Intestinal colonization: How key microbial players become established in this dynamic process: Microbial metabolic activities and the interplay between the host and microbes Prospects & Overviews S. E. Aidy et al.

BioEssays

Volumn 35, Issue 10, 2013, Pages 913-923

  El Aidy, Sahar ^a   Van Den Abbeele, Pieter ^b   Van De Wiele, Tom ^b   Louis, Petra ^c   Kleerebezem, Michiel ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b GHENT UNIVERSITY   (Belgium)

^c ROWETT RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Butyrate; Clostridium cluster IV and XIVa; Core microbiome; Cross feeding; Fucosylation; Mucus; Sulfate reducing bacteria

Indexed keywords

BUTYRIC ACID; FUCOSYLTRANSFERASE; LACTIC ACID; METHYLAMINE; SHORT CHAIN FATTY ACID; SUCCINIC ACID;

ARTICLE; BACTEROIDES; BIFIDOBACTERIUM; BINDING SITE; CLOSTRIDIUM; ENVIRONMENTAL FACTOR; GASTROINTESTINAL TRACT; HUMAN; IMMUNE RESPONSE; INTESTINE FLORA; INTESTINE MUCOSA; METABOLISM; MICROBIAL COLONIZATION; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROBIOME; NONHUMAN; PROTEIN EXPRESSION;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM;

BUTYRATE; CLOSTRIDIUM CLUSTER IV AND XIVA; CORE MICROBIOME; CROSS-FEEDING; FUCOSYLATION; MUCUS; SULFATE REDUCING BACTERIA;

ANIMALS; BUTYRATES; CLOSTRIDIUM; HOMEOSTASIS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTESTINES; METABOLOME; MICROBIOTA; SYMBIOSIS;

EID: 84884705771     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201300073     Document Type: Article

References (120)

1. El Aidy S, van Baarlen P, Derrien M, Lindenbergh-Kortleve DJ, et al. 2012. Temporal and spatial interplay of microbiota and intestinal mucosa drive establishment of immune homeostasis in conventionalized mice. Mucosal Immunol 5: 567-79.
2. Holmes E, Kinross J, Gibson GR, Burcelin R, et al. 2012. Therapeutic modulation of microbiota-host metabolic interactions. Sci Transl Med 4: 137rv6.
3. Hooper LV, Littman DR, MacPherson AJ. 2012. Interactions between the microbiota and the immune system. Science 336: 1268-73.
4. Blumberg R, Powrie F. 2012. Microbiota, disease, and back to health: a metastable journey. Sci Transl Med 4: 137rv7.
5. Ley RE, Peterson DA, Gordon JI. 2006. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124: 837-48.
6. Qin J, Li R, Raes J, Arumugam M, et al. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59-65.
7. Arumugam M, Raes J, Pelletier E, Le Paslier D, et al. 2011. Enterotypes of the human gut microbiome. Nature 473: 174-80.
8. Yatsunenko T, Rey FE, Manary MJ, Trehan I, et al. 2012. Human gut microbiome viewed across age and geography. Nature 486: 222-7.
9. Bäckhed F, Ley RE, Sonnenburg JL, Peterson DA, et al. 2005. Host-bacterial mutualism in the human intestine. Science 307: 1915-20.
10. Bates JM, Mittge E, Kuhlman J, Baden KN, et al. 2006. Distinct signals from the microbiota promote different aspects of zebrafish gut differentiation. Dev Biol 297: 374-86.
11. Rawls JF, Samuel BS, Gordon JI. 2004. Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc Natl Acad Sci USA 101: 4596-601.
12. Freitas M, Axelsson LG, Cayuela C, Midtvedt T, et al. 2005. Indigenous microbes and their soluble factors differentially modulate intestinal glycosylation steps in vivo. Use of a "lectin assay" to survey in vivo glycosylation changes. Histochem Cell Biol 124: 423-33.
13. MacPherson AJ, Harris NL. 2004. Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 4: 478-85.
14. Nicholson JK, Holmes E, Kinross J, Burcelin R, et al. 2012. Host-gut microbiota metabolic interactions. Science 336: 1262-7.
15. McFall-Ngai MJ. 2007. Care for the community: a memory-based immune system may have evolved in vertebrates because of the need to recognize and manage complex communities of beneficial microbes. Nature 445: 153.
16. O'Hara AM, Shanahan F. 2006. The gut flora as a forgotten organ. EMBO Rep 7: 688-93.
17. Louis P, Flint HJ. 2009. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett 294: 1-8.
18. Flint HJ, Scott KP, Duncan SH, Louis P, et al. 2012. Microbial degradation of complex carbohydrates in the gut. Gut Microbes 3: 289-306.
19. Martens EC, Koropatkin NM, Smith TJ, Gordon JI. 2009. Complex glycan catabolism by the human gut microbiota: the Bacteroidetes Sus-like paradigm. J Biol Chem 284: 24673-7.
20. Flint HJ, Scott KP, Louis P, Duncan SH. 2012. The role of the gut microbiota in nutrition and health. Nat Rev Gastroenterol Hepatol 9: 577-89.
21. 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: 1535-43.
22. Ze X, Le Mougen F, Duncan SH, Louis P, et al. 2013. Some are more equal than others: the role of "keystone" species in the degradation of recalcitrant substrates. Gut Microbes 4: 236-40.
23. Kovatcheva-Datchary P, Egert M, Maathuis A, Rajilić-Stojanović M, et al. 2009. Linking phylogenetic identities of bacteria to starch fermentation in an in vitro model of the large intestine by RNA-based stable isotope probing. Environ Microbiol 11: 914-26.
24. Kau AL, Ahern PP, Griffin NW, Goodman AL, et al. 2011. Human nutrition, the gut microbiome and the immune system. Nature 474: 327-36.
25. Palmer C, Bik EM, DiGiulio DB, Relman DA, et al. 2007. Development of the human infant intestinal microbiota. PLoS Biol 5: e177.
26. El Aidy S, Derrien M, Merrifield CA, Levenez F, et al. 2013. Gut bacteria-host metabolic interplay during conventionalisation of the mouse germfree colon. ISME J 7: 743-55.
27. Martin JA, Hamilton BE, Ventura SJ, Osterman MJK, et al. 2012. Births: final data for 2012. Natl Vital Stat Rep 61: 1-72.
28. Biasucci G, Benenati B, Morelli L, Bessi E, et al. 2008. Cesarean delivery may affect the early biodiversity of intestinal bacteria. J Nutr 138: 1796S-800S.
29. Sela DA, Mills DA. 2010. Nursing our microbiota: molecular linkages between bifidobacteria and milk oligosaccharides. Trends Microbiol 18: 298-307.
30. Cabrera-Rubio R, Collado MC, Laitinen K, Salminen S, et al. 2012. The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am J Clin Nutr 96: 544-51.
31. 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.
32. Mackie RI, Sghir A, Gaskins HR. 1999. Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 69: 1035S-45S.
33. 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.
34. Adlerberth I, Wold AE. 2009. Establishment of the gut microbiota in Western infants. Acta Paediatr 98: 229-38.
35. Duncan SH, Louis P, Flint HJ. 2004. Lactate-utilising bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl Environ Microb 70: 5810-7.
36. Falony G, Vlachou A, Verbrugghe K, De Vuyst L. 2006. Cross-feeding between Bifidobacterium longum BB536 and acetate-converting, butyrate-producing colon bacteria during growth on oligofructose. App Environ Microbiol 72: 7835-41.
37. Fischbach MA, Sonnenburg JL. 2011. Eating for two: how metabolism establishes interspecies interactions in the gut. Cell Host Microbe 10: 336-47.
38. Sharma R, Young C, Neu J. 2010. Molecular modulation of intestinal epithelial barrier: contribution of microbiota. J Biomed Biotechnol 2010: 305879.
39. Meng D, Newburg DS, Young C, Baker A, et al. 2007. Bacterial symbionts induce a FUT2-dependent fucosylated niche on colonic epithelium via ERK and JNK signaling. Am J Physiol Gastrointest Liver Physiol 293: G780-7.
40. Bry L, Falk PG, Midtvedt T, Gordon JI. 1996. A model of host-microbial interactions in an open mammalian ecosystem. Science 273: 1380-3.
41. Umesaki Y, Okada Y, Matsumoto S, Imaoka A, et al. 1995. Segmented filamentous bacteria are indigenous intestinal bacteria that activate intraepithelial lymphocytes and induce MHC class II molecules and fucosyl asialo GM1 glycolipids on the small intestinal epithelial cells in the ex-germ-free mouse. Microbiol Immunol 39: 555-62.
42. Iwamori M, Domino SE. 2004. Tissue-specific loss of fucosylated glycolipids in mice with targeted deletion of alpha(1, 2)fucosyltransferase genes. Biochem J 380: 75-81.
43. Xu J, Bjursell MK, Himrod J, Deng S, et al. 2003. A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 299: 2074-6.
44. Pacheco AR, Curtis MM, Ritchie JM, Munera D, et al. 2012. Fucose sensing regulates bacterial intestinal colonization. Nature 492: 113-7.
45. Mukherjee S, Vaishnava S, Hooper LV. 2008. Multi-layered regulation of intestinal antimicrobial defense. Cell Mol Life Sci 65: 3019-27.
46. Cheesman SE, Guillemin K. 2007. We know you are in there: conversing with the indigenous gut microbiota. Res Microbiol 158: 2-9.
47. Canny GO, McCormick BA. 2008. Bacteria in the intestine, helpful residents or enemies from within? Infect Immun 76: 3360-73.
48. Marquet P, Duncan SH, Chassard C, Bernalier-Donadille A, et al. 2009. Lactate has the potential to promote hydrogen sulphide formation in the human colon. FEMS Microbiol Lett 299: 128-34.
49. Gibson GR. 1990. Physiology and ecology of the sulphate-reducing bacteria. J Appl Bacteriol 69: 769-97.
50. Hashizume K, Tsukahara T, Yamada K, Koyama H, et al. 2003. Megasphaera elsdenii JCM1772T normalizes hyperlactate production in the large intestine of fructooligosaccharide-fed rats by stimulating butyrate production. J Nutr 133: 3187-90.
51. Bourriaud C, Robins RJ, Martin L, Kozlowski F, et al. 2005. Lactate is mainly fermented to butyrate by human intestinal microfloras but inter-individual variation is evident. J Appl Microbiol 99: 201-12.
52. Belenguer A, Duncan SH, Calder G, Holtrop G, et al. 2006. Two routes of metabolic cross-feeding between bifidobacteria and butyrate-producing anaerobes from the human gut. Appl Environ Microb 72: 3593-9.
53. Belenguer A, Duncan SH, Holtrop G, Anderson E, et al. 2007. Impact of pH on lactate formation and utilization by human fecal microbial communities. Appl Environ Microb 73: 6526-33.
54. Morrison DJ, Mackay WG, Edwards CA, Preston T, et al. 2006. Butyrate production from oligofructose fermentation by the human faecal flora: what is the contribution of extracellular acetate and lactate? Brit J Nutr 96: 570-7.
55. Okada T, Fukuda S, Hase K, Nishiumi S, et al. 2013. Microbiota-derived lactate accelerates colon epithelial cell turnover in starvation-refed mice. Nat Commun 4: 1654.
56. Deplancke B, Hristova KR, Oakley HA, McCracken VJ, et al. 2000. Molecular ecological analysis of the succession and diversity of sulfate-reducing bacteria in the mouse gastrointestinal tract. Appl Environ Microbiol 66: 2166-74.
57. Tsai HH, Sunderland D, Gibson GR, Hart CA, et al. 1992. A novel mucin sulphatase from human feces: its identification, purification and characterization. Clin Sci (Lond) 82: 447-54.
58. Forstner JF, Oliver MG, Sylvester FA. 1995. Production, structure, and biologic relevance of gastrointestinal mucins. In Blauser MJ, Smith PD, Ravdin JJ, Greenberg HD, et al. eds.; Infections of the Gastrointestinal Tract. New York, NY: Raven Press. 71-88.
59. Wilkinson RK, Roberton AM. 1988. A novel glycosulphatase isolated from a mucus glycopeptide-degrading Bacteroides sp. FEMS Microbiol Lett 50: 195-9.
60. Roberton AM, McKenzie CG, Sharfe N, Stubbs LB. 1993. A glycosulphatase that removes sulphate from mucus glycoprotein. Biochem J 293: 683-9.
61. Corfield AP, Wagner SA, Clamp JR. 1987. Detection of a carbohydrate sulphatase in human faecal extracts. Biochem Soc Trans 15: 1089.
62. Rhodes JM, Gallimore R, Elias E, Kennedy JF. 1985. Faecal sulphatase in health and inflammatory bowel disease. Gut 26: 466-9.
63. Fite A, MacFarlane GT, Cummings JH, Hopkins MJ, et al. 2004. Identification and quantitation of mucosal and faecal desulfovibrios using real time polymerase chain reaction. Gut 53: 523-9.
64. Karkhoff-Schweizer RR, Huber DPW, Voordouw G. 1995. Conservation of the genes for dissimilatory sulfite reductase from Desulfovibrio vulgaris and Archaeoglobus fulgidus allows their detection by PCR. Appl Environ Microbiol 61: 290-6.
65. Widdel F, Hansen TA. 1992. The dissimilatory sulfate- and sulfurreducing bacteria. In Balows A, Trüper HG, Dworkin M, Harder W, et al. eds; The Prokaryotes 2nd ed. New York, NY: Springer-Verlag. p. 583-624.
66. Goubern M, Andriamihaja M, Nübel T, Blachier F, et al. 2007. Sulfide, the first inorganic substrate for human cells. FASEB J 21: 1699-706.
67. Gallego D, Clavé P, Donovan J, Rahmati R, et al. 2008. The gaseous mediator, hydrogen sulphide, inhibits in vitro motor patterns in the human, rat and mouse colon and jejunum. Neurogastroenterol Motil 20: 1306-16.
68. Loubinoux J, Bronowicki JP, Pereira IA, Mougenel JL, et al. 2002. Sulfate-reducing bacteria in human feces and their association with inflammatory bowel diseases. FEMS Microbiol Ecol 40: 107-12.
69. Stebbings S, Munro K, Simon MA, Tannock G, et al. 2002. Comparison of the faecal microflora of patients with ankylosing spondylitis and controls using molecular methods of analysis. Rheumatology (Oxford) 41: 1395-401.
70. Lewis S, Cochrane S. 2007. Alteration of sulfate and hydrogen metabolism in the human colon by changing intestinal transit rate. Am J Gastroenterol 102: 624-33.
71. Gibson GR, Cummings JH, MacFarlane GT. 1991. Growth and activities of sulphate-reducing bacteria in gut contents of healthy subjects and patients with ulcerative colitis. FEMS Microbiol Ecol 86: 101-12.
72. Pitcher MCL, Beatty ER, Cummings JH. 2000. The contribution of sulphate reducing bacteria and 5-aminosalicyclic acid to faecal sulphide in patients with ulcerative colitis. Gut 46: 64-72.
73. Roediger WE, Moore J, Babidge W. 1997. Colonic sulfide in pathogenesis and treatment of ulcerative colitis. Dig Dis Sci 42: 1571-9.
74. Pitcher MC, Cummings JH. 1996. Hydrogen sulphide: a bacterial toxin in ulcerative colitis? Gut 39: 1-4.
75. Attene-Ramos MS, Wagner ED, Gaskins HR, Plewa MJ. 2007. Hydrogen sulfide induces direct radical-associated DNA damage. Mol Cancer Res 5: 455-9.
76. Fukushima K, Ogawa H, Takahashi K, Naito H, et al. 2003. Non-pathogenic bacteria modulate colonic epithelial gene expression in germ-free mice. Scand J Gastroenterol 38: 626-34.
77. Louis P, Flint HJ. 2007. Development of a semiquantitative degenerate real-time pcr-based assay for estimation of numbers of butyryl-coenzyme A (CoA) CoA transferase genes in complex bacterial samples. Appl Environ Microbiol 73: 2009-12.
78. Atarashi K, Tanoue T, Shima T, Imaoka A, et al. 2011. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331: 337-41.
79. Frank DN, St Amand AL, Feldman RA, Boedeker EC, et al. 2007. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 104: 13780-5.
80. Van den Abbeele P, Belzer C, Goossens M, Kleerebezem M, et al. 2013. Butyrate-producing Clostridium cluster XIVa species specifically colonize mucins in an in vitro gut model. ISME J 7: 949-61.
81. Crellin NK, Garcia RV, Hadisfar O, Allan SE, et al. 2005. Human CD4+ T cells express TLR5 and its ligand flagellin enhances the suppressive capacity and expression of FOXP3 in CD4+CD25+T regulatory cells. J Immunol 175: 8051-9.
82. Cummings JH, MacFarlane GT. 1991. The control and consequences of bacterial fermentation in the human colon. J Appl Bacteriol 70: 443-59.
83. Walker AW, Duncan SH, McWilliam Leitch EC, Child MW, et al. 2005. pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl Environ Microbiol 71: 3692-700.
84. Kleerebezem M, Vaughan EE. 2009. Probiotic and gut lactobacilli and bifidobacteria: molecular approaches to study diversity and activity. Annu Rev Microbiol 63: 269-90.
85. Schauber J, Svanholm C, Termén S, Iffland K, et al. 2003. Expression of the cathelicidin LL-37 is modulated by short chain fatty acids in colonocytes: relevance of signalling pathways. Gut 52: 735-41.
86. Maslowski KM, Vieira AT, Ng A, Kranich J, et al. 2009. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461: 1282-6.
87. Cummings JH, Pomare EW, Branch WJ, Naylor CP, et al. 1987. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28: 1221-7.
88. Hamer HM, Jonkers DM, Bast A, Vanhoutvin SA, et al. 2009. Butyrate modulates oxidative stress in the colonic mucosa of healthy humans. Clin Nutr 28: 88-93.
89. Blottière HM, Buecher B, Galmiche JP, Cherbut C. 2003. Molecular analysis of the effect of short-chain fatty acids on intestinal cell proliferation. Proc Nutr Soc 62: 101-6.
90. Bjursell M, Admyre T, Göransson M, Marley AE, et al. 2011. Improved glucose control and reduced body fat mass in free fatty acid receptor 2-deficient mice fed a high-fat diet. Am J Physiol Endocrinol Metab 300: E211-20.
91. Wang Z, Klipfell E, Bennett BJ, Koeth R. 2011. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472: 57-63.
92. Tap J, Mondot S, Levenez F, Pelletier E, et al. 2009. Towards the human intestinal microbiota phylogenetic core. Environ Microbiol 11: 2574-84.
93. Louis P, Young P, Holtrop G, Flint HJ. 2010. Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA:acetate CoA-transferase gene. Environ Microbiol 12: 304-14.
94. Johansson ME, Larsson JM, Hansson GC. 2011. The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc Natl Acad Sci USA 108 (Suppl 1): 4659-65.
95. Van den Abbeele P, Gérard P, Rabot S, Bruneau A, et al. 2011. Arabinoxylans and inulin differentially modulate the mucosal and luminal gut microbiota and mucin-degradation in humanized rats. Environ Microbiol 13: 2667-80.
96. Nava GM, Friedrichsen HJ, Stappenbeck TS. 2011. Spatial organization of intestinal microbiota in the mouse ascending colon. ISME J 5: 627-38.
97. Hong P-Y, Croix JA, Greenberg E, Gaskins HR, et al. 2011. Pyrosequencing-based analysis of the mucosal microbiota in healthy individuals reveals ubiquitous bacterial groups and micro-heterogeneity. PLoS One 6: e25042.
98. Shen XJ, Rawls JF, Randall TA, Burcall L, et al. 2010. Molecular characterization of mucosal adherent bacteria and associations with colorectal adenomas. Gut Microbes 1: 138-47.
99. Wang Y, Antonopoulos D, Zhu X, Harrell L, et al. 2010. Laser capture microdissection and metagenomic analysis of intact mucosa-associated microbial communities of human colon. Appl Environ Microbiol 88: 1333-42.
100. Willing BP, Dicksved J, Halfvarson J, Andersson AF, et al. 2010. A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterol 139: 1844-54.e1841.
101. Leitch ECM, Walker AW, Duncan SH, Holtrop G, et al. 2007. Selective colonization of insoluble substrates by human faecal bacteria. Environ Microbiol 9: 667-79.
102. Walker AW, Duncan SH, Harmsen HJM, Holtrop G, et al. 2008. The species composition of the human intestinal microbiota differs between particle-associated and liquid phase communities. Environ Microbiol 10: 3275-83.
103. Belzer C, de Vos WM. 2012. Microbes inside - from diversity to function: the case of Akkermansia. ISME J 6: 1449-58.
104. Espey MG. 2013. Role of oxygen gradients in shaping redox relationships between the human intestine and its microbiota. Free Radic Biol Med 55: 130-40.
105. Khan MT, Duncan SH, Stams AJM, van Dijl JM, et al. 2012. The gut anaerobe Faecalibacterium prausnitzii uses an extracellular electron shuttle to grow at oxic-anoxic interphases. ISME J 6: 1578-85.
106. Claesson MJ, Cusack S, O'Sullivan O, Greene-Diniz R, et al. 2011. Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci USA 108 (Suppl 1): 4586-91.
107. Duytschaever G, Huys G, Bekaert M, Boulanger L, et al. 2012. Dysbiosis of bifidobacteria and Clostridium cluster XIVa in the cystic fibrosis fecal microbiota. J Cyst Fibros 12: 206-15.
108. Duck LW, Walter MR, Novak J, Kelly D, et al. 2007. Isolation of flagellated bacteria implicated in Crohn's disease. Inflamm Bowel Dis 13: 1191-201.
109. Sokol H, Pigneur B, Watterlot L, Lakhdari O, et al. 2008. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 105: 16731-6.
110. Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, et al. 2006. Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut 55: 205-11.
111. Mäkivuokko H, Tiihonen K, Tynkkynen S, Paulin L, et al. 2010. The effect of age and non-steroidal anti-inflammatory drugs on human intestinal microbiota composition. Br J Nutr 103: 227-34.
112. Biagi E, Nylund L, Candela M, Ostan R, et al. 2010. Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLoS One 5: e10667.
113. Collado MC, Derrien M, Isolauri E, de Vos WM, et al. 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: 7767-70.
114. Swidsinski A, Loening-Baucke V, Theissig F, Engelhardt H, et al. 2007. Comparative study of the intestinal mucus barrier in normal and inflamed colon. Gut 56: 343-50.
115. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, et al. 2010. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 107: 14691-6.
116. Duncan SH, Belenguer A, Holtrop G, Johnstone AM, et al. 2007. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl Environ Microbiol 73: 1073-8.
117. Duncan SH, Louis P, Thomson JM, Flint HJ. 2009. The role of pH in determining the species composition of the human colonic microbiota Environ Microbiol 11: 2112-22.
118. Willing BP, Russell SL, Finlay BB. 2011. Shifting the balance: antibiotic effects on host-microbiota mutualism. Nat Rev Microbiol 9: 233-43.
119. Dostal A, Chassard C, Hilty FM, Zimmermann MB, et al. 2012. Iron depletion and repletion with ferrous sulfate or electrolytic iron modifies the composition and metabolic activity of the gut microbiota in rats. J Nutr 142: 271-7.
120. Walker AW, Ince J, Duncan SH, Webster LM, et al. 2011. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J 5: 220-30.