392
Fallani M, Young D, Scott J, Norin E, Amarri S, Adam R, Aguilera M, Khanna S, Gil A, Edwards CA et al (2010) Intestinal microbiota of 6-week-old infants across Europe: geographic influence beyond delivery mode, breast-feeding, and antibiotics. J Pediatr Gastroenterol Nutr 51:77–84
Falony G, Calmeyn T, Leroy F, De Vuyst L (2009) Coculture fermentations of Bifidobacterium species and Bacteroides thetaiotaomicron reveal a mechanistic insight into the prebiotic effect of inulin-type fructans. Appl Environ Microbiol 75:2312–2319
Fanning S, Hall LJ, Cronin M, Zomer A, MacSharry J, Goulding D, Motherway MO, Shanahan F, Nally K, Dougan G et al (2012) Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. Proc Natl Acad Sci USA 109:2108–2113
Farfan MJ, Cantero L, Vidal R, Botkin DJ, Torres AG (2011) Long polar fimbriae of enterohemorrhagic Escherichia coli O157:H7 bind to extracellular matrix proteins. Infect Immun 79:3744–3750
Foroni E, Serafini F, Amidani D, Turroni F, He F, Bottacini F, O’Connell Motherway M, Viappiani A, Zhang Z, Rivetti C et al (2011) Genetic analysis and morphological identification of pilus-like structures in members of the genus Bifidobacterium. Microb Cell Fact 10(Suppl 1):S16
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. J Biol Chem 280:37415–37422
Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y, Yoshimura K, Tobe T, Clarke JM, Topping DL, Suzuki T et al (2011) Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469:543–547
Funkhouser LJ, Bordenstein SR (2013) Mom knows best: the universality of maternal microbial transmission. PLoS Biol 11:e1001631
Garrido D, Ruiz-Moyano S, Lemay DG, Sela DA, German JB, Mills DA (2015) Comparative transcriptomics reveals key differences in the response to milk oligosaccharides of infant gut-associated bifidobacteria. Sci Rep 5:13517
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 102:10321–10326
Hinde K, German JB (2012) Food in an evolutionary context: insights from mother’s milk. J Sci Food Agric 92:2219–2223
Hinde K, Milligan LA (2011) Primate milk: proximate mechanisms and ultimate perspectives. Evol Anthropol 20:9–23
Hollister EB, Riehle K, Luna RA, Weidler EM, Rubio-Gonzales M, Mistretta TA, Raza S, Doddapaneni HV, Metcalf GA, Muzny DM et al (2015) Structure and function of the healthy pre-adolescent pediatric gut microbiome. Microbiome 3:36
Huh SY, Rifas-Shiman SL, Zera CA, Edwards JW, Oken E, Weiss ST, Gillman MW (2012) Delivery by caesarean section and risk of obesity in preschool age children: a prospective cohort study. Arch Dis Child 97:610–616
Huurre A, Kalliomaki M, Rautava S, Rinne M, Salminen S, Isolauri E (2008) Mode of delivery—effects on gut microbiota and humoral immunity. Neonatology 93:236–240
James K, Motherway MO, Bottacini F, van Sinderen D (2016) Bifidobacterium breve UCC2003 metabolises the human milk oligosaccharides lacto-N-tetraose and lacto-N-neo-tetraose through overlapping, yet distinct pathways. Sci Rep 6:38560
Jimenez E, Delgado S, Fernandez L, Garcia N, Albujar M, Gomez A, Rodriguez JM (2008) Assessment of the bacterial diversity of human colostrum and screening of staphylococcal and enterococcal populations for potential virulence factors. Res Microbiol 159:595–601
Jimenez E, Marin ML, Martin R, Odriozola JM, Olivares M, Xaus J, Fernandez L, Rodriguez JM (2008) Is meconium from healthy newborns actually sterile? Res Microbiol 159:187–193
Karav S, Parc AL, de Moura Bell JM, Rouquie C, Mills DA, Barile D, Block DE (2015) Kinetic characterization of a novel endo-beta-N-acetylglucosaminidase on concentrated bovine colostrum whey to release bioactive glycans. Enzyme Microb Technol 77:46–53
Kelly ED, Bottacini F, O’Callaghan J, Motherway MO, O’Connell KJ, Stanton C, van Sinderen D (2016) Glycoside hydrolase family 13 alpha-glucosidases encoded by Bifidobacterium breve UCC2003; A comparative analysis of function, structure and phylogeny. Int J Food Microbiol 224:55–65
Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, Angenent LT, Ley RE (2011) Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA 108(Suppl 1):4578–4585
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 101:14919–14924
Lahtinen SJ, Boyle RJ, Kivivuori S, Oppedisano F, Smith KR, Robins-Browne R, Salminen SJ, Tang ML (2009) Prenatal probiotic administration can influence Bifidobacterium microbiota development in infants at high risk of allergy. J Allergy Clin Immunol 123:499–501
Lamendella R, Santo Domingo JW, Kelty C, Oerther DB (2008) Bifidobacteria in feces and environmental waters. Appl Environ Microbiol 74:575–584
Lee DW, Selamoglu N, Lanciano P, Cooley JW, Forquer I, Kramer DM, Daldal F (2011) Loss of a conserved tyrosine residue of cytochrome b induces reactive oxygen species production by cytochrome bc1. J Biol Chem 286:18139–18148
Lee JH, O’Sullivan DJ (2010) Genomic insights into bifidobacteria. Microbiol Mol Biol Rev 74:378–416
Lewis ZT, Totten SM, Smilowitz JT, Popovic M, Parker E, Lemay DG, Van Tassell ML, Miller MJ, Jin YS, German JB et al (2015) Maternal fucosyltransferase 2 status affects the gut bifidobacterial communities of breastfed infants. Microbiome 3:13
Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444:1022–1023
Lugli GA, Milani C, Turroni F, Tremblay D, Ferrario C, Mancabelli L, Duranti S, Ward DV, Ossiprandi MC, Moineau S et al (2015) Prophages of the genus Bifidobacterium as modulating agents of the infant gut microbiota. Environ Microbiol 18(7):2196–2213
Madan JC, Salari RC, Saxena D, Davidson L, O’Toole GA, Moore JH, Sogin ML, Foster JA, Edwards WH, Palumbo P et al (2012) Gut microbial colonisation in premature neonates predicts neonatal sepsis. Arch Dis Child Fetal Neonatal Ed 97:F456–F462
Marcobal A, Barboza M, Sonnenburg ED, Pudlo N, Martens EC, Desai P, Lebrilla CB, Weimer BC, Mills DA, German JB et al (2011) Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host Microbe 10:507–514
Matamoros S, Gras-Leguen C, Le Vacon F, Potel G, de La Cochetiere MF (2013) Development of intestinal microbiota in infants and its impact on health. Trends Microbiol 21:167–173
Matsuki T, Yahagi K, Mori H, Matsumoto H, Hara T, Tajima S, Ogawa E, Kodama H, Yamamoto K, Yamada T et al (2016) A key genetic factor for fucosyllactose utilization affects infant gut microbiota development. Nat Commun 7:11939
Milani C, Hevia A, Foroni E, Duranti S, Turroni F, Lugli GA, Sanchez B, Martin R, Gueimonde M, van Sinderen D et al (2013) Assessing the fecal microbiota: an optimized ion torrent 16S rRNA gene-based analysis protocol. PLoS One 8:e68739
Milani C, Lugli GA, Duranti S, Turroni F, Bottacini F, Mangifesta M, Sanchez B, Viappiani A, Mancabelli L, Taminiau B et al (2014) Genomic encyclopedia of type strains of the genus Bifidobacterium. Appl Environ Microbiol 80:6290–6302
Milani C, Lugli GA, Duranti S, Turroni F, Mancabelli L, Ferrario C, Mangifesta M, Hevia A, Viappiani A, Scholz M et al (2015) Bifidobacteria exhibit social behavior through carbohydrate resource sharing in the gut. Sci Rep 5:15782
Milani C, Mancabelli L, Lugli GA, Duranti S, Turroni F, Ferrario C, Mangifesta M, Viappiani A, Ferretti P, Gorfer V et al (2015b) Exploring vertical transmission of bifidobacteria from mother to child. Appl Environ Microbiol 81(20):7078–7087
Milani C, Turroni F, Duranti S, Lugli GA, Mancabelli L, Ferrario C, van Sinderen D, Ventura M (2016) Genomics of the genus bifidobacterium reveals species-specific adaptation to the glycan-rich gut environment. Appl Environ Microbiol 82:980–991
Mohamadzadeh M, Pfeiler EA, Brown JB, Zadeh M, Gramarossa M, Managlia E, Bere P, Sarraj B, Khan MW, Pakanati KC et al (2011) Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc Natl Acad Sci USA 108(Suppl 1):4623–4630
Morris BE, Henneberger R, Huber H, Moissl-Eichinger C (2013) Microbial syntrophy: interaction for the common good. FEMS Microbiol Rev 37:384–406
Morrison DJ, Mackay WG, Edwards CA, Preston T, Dodson B, Weaver LT (2006) Butyrate production from oligofructose fermentation by the human faecal flora: what is the contribution of extracellular acetate and lactate? Br J Nutr 96:570–577
Mueller S, Saunier K, Hanisch C, Norin E, Alm L, Midtvedt T, Cresci A, Silvi S, Orpianesi C, Verdenelli MC et al (2006) Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Appl Environ Microbiol 72:1027–1033
Munoz-Tamayo R, Laroche B, Walter E, Dore J, Duncan SH, Flint HJ, Leclerc M (2011) Kinetic modelling of lactate utilization and butyrate production by key human colonic bacterial species. FEMS Microbiol Ecol 76:615–624
Murphy R, Stewart AW, Braithwaite I, Beasley R, Hancox RJ, Mitchell EA, IPTS Group (2014) Antibiotic treatment during infancy and increased body mass index in boys: an international cross-sectional study. Int J Obes 38:1115–1119
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. Appl Environ Microbiol 73:6444–6449
Nuriel-Ohayon M, Neuman H, Koren O (2016) Microbial changes during pregnancy, birth, and infancy. Front Microbiol 7:1031
O’Callaghan A, van Sinderen D (2016) Bifidobacteria and their role as members of the human gut microbiota. Front Microbiol 7:925
O’Connell Motherway M, Fitzgerald GF, van Sinderen D (2011) Metabolism of a plant derived galactose-containing polysaccharide by Bifidobacterium breve UCC2003. Microb Biotechnol 4:403–416
O’Connell Motherway M, Kinsella M, Fitzgerald GF, van Sinderen D (2013) Transcriptional and functional characterization of genetic elements involved in galacto-oligosaccharide utilization by Bifidobacterium breve UCC2003. Microb Biotechnol 6:67–79
O’Connell Motherway M, Zomer A, Leahy SC, Reunanen J, Bottacini F, Claesson MJ, O’Brien F, Flynn K, Casey PG, Munoz JA et al (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 108:11217–11222
Ottman N, Smidt H, de Vos WM, Belzer C (2012) The function of our microbiota: who is out there and what do they do? Front Cell Infect Microbiol 2:104
Pande S, Shitut S, Freund L, Westermann M, Bertels F, Colesie C, Bischofs IB, Kost C (2015) Metabolic cross-feeding via intercellular nanotubes among bacteria. Nat Commun 6:6238
Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, van den Brandt PA, Stobberingh EE (2006) Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118:511–521
Phelan VV, Liu WT, Pogliano K, Dorrestein PC (2012) Microbial metabolic exchange—the chemotype-to-phenotype link. Nat Chem Biol 8:26–35
Pokusaeva K, Fitzgerald GF, van Sinderen D (2011) Carbohydrate metabolism in Bifidobacteria. Genes Nutr 6:285–306
Pokusaeva K, Neves AR, Zomer A, O’Connell-Motherway M, MacSharry J, Curley P, Fitzgerald GF, van Sinderen D (2010) Ribose utilization by the human commensal Bifidobacterium breve UCC2003. Microb Biotechnol 3:311–323
Pokusaeva K, O’Connell-Motherway M, Zomer A, Fitzgerald GF, van Sinderen D (2009) Characterization of two novel alpha-glucosidases from Bifidobacterium breve UCC2003. Appl Environ Microbiol 75:1135–1143
Potempa J, Korzus E, Travis J (1994) The serpin superfamily of proteinase inhibitors: structure, function, and regulation. J Biol Chem 269:15957–15960
Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T et al (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65
Rajilic-Stojanovic M, de Vos WM (2014) The first 1000 cultured species of the human gastrointestinal microbiota. FEMS Microbiol Rev 38:996–1047
Rajilic-Stojanovic M, Heilig HG, Molenaar D, Kajander K, Surakka A, Smidt H, de Vos WM (2009) Development and application of the human intestinal tract chip, a phylogenetic microarray: analysis of universally conserved phylotypes in the abundant microbiota of young and elderly adults. Environ Microbiol 11:1736–1751
Rinne M, Kalliomaki M, Arvilommi H, Salminen S, Isolauri E (2005) Effect of probiotics and breastfeeding on the bifidobacterium and lactobacillus/enterococcus microbiota and humoral immune responses. J Pediatr 147:186–191
Roger LC, Costabile A, Holland DT, Hoyles L, McCartney AL (2010) Examination of faecal Bifidobacterium populations in breast- and formula-fed infants during the first 18 months of life. Microbiology 156:3329–3341
Ruas-Madiedo P, Gueimonde M, Arigoni F, de los Reyes-Gavilan CG, Margolles A (2009) Bile affects the synthesis of exopolysaccharides by Bifidobacterium animalis. Appl Environ Microbiol 75:1204–1207
Ruas-Madiedo P, Gueimonde M, Fernandez-Garcia M, de los Reyes-Gavilan CG, Margolles A (2008) Mucin degradation by Bifidobacterium strains isolated from the human intestinal microbiota. Appl Environ Microbiol 74:1936–1940
Ruiz L, Delgado S, Ruas-Madiedo P, Margolles A, Sanchez B (2016) Proteinaceous molecules mediating bifidobacterium-host interactions. Front Microbiol 7:1193
Ruiz L, Gueimonde M, Coute Y, Salminen S, Sanchez JC, de los Reyes-Gavilan CG, Margolles A (2011) Evaluation of the ability of Bifidobacterium longum to metabolize human intestinal mucus. FEMS Microbiol Lett 314:125–130
Ruiz L, Margolles A, Sanchez B (2013) Bile resistance mechanisms in Lactobacillus and Bifidobacterium. Front Microbiol 4:396
Ryan SM, Fitzgerald GF, van Sinderen D (2006) Screening for and identification of starch-, amylopectin-, and pullulan-degrading activities in bifidobacterial strains. Appl Environ Microbiol 72:5289–5296
Sabbioni A, Ferrario C, Milani C, Mancabelli L, Riccardi E, Di Ianni F, Beretti V, Superchi P, Ossiprandi MC (2016) Modulation of the bifidobacterial communities of the dog microbiota by zeolite. Front Microbiol 7:1491
Salminen S, Gibson GR, McCartney AL, Isolauri E (2004) Influence of mode of delivery on gut microbiota composition in seven year old children. Gut 53:1388–1389
Samuel BS, Gordon JI (2006) A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. Proc Natl Acad Sci USA 103:10011–10016
Sanchez B, Champomier-Verges MC, Anglade P, Baraige F, de Los Reyes-Gavilan CG, Margolles A, Zagorec M (2005) Proteomic analysis of global changes in protein expression during bile salt exposure of Bifidobacterium longum NCIMB 8809. J Bacteriol 187:5799–5808
Sanchez B, Champomier-Verges MC, Stuer-Lauridsen B, Ruas-Madiedo P, Anglade P, Baraige F, de los Reyes-Gavilan CG, Johansen E, Zagorec M, Margolles A (2007) Adaptation and response of Bifidobacterium animalis subsp. lactis to bile: a proteomic and physiological approach. Appl Environ Microbiol 73:6757–6767
Satokari R, Gronroos T, Laitinen K, Salminen S, Isolauri E (2009) Bifidobacterium and Lactobacillus DNA in the human placenta. Lett Appl Microbiol 48:8–12
Schiavi E, Gleinser M, Molloy E, Groeger D, Frei R, Ferstl R, Rodriguez-Perez N, Ziegler M, Grant R, Moriarty TF et al (2016) The surface-associated exopolysaccharide of Bifidobacterium longum 35624 plays an essential role in dampening host proinflammatory responses and repressing local TH17 responses. Appl Environ Microbiol 82:7185–7196
Schreiner HC, Sinatra K, Kaplan JB, Furgang D, Kachlany SC, Planet PJ, Perez BA, Figurski DH, Fine DH (2003) Tight-adherence genes of Actinobacillus actinomycetemcomitans are required for virulence in a rat model. Proc Natl Acad Sci USA 100:7295–7300
Scott KP, Martin JC, Chassard C, Clerget M, Potrykus J, Campbell G, Mayer CD, Young P, Rucklidge G, Ramsay AG et al (2011) Substrate-driven gene expression in Roseburia inulinivorans: importance of inducible enzymes in the utilization of inulin and starch. Proc Natl Acad Sci USA 108(Suppl 1):4672–4679
Seksik P, Lepage P, de la Cochetiere MF, Bourreille A, Sutren M, Galmiche JP, Dore J, Marteau P (2005) Search for localized dysbiosis in Crohn’s disease ulcerations by temporal temperature gradient gel electrophoresis of 16S rRNA. J Clin Microbiol 43:4654–4658
Sela DA (2011) Bifidobacterial utilization of human milk oligosaccharides. Int J Food Microbiol 149:58–64
Sela DA, Chapman J, Adeuya A, Kim JH, Chen F, Whitehead TR, Lapidus A, Rokhsar DS, Lebrilla CB, German JB et al (2008) The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc Natl Acad Sci USA 105:18964–18969
Smilowitz JT, Lebrilla CB, Mills DA, German JB, Freeman SL (2014) Breast milk oligosaccharides: structure-function relationships in the neonate. Annu Rev Nutr 34:143–169
Sonnenburg JL, Chen CT, Gordon JI (2006) Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host. PLoS Biol 4:e413
Stewart CJ, Embleton ND, Marrs EC, Smith DP, Nelson A, Abdulkadir B, Skeath T, Petrosino JF, Perry JD, Berrington JE et al (2016) Temporal bacterial and metabolic development of the preterm gut reveals specific signatures in health and disease. Microbiome 4:67
Tailford LE, Crost EH, Kavanaugh D, Juge N (2015) Mucin glycan foraging in the human gut microbiome. Front Genet 6:81
Tanaka S, Kobayashi T, Songjinda P, Tateyama A, Tsubouchi M, Kiyohara C, Shirakawa T, Sonomoto K, Nakayama J (2009) Influence of antibiotic exposure in the early postnatal period on the development of intestinal microbiota. FEMS Immunol Med Microbiol 56:80–87
Tao N, Wu S, Kim J, An HJ, Hinde K, Power ML, Gagneux P, German JB, Lebrilla CB (2011) Evolutionary glycomics: characterization of milk oligosaccharides in primates. J Proteome Res 10:1548–1557
Turroni F, Berry D, Ventura M (2016) Editorial: bifidobacteria and their role in the human gut microbiota. Front Microbiol 7:2148
Turroni F, Bottacini F, Foroni E, Mulder I, Kim JH, Zomer A, Sanchez B, Bidossi A, Ferrarini A, Giubellini V et al (2010) Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proc Natl Acad Sci USA 107:19514–19519
Turroni F, Duranti S, Bottacini F, Guglielmetti S, Van Sinderen D, Ventura M (2014) Bifidobacterium bifidum as an example of a specialized human gut commensal. Front Microbiol 5:437
Turroni F, Foroni E, O’Connell Motherway M, Bottacini F, Giubellini V, Zomer A, Ferrarini A, Delledonne M, Zhang Z, van Sinderen D et al (2010) Characterization of the serpin-encoding gene of Bifidobacterium breve 210B. Appl Environ Microbiol 76:3206–3219
Turroni F, Foroni E, Pizzetti P, Giubellini V, Ribbera A, Merusi P, Cagnasso P, Bizzarri B, de’Angelis GL, Shanahan F et al (2009) Exploring the diversity of the bifidobacterial population in the human intestinal tract. Appl Environ Microbiol 75:1534–1545
Turroni F, Marchesi JR, Foroni E, Gueimonde M, Shanahan F, Margolles A, van Sinderen D, Ventura M (2009) Microbiomic analysis of the bifidobacterial population in the human distal gut. ISME J 3:745–751
Turroni F, Milani C, Duranti S, Mancabelli L, Mangifesta M, Viappiani A, Lugli GA, Ferrario C, Gioiosa L, Ferrarini A et al (2016) Deciphering bifidobacterial-mediated metabolic interactions and their impact on gut microbiota by a multi-omics approach. Isme J 10(7):1656–1668
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 2:183–189
Turroni F, Ozcan E, Milani C, Mancabelli L, Viappiani A, van Sinderen D, Sela DA, Ventura M (2015) Glycan cross-feeding activities between bifidobacteria under in vitro conditions. Front Microbiol 6:1030
Turroni F, Peano C, Pass DA, Foroni E, Severgnini M, Claesson MJ, Kerr C, Hourihane J, Murray D, Fuligni F et al (2012) Diversity of bifidobacteria within the infant gut microbiota. PLoS One 7:e36957
Turroni F, Serafini F, Foroni E, Duranti S, O’Connell Motherway M, Taverniti V, Mangifesta M, Milani C, Viappiani A, Roversi T et al (2013) Role of sortase-dependent pili of Bifidobacterium bifidum PRL2010 in modulating bacterium-host interactions. Proc Natl Acad Sci USA 110(27):11151–11156
Turroni F, Serafini F, Mangifesta M, Arioli S, Mora D, van Sinderen D, Ventura M (2014) Expression of sortase-dependent pili of Bifidobacterium bifidum PRL2010 in response to environmental gut conditions. FEMS Microbiol Lett 357:23–33
Turroni F, Ventura M, Butto LF, Duranti S, O’Toole PW, Motherway MO, van Sinderen D (2014) Molecular dialogue between the human gut microbiota and the host: a Lactobacillus and Bifidobacterium perspective. Cell Mol Life Sci 71:183–203
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 2:53–66
van der Maarel MJ, van der Veen B, Uitdehaag JC, Leemhuis H, Dijkhuizen L (2002) Properties and applications of starch-converting enzymes of the alpha-amylase family. J Biotechnol 94:137–155
Vanhoutte T, Huys G, Brandt E, Swings J (2004) Temporal stability analysis of the microbiota in human feces by denaturing gradient gel electrophoresis using universal and group-specific 16S rRNA gene primers. FEMS Microbiol Ecol 48:437–446
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 91:351–372
Ventura M, Canchaya C, Tauch A, Chandra G, Fitzgerald GF, Chater KF, van Sinderen D (2007) Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol Mol Biol Rev 71:495–548
Ventura M, Turroni F, Lugli GA, van Sinderen D (2014) Bifidobacteria and humans: our special friends, from ecological to genomics perspectives. J Sci Food Agric 94(2):163–168
Ventura M, Turroni F, Canchaya C, Vaughan EE, O’Toole PW, van Sinderen D (2009) Microbial diversity in the human intestine and novel insights from metagenomics. Front Biosci 14:3214–3221
Ventura M, Turroni F, Lugli GA, van Sinderen D (2014) Bifidobacteria and humans: our special friends, from ecological to genomics perspectives. J Sci Food Agric 94:163–168
Ventura M, Turroni F, Motherway MO, MacSharry J, van Sinderen D (2012) Host-microbe interactions that facilitate gut colonization by commensal bifidobacteria. Trends Microbiol 20:467–476
Ventura M, Turroni F, Zomer A, Foroni E, Giubellini V, Bottacini F, Canchaya C, Claesson MJ, He F, Mantzourani M et al (2009) The Bifidobacterium dentium Bd1 genome sequence reflects its genetic adaptation to the human oral cavity. PLoS Genet 5:e1000785
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. Appl Environ Microbiol 74:3996–4004
Watson D, O’Connell Motherway M, Schoterman MH, van Neerven RJ, Nauta A, van Sinderen D (2013) Selective carbohydrate utilization by lactobacilli and bifidobacteria. J Appl Microbiol 114:1132–1146
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 25:361–368
Xavier KB, Bassler BL (2003) LuxS quorum sensing: more than just a numbers game. Curr Opin Microbiol 6:191–197
Xia G, Kohler T, Peschel A (2010) The wall teichoic acid and lipoteichoic acid polymers of Staphylococcus aureus. Int J Med Microbiol IJMM 300:148–154
Yassour M, Vatanen T, Siljander H, Hamalainen AM, Harkonen T, Ryhanen SJ, Franzosa EA, Vlamakis H, Huttenhower C, Gevers D et al (2016) Natural history of the infant gut microbiome and impact of antibiotic treatment on bacterial strain diversity and stability. Sci Transl Med 8:343ra381
Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP et al (2012) Human gut microbiome viewed across age and geography. Nature 486:222–227
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 22:361–368
Zanotti I, Turroni F, Piemontese A, Mancabelli L, Milani C, Viappiani A, Prevedini G, Sanchez B, Margolles A, Elviri L et al (2015) Evidence for cholesterol-lowering activity by Bifidobacterium bifidum PRL2010 through gut microbiota modulation. Appl Microbiol Biotechnol 99:6813–6829
Ze X, Duncan SH, Louis P, Flint HJ (2012) Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon. ISME J 6:1535–1543
Acknowledgements
This work was funded by the EU Joint Programming Initiative—a Healthy Diet for a Healthy Life (JPI HDHL, http://www.healthydietforhealthylife.eu/) and the MIUR to MV. We thank GenProbio srl for financial support of the Laboratory of Probiogenomics. LM is supported by Fondazione Cariparma, Parma, Italy. SD is supported by Fondazione Caritro, Trento, Italy. DvS is a member of The APC Microbiome Institute funded by Science Foundation Ireland (SFI), through the Irish Government’s National Development Plan (Grant number SFI/12/RC/2273).
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Turroni, F., Milani, C., Duranti, S. et al. Bifidobacteria and the infant gut: an example of co-evolution and natural selection. Cell. Mol. Life Sci. 75, 103–118 (2018). https://doi.org/10.1007/s00018-017-2672-0
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DOI: https://doi.org/10.1007/s00018-017-2672-0