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Composition and Function of the Gut Microbiome

  • Michael Blaut
Chapter

Abstract

The human gastrointestinal tract harbors a plethora of microorganisms, most of which belong to the domain Bacteria. Owing to manifold effects on host physiology and host health, there is a growing interest in better understanding the role and function of gut microbial communities. Microbiota composition changes along the gastrointestinal tract in response to changes in the physicochemical conditions and substrate availability. Moreover, large interindividual differences are observed. One major function of the gut microbiota lies in the conversion of indigestible dietary carbohydrates and host-derived glycans to short-chain fatty acids, which provide energy to the host and have regulatory functions. Microbiome analysis has led to the notion of a “core microbiome” which encodes functions shared by human individuals. Gut microbial community members interact with each other and with the host constituting a functional microbial ecosystem. However, there are still major gaps in our understanding of the molecular mechanisms underlying such interactions.

References

  1. Abell, G. C., Cooke, C. M., Bennett, C. N., Conlon, M. A., & McOrist, A. L. (2008). Phylotypes related to Ruminococcus bromii are abundant in the large bowel of humans and increase in response to a diet high in resistant starch. FEMS Microbiology Ecology, 66, 505–515.PubMedCrossRefGoogle Scholar
  2. Amann, R. I., Ludwig, W., & Schleifer, K.-H. (1995). Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiological Reviews, 59, 143–169.PubMedPubMedCentralGoogle Scholar
  3. Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D. R., Fernandes, G. R., Tap, J., Bruls, T., Batto, J. M., et al. (2011). Enterotypes of the human gut microbiome. Nature, 473, 174–180.PubMedPubMedCentralCrossRefGoogle Scholar
  4. Atkinson, C., Berman, S., Humbert, O., & Lampe, J. W. (2004). In vitro incubation of human feces with daidzein and antibiotics suggests interindividual differences in the bacteria responsible for equol production. The Journal of Nutrition, 134, 596–599.PubMedCrossRefGoogle Scholar
  5. Axelson, M., Sjövall, J., Gustafsson, B. E., & Setchell, K. D. R. (1982). Origin of lignans in mammals and identification of a precursor from plants. Nature, 298, 659–660.PubMedCrossRefGoogle Scholar
  6. Backhed, F., Ley, R. E., Sonnenburg, J. L., Peterson, D. A., & Gordon, J. I. (2005). Host-bacterial mutualism in the human intestine. Science, 307, 1915–1920.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Baughn, A. D., & Malamy, M. H. (2004). The strict anaerobe Bacteroides fragilis grows in and benefits from nanomolar concentrations of oxygen. Nature, 427, 441–444.PubMedCrossRefGoogle Scholar
  8. Belenguer, A., Duncan, S. H., Holtrop, G., Anderson, S. E., Lobley, G. E., & Flint, H. J. (2007). Impact of pH on lactate formation and utilization by human fecal microbial communities. Applied and Environmental Microbiology, 73, 6526–6533.PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bennett, B. J., de Aguiar Vallim, T. Q., Wang, Z., Shih, D. M., Meng, Y., Gregory, J., Allayee, H., Lee, R., Graham, M., Crooke, R., et al. (2013). Trimethylamine-N-oxide, a metabolite associated with atherosclerosis, exhibits complex genetic and dietary regulation. Cell Metabolism, 17, 49–60.PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bernalier, A., Willems, A., Leclerc, M., Rochet, V., & Collins, M. D. (1996). Ruminococcus hydrogenotrophicus sp. nov., a new H2/CO2-utilizing acetogenic bacterium isolated from human feces. Archives of Microbiology, 166, 176–183.PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bik, E. M., Eckburg, P. B., Gill, S. R., Nelson, K. E., Purdom, E. A., Francois, F., Perez-Perez, G., Blaser, M. J., & Relman, D. A. (2006). Molecular analysis of the bacterial microbiota in the human stomach. Proceedings of the National Academy of Sciences of the United States of America, 103, 732–737.PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bindels, L. B., Delzenne, N. M., Cani, P. D., & Walter, J. (2015). Towards a more comprehensive concept for prebiotics. Nature Reviews. Gastroenterology & Hepatology, 12, 303–310.CrossRefGoogle Scholar
  13. Booijink, C. C., El-Aidy, S., Rajilic-Stojanovic, M., Heilig, H. G., Troost, F. J., Smidt, H., Kleerebezem, M., De Vos, W. M., & Zoetendal, E. G. (2010). High temporal and inter-individual variation detected in the human ileal microbiota. Environmental Microbiology, 12, 3213–3227.PubMedCrossRefGoogle Scholar
  14. Braune, A., & Blaut, M. (2012). Intestinal bacterium Eubacterium cellulosolvens deglycosylates flavonoid C- and O-glucosides. Applied and Environmental Microbiology, 78, 8151–8153.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Braune, A., & Blaut, M. (2016). Bacterial species involved in the conversion of dietary flavonoids in the human gut. Gut Microbes, 7, 216–234.PubMedPubMedCentralCrossRefGoogle Scholar
  16. Braune, A., Engst, W., & Blaut, M. (2016). Identification and functional expression of genes encoding flavonoid O- and C-glycosidases in intestinal bacteria. Environmental Microbiology, 18, 2117–2129.PubMedCrossRefGoogle Scholar
  17. Brown, A. J., Goldsworthy, S. M., Barnes, A. A., Eilert, M. M., Tcheang, L., Daniels, D., Muir, A. I., Wigglesworth, M. J., Kinghorn, I., Fraser, N. J., et al. (2003). The orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. The Journal of Biological Chemistry, 278, 11312–11319.PubMedCrossRefGoogle Scholar
  18. Bry, L., Falk, P. G., Midtvedt, T., & Gordon, J. I. (1996). A model of host-microbial interactions in an open mammalian ecosystem. Science, 273, 1380–1383.PubMedCrossRefGoogle Scholar
  19. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., & Henrissat, B. (2009). The Carbohydrate-Active EnZymes database (CAZy): An expert resource for glycogenomics. Nucleic Acids Research, 37, D233–D238.PubMedCrossRefGoogle Scholar
  20. Carbonero, F., Benefiel, A. C., Alizadeh-Ghamsari, A. H., & Gaskins, H. R. (2012). Microbial pathways in colonic sulfur metabolism and links with health and disease. Frontiers in Physiology, 3, 448.PubMedPubMedCentralCrossRefGoogle Scholar
  21. Chassard, C., Goumy, V., Leclerc, M., Del'homme, C., & Bernalier-Donadille, A. (2007). Characterization of the xylan-degrading microbial community from human faeces. FEMS Microbiology Ecology, 61, 121–131.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Chen, Y., Ji, F., Guo, J., Shi, D., Fang, D., & Li, L. (2016). Dysbiosis of small intestinal microbiota in liver cirrhosis and its association with etiology. Scientific Reports, 6, 34055.PubMedPubMedCentralCrossRefGoogle Scholar
  23. Chen, T., Long, W., Zhang, C., Liu, S., Zhao, L., & Hamaker, B. R. (2017). Fiber-utilizing capacity varies in Prevotella- versus Bacteroides-dominated gut microbiota. Scientific Reports, 7, 2594.PubMedPubMedCentralCrossRefGoogle Scholar
  24. Cho, K. H., Cho, D., Wang, G. R., & Salyers, A. A. (2001). New regulatory gene that contributes to control of Bacteroides thetaiotaomicron starch utilization genes. Journal of Bacteriology, 183, 7198–7205.PubMedPubMedCentralCrossRefGoogle Scholar
  25. Christl, S. U., Gibson, G. R., & Cummings, J. H. (1992). Role of dietary sulphate in the regulation of methanogenesis in the human large intestine. Gut, 33, 1234–1238.PubMedPubMedCentralCrossRefGoogle Scholar
  26. Clavel, T., Henderson, G., Alpert, C. A., Philippe, C., Rigottier-Gois, L., Dore, J., & Blaut, M. (2005). Intestinal bacterial communities that produce active estrogen-like compounds enterodiol and enterolactone in humans. Applied and Environmental Microbiology, 71, 6077–6085.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Clavel, T., Borrmann, D., Braune, A., Dore, J., & Blaut, M. (2006a). Occurrence and activity of human intestinal bacteria involved in the conversion of dietary lignans. Anaerobe, 12, 140–147.PubMedPubMedCentralCrossRefGoogle Scholar
  28. Clavel, T., Dore, J., & Blaut, M. (2006b). Bioavailability of lignans in human subjects. Nutrition Research Reviews, 19, 187–196.PubMedPubMedCentralCrossRefGoogle Scholar
  29. Clavel, T., Lippman, R., Gavini, F., Dore, J., & Blaut, M. (2007). Clostridium saccharogumia sp. nov. and Lactonifactor longoviformis gen. nov., sp. nov., two novel human faecal bacteria involved in the conversion of the dietary phytoestrogen secoisolariciresinol diglucoside. Systematic and Applied Microbiology, 30, 16–26.PubMedPubMedCentralCrossRefGoogle Scholar
  30. Cummings, J. H. (1995). Short chain fatty acids. In G. R. Gibson & G. T. Macfarlane (Eds.), Human colonic bacteria: Role in nutrition, physiology and pathology (pp. 101–130). CRC Press: Boca Raton.Google Scholar
  31. Cummings, J. H., & Macfarlane, G. T. (1991). The control and consequences of bacterial fermentation in the human colon. The Journal of Applied Bacteriology, 70, 443–459.PubMedCrossRefGoogle Scholar
  32. Cummings, J. H., Pomare, E. W., Branch, W. J., Naylor, C. P., & Macfarlane, G. T. (1987). Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut, 28, 1221–1227.PubMedPubMedCentralCrossRefGoogle Scholar
  33. Darragh, A. J., & Hodgkinson, S. M. (2000). Quantifying the digestibility of dietary protein. The Journal of Nutrition, 130, 1850S–1856S.PubMedCrossRefGoogle Scholar
  34. De Filippo, C., Cavalieri, D., Di Paola, M., Ramazzotti, M., Poullet, J. B., Massart, S., Collini, S., Pieraccini, G., & Lionetti, P. (2010). Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proceedings of the National Academy of Sciences of the United States of America, 107, 14691–14696.PubMedPubMedCentralCrossRefGoogle Scholar
  35. Devlin, A. S., & Fischbach, M. A. (2015). A biosynthetic pathway for a prominent class of microbiota-derived bile acids. Nature Chemical Biology, 11, 685–690.PubMedPubMedCentralCrossRefGoogle Scholar
  36. Di Rienzi, S. C., Sharon, I., Wrighton, K. C., Koren, O., Hug, L. A., Thomas, B. C., Goodrich, J. K., Bell, J. T., Spector, T. D., Banfield, J. F., & Ley, R. E. (2013). The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria. eLife, 2, e01102.PubMedPubMedCentralCrossRefGoogle Scholar
  37. Dumas, M. E., Barton, R. H., Toye, A., Cloarec, O., Blancher, C., Rothwell, A., Fearnside, J., Tatoud, R., Blanc, V., Lindon, J. C., et al. (2006). Metabolic profiling reveals a contribution of gut microbiota to fatty liver phenotype in insulin-resistant mice. Proceedings of the National Academy of Sciences of the United States of America, 103, 12511–12516.PubMedPubMedCentralCrossRefGoogle Scholar
  38. Duncan, S. H., Barcenilla, A., Stewart, C. S., Pryde, S. E., & Flint, H. J. (2002). Acetate utilization and butyryl coenzyme A (CoA): Acetate-CoA transferase in butyrate-producing bacteria from the human large intestine. Applied and Environmental Microbiology, 68, 5186–5190.PubMedPubMedCentralCrossRefGoogle Scholar
  39. Duncan, S. H., Louis, P., & Flint, H. J. (2004). Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Applied and Environmental Microbiology, 70, 5810–5817.PubMedPubMedCentralCrossRefGoogle Scholar
  40. Eckburg, P. B., Bik, E. M., Bernstein, C. N., Purdom, E., Dethlefsen, L., Sargent, M., Gill, S. R., Nelson, K. E., & Relman, D. A. (2005). Diversity of the human intestinal microbial flora. Science, 308, 1635–1638.PubMedPubMedCentralCrossRefGoogle Scholar
  41. Faith, J. J., Guruge, J. L., Charbonneau, M., Subramanian, S., Seedorf, H., Goodman, A. L., Clemente, J. C., Knight, R., Heath, A. C., Leibel, R. L., et al. (2013). The long-term stability of the human gut microbiota. Science, 341, 1237439.PubMedPubMedCentralCrossRefGoogle Scholar
  42. Finegold, S. M., Flora, D. J., Attebery, H. R., & Sutter, V. L. (1975). Fecal bacteriology of colonic polyp patients and control patients. Cancer Research, 35, 3407–3417.PubMedGoogle Scholar
  43. Finegold, S. M., Sutter, V. L., & Mathisen, G. E. (1983). Normal indigenous intestinal flora. In D. J. Hentges (Ed.), Human intestinal microflora in health and disease (pp. 3–31). Academic Press: New York/London.CrossRefGoogle Scholar
  44. Flint, H. J., Scott, K. P., Duncan, S. H., Louis, P., & Forano, E. (2012). Microbial degradation of complex carbohydrates in the gut. Gut Microbes, 3, 289–306.PubMedPubMedCentralCrossRefGoogle Scholar
  45. Florin, T. H., Zhu, G., Kirk, K. M., & Martin, N. G. (2000). Shared and unique environmental factors determine the ecology of methanogens in humans and rats. The American Journal of Gastroenterology, 95, 2872–2879.PubMedCrossRefGoogle Scholar
  46. Frank, D. N., St Amand, A. L., Feldman, R. A., Boedeker, E. C., Harpaz, N., & Pace, N. R. (2007). Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proceedings of the National Academy of Sciences of the United States of America, 104, 13780–13785.PubMedPubMedCentralCrossRefGoogle Scholar
  47. Gibson, S. A., McFarlan, C., Hay, S., & MacFarlane, G. T. (1989). Significance of microflora in proteolysis in the colon. Applied and Environmental Microbiology, 55, 679–683.PubMedPubMedCentralGoogle Scholar
  48. Gill, S. R., Pop, M., Deboy, R. T., Eckburg, P. B., Turnbaugh, P. J., Samuel, B. S., Gordon, J. I., Relman, D. A., Fraser-Liggett, C. M., & Nelson, K. E. (2006). Metagenomic analysis of the human distal gut microbiome. Science, 312, 1355–1359.PubMedPubMedCentralCrossRefGoogle Scholar
  49. Hayashi, H., Takahashi, R., Nishi, T., Sakamoto, M., & Benno, Y. (2005). Molecular analysis of jejunal, ileal, caecal and recto-sigmoidal human colonic microbiota using 16S rRNA gene libraries and terminal restriction fragment length polymorphism. Journal of Medical Microbiology, 54, 1093–1101.PubMedCrossRefGoogle Scholar
  50. Hehemann, J. H., Correc, G., Barbeyron, T., Helbert, W., Czjzek, M., & Michel, G. (2010). Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature, 464, 908–912.PubMedCrossRefGoogle Scholar
  51. Hespell, R. B., & Smith, C. J. (1983). Utilization of nitrogen sources by gastrointestinal tract bacteria. In D. J. Hentges (Ed.), Human intestinal microflora in health and disease (p. 21). New York, London: Academic Press.Google Scholar
  52. Hoffmann, C., Dollive, S., Grunberg, S., Chen, J., Li, H., Wu, G. D., Lewis, J. D., & Bushman, F. D. (2013). Archaea and fungi of the human gut microbiome: Correlations with diet and bacterial residents. PLoS One, 8, e66019.PubMedPubMedCentralCrossRefGoogle Scholar
  53. Hollman, P. C., & Katan, M. B. (1999). Dietary flavonoids: Intake, health effects and bioavailability. Food and Chemical Toxicology, 37, 937–942.PubMedCrossRefGoogle Scholar
  54. Hooper, L. V., Xu, J., Falk, P. G., Midtvedt, T., & Gordon, J. I. (1999). A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem. Proceedings of the National Academy of Sciences of the United States of America, 96, 9833–9838.PubMedPubMedCentralCrossRefGoogle Scholar
  55. Hornich, M., & Chrastova, V. (1981). The redox potential of the large intestine in swine in relation to swine dysentery. Veterinary Medicine (Praha), 26, 593–598.Google Scholar
  56. Hoskins, L. C. (1993). Mucin degradation in the human gastrointestinal tract and its significance to enteric microbial ecology. European Journal of Gastroenterology & Hepatology, 5, 205–213.CrossRefGoogle Scholar
  57. Huffnagle, G. B., & Noverr, M. C. (2013). The emerging world of the fungal microbiome. Trends in Microbiology, 21, 334–341.PubMedPubMedCentralCrossRefGoogle Scholar
  58. Hug, L. A., Baker, B. J., Anantharaman, K., Brown, C. T., Probst, A. J., Castelle, C. J., Butterfield, C. N., Hernsdorf, A. W., Amano, Y., Ise, K., et al. (2016). A new view of the tree of life. Nature Microbiology, 1, 16048.PubMedCrossRefGoogle Scholar
  59. Hungate, R. E. (1969). A roll tube method for cultivation of strict anaerobes. In J. R. Norris & D. W. Ribbons (Eds.), Methods in microbiology (p. 117). Academic Press: New York.Google Scholar
  60. Huse, S. M., Ye, Y., Zhou, Y., & Fodor, A. A. (2012). A core human microbiome as viewed through 16S rRNA sequence clusters. PLoS One, 7, e34242.PubMedPubMedCentralCrossRefGoogle Scholar
  61. Jiang, Y., Xiong, X., Danska, J., & Parkinson, J. (2016). Metatranscriptomic analysis of diverse microbial communities reveals core metabolic pathways and microbiome-specific functionality. Microbiome, 4, 2.PubMedPubMedCentralCrossRefGoogle Scholar
  62. Jones, B. V., Begley, M., Hill, C., Gahan, C. G., & Marchesi, J. R. (2008). Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome. Proceedings of the National Academy of Sciences of the United States of America, 105, 13580–13585.PubMedPubMedCentralCrossRefGoogle Scholar
  63. Khan, M. T., Duncan, S. H., Stams, A. J., van Dijl, J. M., Flint, H. J., & Harmsen, H. J. (2012). The gut anaerobe Faecalibacterium prausnitzii uses an extracellular electron shuttle to grow at oxic-anoxic interphases. The ISME Journal, 6, 1578–1585.PubMedPubMedCentralCrossRefGoogle Scholar
  64. Kitahara, M., Sakamoto, M., Ike, M., Sakata, S., & Benno, Y. (2005). Bacteroides plebeius sp. nov. and Bacteroides coprocola sp. nov., isolated from human faeces. International Journal of Systematic and Evolutionary Microbiology, 55, 2143–2147.PubMedCrossRefGoogle Scholar
  65. Knights, D., Ward, T. L., McKinlay, C. E., Miller, H., Gonzalez, A., McDonald, D., & Knight, R. (2014). Rethinking “enterotypes”. Cell Host & Microbe, 16, 433–437.CrossRefGoogle Scholar
  66. Kumar, R., Mukherjee, M., Bhandari, M., Kumar, A., Sidhu, H., & Mittal, R. D. (2002). Role of Oxalobacter formigenes in calcium oxalate stone disease: A study from North India. European Urology, 41, 318–322.PubMedCrossRefGoogle Scholar
  67. Lazarova, D. L., Chiaro, C., Wong, T., Drago, E., Rainey, A., O’Malley, S., & Bordonaro, M. (2013). CBP activity mediates effects of the histone deacetylase inhibitor butyrate on WNT activity and apoptosis in colon cancer cells. Journal of Cancer, 4, 481–490.PubMedPubMedCentralCrossRefGoogle Scholar
  68. Ley, R. E., Hamady, M., Lozupone, C., Turnbaugh, P. J., Ramey, R. R., Bircher, J. S., Schlegel, M. L., Tucker, T. A., Schrenzel, M. D., Knight, R., & Gordon, J. I. (2008). Evolution of mammals and their gut microbes. Science, 320, 1647–1651.PubMedPubMedCentralCrossRefGoogle Scholar
  69. Liang, C., Tseng, H. C., Chen, H. M., Wang, W. C., Chiu, C. M., Chang, J. Y., Lu, K. Y., Weng, S. L., Chang, T. H., Chang, C. H., et al. (2017). Diversity and enterotype in gut bacterial community of adults in Taiwan. BMC Genomics, 18, 932.PubMedPubMedCentralCrossRefGoogle Scholar
  70. Lim, M. Y., Rho, M., Song, Y. M., Lee, K., Sung, J., & Ko, G. (2014). Stability of gut enterotypes in Korean monozygotic twins and their association with biomarkers and diet. Scientific Reports, 4, 7348.PubMedPubMedCentralCrossRefGoogle Scholar
  71. Lin, H. V., Frassetto, A., Kowalik, E. J., Jr., Nawrocki, A. R., Lu, M. M., Kosinski, J. R., Hubert, J. A., Szeto, D., Yao, X., Forrest, G., & Marsh, D. J. (2012). Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS One, 7, e35240.PubMedPubMedCentralCrossRefGoogle Scholar
  72. Liu, C., Finegold, S. M., Song, Y., & Lawson, P. A. (2008). Reclassification of Clostridium coccoides, Ruminococcus hansenii, Ruminococcus hydrogenotrophicus, Ruminococcus luti, Ruminococcus productus and Ruminococcus schinkii as Blautia coccoides gen. nov., comb. nov., Blautia hansenii comb. nov., Blautia hydrogenotrophica comb. nov., Blautia luti comb. nov., Blautia producta comb. nov., Blautia schinkii comb. nov. and description of Blautia wexlerae sp. nov., isolated from human faeces. International Journal of Systematic and Evolutionary Microbiology, 58, 1896–1902.PubMedCrossRefGoogle Scholar
  73. Lopez, C. A., Winter, S. E., Rivera-Chavez, F., Xavier, M. N., Poon, V., Nuccio, S. P., Tsolis, R. M., & Baumler, A. J. (2012). Phage-mediated acquisition of a type III secreted effector protein boosts growth of salmonella by nitrate respiration. MBio, 3, e00143–e00112.PubMedPubMedCentralCrossRefGoogle Scholar
  74. Lopez-Siles, M., Khan, T. M., Duncan, S. H., Harmsen, H. J., Garcia-Gil, L. J., & Flint, H. J. (2012). Cultured representatives of two major phylogroups of human colonic Faecalibacterium prausnitzii can utilize pectin, uronic acids, and host-derived substrates for growth. Applied and Environmental Microbiology, 78, 420–428.PubMedPubMedCentralCrossRefGoogle Scholar
  75. Macfarlane, G. T., Cummings, J. H., & Allison, C. (1986). Protein degradation by human intestinal bacteria. Journal of General Microbiology, 132, 1647–1656.PubMedGoogle Scholar
  76. Macfarlane, G. T., Gibson, G. R., & Cummings, J. H. (1992). Comparison of fermentation reactions in different regions of the human colon. The Journal of Applied Bacteriology, 72, 57–64.PubMedGoogle Scholar
  77. Magee, E. A., Richardson, C. J., Hughes, R., & Cummings, J. H. (2000). Contribution of dietary protein to sulfide production in the large intestine: An in vitro and a controlled feeding study in humans. The American Journal of Clinical Nutrition, 72, 1488–1494.PubMedCrossRefGoogle Scholar
  78. Martens, E. C., Chiang, H. C., & Gordon, J. I. (2008). Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host & Microbe, 4, 447–457.CrossRefGoogle Scholar
  79. Maruo, T., Sakamoto, M., Ito, C., Toda, T., & Benno, Y. (2008). Adlercreutzia equolifaciens gen. nov., sp. nov., an equol-producing bacterium isolated from human faeces, and emended description of the genus Eggerthella. International Journal of Systematic and Evolutionary Microbiology, 58, 1221–1227.PubMedCrossRefGoogle Scholar
  80. Matthies, A., Blaut, M., & Braune, A. (2009). Isolation of a human intestinal bacterium capable of daidzein and genistein conversion. Applied and Environmental Microbiology, 75, 1740–1744.PubMedPubMedCentralCrossRefGoogle Scholar
  81. McNulty, N. P., Wu, M., Erickson, A. R., Pan, C., Erickson, B. K., Martens, E. C., Pudlo, N. A., Muegge, B. D., Henrissat, B., Hettich, R. L., & Gordon, J. I. (2013). Effects of diet on resource utilization by a model human gut microbiota containing Bacteroides cellulosilyticus WH2, a symbiont with an extensive glycobiome. PLoS Biology, 11, e1001637.PubMedPubMedCentralCrossRefGoogle Scholar
  82. Metcalf, A. M., Phillips, S. F., Zinsmeister, A. R., MacCarty, R. L., Beart, R. W., & Wolff, B. G. (1987). Simplified assessment of segmental colonic transit. Gastroenterology, 92, 40–47.PubMedCrossRefGoogle Scholar
  83. Minot, S., Sinha, R., Chen, J., Li, H., Keilbaugh, S. A., Wu, G. D., Lewis, J. D., & Bushman, F. D. (2011). The human gut virome: Inter-individual variation and dynamic response to diet. Genome Research, 21, 1616–1625.PubMedPubMedCentralCrossRefGoogle Scholar
  84. Nava, G. M., Carbonero, F., Croix, J. A., Greenberg, E., & Gaskins, H. R. (2012). Abundance and diversity of mucosa-associated hydrogenotrophic microbes in the healthy human colon. The ISME Journal, 6, 57–70.PubMedCrossRefGoogle Scholar
  85. Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., 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.PubMedPubMedCentralCrossRefGoogle Scholar
  86. Ragsdale, S. W. (2006). Metals and their scaffolds to promote difficult enzymatic reactions. Chemical Reviews, 106, 3317–3337.PubMedCrossRefGoogle Scholar
  87. Ramsay, A. G., Scott, K. P., Martin, J. C., Rincon, M. T., & Flint, H. J. (2006). Cell-associated alpha-amylases of butyrate-producing Firmicute bacteria from the human colon. Microbiology, 152, 3281–3290.PubMedCrossRefGoogle Scholar
  88. Reeves, A. R., Wang, G. R., & Salyers, A. A. (1997). Characterization of four outer membrane proteins that play a role in utilization of starch by Bacteroides thetaiotaomicron. Journal of Bacteriology, 179, 643–649.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Reichardt, N., Duncan, S. H., Young, P., Belenguer, A., McWilliam Leitch, C., Scott, K. P., Flint, H. J., & Louis, P. (2014). Phylogenetic distribution of three pathways for propionate production within the human gut microbiota. The ISME Journal, 8, 1323–1335.PubMedPubMedCentralCrossRefGoogle Scholar
  90. Ridlon, J. M., Kang, D. J., & Hylemon, P. B. (2006). Bile salt biotransformations by human intestinal bacteria. Journal of Lipid Research, 47, 241–259.PubMedPubMedCentralCrossRefGoogle Scholar
  91. Roediger, W. E. (1980). Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut, 21, 793–798.PubMedPubMedCentralCrossRefGoogle Scholar
  92. Salyers, A. A., Palmer, J. K., & Wilkins, T. D. (1977a). Laminarinase (beta-glucanase) activity in Bacteroides from the human colon. Applied and Environmental Microbiology, 33, 1118–1124.PubMedPubMedCentralGoogle Scholar
  93. Salyers, A. A., West, S. E., Vercellotti, J. R., & Wilkins, T. D. (1977b). Fermentation of mucins and plant polysaccharides by anaerobic bacteria from the human colon. Applied and Environmental Microbiology, 34, 529–533.PubMedPubMedCentralGoogle Scholar
  94. Savage, D. C. (1977). Microbial ecology of the gastrointestinal tract. Annual Review of Microbiology, 31, 107–133.PubMedPubMedCentralCrossRefGoogle Scholar
  95. Schauer, K., Rodionov, D. A., & de Reuse, H. (2008). New substrates for TonB-dependent transport: Do we only see the ‘tip of the iceberg’? Trends in Biochemical Sciences, 33, 330–338.PubMedPubMedCentralCrossRefGoogle Scholar
  96. Schoefer, L., Mohan, R., Braune, A., Birringer, M., & Blaut, M. (2002). Anaerobic C-ring cleavage of genistein and daidzein by Eubacterium ramulus. FEMS Mircrobiology Letters, 208, 197–202.CrossRefGoogle Scholar
  97. Schroder, C., Matthies, A., Engst, W., Blaut, M., & Braune, A. (2013). Identification and expression of genes involved in the conversion of daidzein and genistein by the equol-forming bacterium Slackia isoflavoniconvertens. Applied and Environmental Microbiology, 79, 3494–3502.PubMedPubMedCentralCrossRefGoogle Scholar
  98. Scott, K. P., Martin, J. C., Chassard, C., Clerget, M., Potrykus, J., Campbell, G., Mayer, C. D., Young, P., Rucklidge, G., Ramsay, A. G., & Flint, H. J. (2011). Substrate-driven gene expression in Roseburia inulinivorans: Importance of inducible enzymes in the utilization of inulin and starch. Proceedings of the National Academy of Sciences of the United States of America, 108(Suppl 1), 4672–4679.PubMedPubMedCentralCrossRefGoogle Scholar
  99. Sender, R., Fuchs, S., & Milo, R. (2016a). Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans. Cell, 164, 337–340.PubMedPubMedCentralCrossRefGoogle Scholar
  100. Sender, R., Fuchs, S., & Milo, R. (2016b). Revised estimates for the number of human and bacteria cells in the body. PLoS Biology, 14, e1002533.PubMedPubMedCentralCrossRefGoogle Scholar
  101. Setchell, K. D., & Clerici, C. (2010). Equol: History, chemistry, and formation. The Journal of Nutrition, 140, 1355S–1362S.PubMedPubMedCentralCrossRefGoogle Scholar
  102. Shipman, J. A., Cho, K. H., Siegel, H. A., & Salyers, A. A. (1999). Physiological characterization of SusG, an outer membrane protein essential for starch utilization by Bacteroides thetaiotaomicron. Journal of Bacteriology, 181, 7206–7211.PubMedPubMedCentralGoogle Scholar
  103. Shipman, J. A., Berleman, J. E., & Salyers, A. A. (2000). Characterization of four outer membrane proteins involved in binding starch to the cell surface of Bacteroides thetaiotaomicron. Journal of Bacteriology, 182, 5365–5372.PubMedPubMedCentralCrossRefGoogle Scholar
  104. Sonnenburg, J. L., Xu, J., Leip, D. D., Chen, C. H., Westover, B. P., Weatherford, J., Buhler, J. D., & Gordon, J. I. (2005). Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science, 307, 1955–1959.PubMedPubMedCentralCrossRefGoogle Scholar
  105. Sonnenburg, E. D., Zheng, H., Joglekar, P., Higginbottom, S. K., Firbank, S. J., Bolam, D. N., & Sonnenburg, J. L. (2010). Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations. Cell, 141, 1241–1252.PubMedPubMedCentralCrossRefGoogle Scholar
  106. Sonnenburg, E. D., Smits, S. A., Tikhonov, M., Higginbottom, S. K., Wingreen, N. S., & Sonnenburg, J. L. (2016). Diet-induced extinctions in the gut microbiota compound over generations. Nature, 529, 212–215.PubMedPubMedCentralCrossRefGoogle Scholar
  107. Suau, A., Bonnet, R., Sutren, M., Godon, J. J., Gibson, G. R., Collins, M. D., & Doré, J. (1999). Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Applied and Environmental Microbiology, 65, 4799–4807.PubMedPubMedCentralGoogle Scholar
  108. Sugihara, P. T., Sutter, V. L., Attebery, H. R., Bricknell, K. S., & Finegold, S. M. (1974). Isolation of Acidaminococcus fermentans and Megasphaera elsdenii from normal human feces. Applied Microbiology, 27, 274–275.PubMedPubMedCentralGoogle Scholar
  109. Suhr, M. J., & Hallen-Adams, H. E. (2015). The human gut mycobiome: Pitfalls and potentials – a mycologist’s perspective. Mycologia, 107, 1057–1073.PubMedPubMedCentralCrossRefGoogle Scholar
  110. Suhr, M. J., Banjara, N., & Hallen-Adams, H. E. (2016). Sequence-based methods for detecting and evaluating the human gut mycobiome. Letters in Applied Microbiology, 62, 209–215.PubMedCrossRefGoogle Scholar
  111. Tanaka, H., Hashiba, H., Kok, J., & Mierau, I. (2000). Bile salt hydrolase of Bifidobacterium longum-biochemical and genetic characterization. Applied and Environmental Microbiology, 66, 2502–2512.PubMedPubMedCentralCrossRefGoogle Scholar
  112. Tang, C., Ahmed, K., Gille, A., Lu, S., Grone, H. J., Tunaru, S., & Offermanns, S. (2015). Loss of FFA2 and FFA3 increases insulin secretion and improves glucose tolerance in type 2 diabetes. Nature Medicine, 21, 173–177.PubMedCrossRefGoogle Scholar
  113. Tasse, L., Bercovici, J., Pizzut-Serin, S., Robe, P., Tap, J., Klopp, C., Cantarel, B. L., Coutinho, P. M., Henrissat, B., Leclerc, M., et al. (2010). Functional metagenomics to mine the human gut microbiome for dietary fiber catabolic enzymes. Genome Research, 20, 1605–1612.PubMedPubMedCentralCrossRefGoogle Scholar
  114. Tazoe, H., Otomo, Y., Kaji, I., Tanaka, R., Karaki, S. I., & Kuwahara, A. (2008). Roles of short-chain fatty acids receptors, GPR41 and GPR43 on colonic functions. Journal of Physiology and Pharmacology, 59(Suppl 2), 251–262.PubMedGoogle Scholar
  115. Tolhurst, G., Heffron, H., Lam, Y. S., Parker, H. E., Habib, A. M., Diakogiannaki, E., Cameron, J., Grosse, J., Reimann, F., & Gribble, F. M. (2012). Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes, 61, 364–371.PubMedPubMedCentralCrossRefGoogle Scholar
  116. Topping, D. L., & Clifton, P. M. (2001). Short-chain fatty acids and human colonic function: Roles of resistant starch and nonstarch polysaccharides. Physiological Reviews, 81, 1031–1064.PubMedCrossRefGoogle Scholar
  117. Turnbaugh, P. J., Hamady, M., Yatsunenko, T., Cantarel, B. L., Duncan, A., Ley, R. E., Sogin, M. L., Jones, W. J., Roe, B. A., Affourtit, J. P., et al. (2009). A core gut microbiome in obese and lean twins. Nature, 457, 480–484.CrossRefGoogle Scholar
  118. Wang, J., Linnenbrink, M., Kunzel, S., Fernandes, R., Nadeau, M. J., Rosenstiel, P., & Baines, J. F. (2014). Dietary history contributes to enterotype-like clustering and functional metagenomic content in the intestinal microbiome of wild mice. Proceedings of the National Academy of Sciences of the United States of America, 111, E2703–E2710.PubMedPubMedCentralCrossRefGoogle Scholar
  119. Winter, S. E., Winter, M. G., Xavier, M. N., Thiennimitr, P., Poon, V., Keestra, A. M., Laughlin, R. C., Gomez, G., Wu, J., Lawhon, S. D., et al. (2013). Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science, 339, 708–711.PubMedPubMedCentralCrossRefGoogle Scholar
  120. Wolin, M. J., & Miller, T. L. (1983). Carbohydrate fermentation. In D. J. Hentges (Ed.), Human intestinal microflora in health and disease (p. 19). New York, London: Academic Press.Google Scholar
  121. Worsoe, J., Fynne, L., Gregersen, T., Schlageter, V., Christensen, L. A., Dahlerup, J. F., Rijkhoff, N. J., Laurberg, S., & Krogh, K. (2011). Gastric transit and small intestinal transit time and motility assessed by a magnet tracking system. BMC Gastroenterology, 11, 145.PubMedCrossRefGoogle Scholar
  122. Woting, A., Clavel, T., Loh, G., & Blaut, M. (2010). Bacterial transformation of dietary lignans in gnotobiotic rats. FEMS Microbiology Ecology, 72, 507–514.PubMedCrossRefGoogle Scholar
  123. Wren, A. M., & Bloom, S. R. (2007). Gut hormones and appetite control. Gastroenterology, 132, 2116–2130.PubMedCrossRefGoogle Scholar
  124. Wu, G. D., Chen, J., Hoffmann, C., Bittinger, K., Chen, Y. Y., Keilbaugh, S. A., Bewtra, M., Knights, D., Walters, W. A., Knight, R., et al. (2011). Linking long-term dietary patterns with gut microbial enterotypes. Science, 334, 105–108.PubMedPubMedCentralCrossRefGoogle Scholar
  125. Xiong, Y., Miyamoto, N., Shibata, K., Valasek, M. A., Motoike, T., Kedzierski, R. M., & Yanagisawa, M. (2004). Short-chain fatty acids stimulate leptin production in adipocytes through the G protein-coupled receptor GPR41. Proceedings of the National Academy of Sciences of the United States of America, 101, 1045–1050.PubMedPubMedCentralCrossRefGoogle Scholar
  126. Xu, J., Mahowald, M. A., Ley, R. E., Lozupone, C. A., Hamady, M., Martens, E. C., Henrissat, B., Coutinho, P. M., Minx, P., Latreille, P., et al. (2007). Evolution of symbiotic bacteria in the distal human intestine. PLoS Biology, 5, e156.PubMedPubMedCentralCrossRefGoogle Scholar
  127. Yao, C. K., Muir, J. G., & Gibson, P. R. (2016). Review article: Insights into colonic protein fermentation, its modulation and potential health implications. Alimentary Pharmacology & Therapeutics, 43, 181–196.CrossRefGoogle Scholar
  128. Ze, X., Duncan, S. H., Louis, P., & Flint, H. J. (2012). Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon. The ISME Journal, 6, 1535–1543.PubMedPubMedCentralCrossRefGoogle Scholar
  129. Zoetendal, E. G., Raes, J., van den Bogert, B., Arumugam, M., Booijink, C. C., Troost, F. J., Bork, P., Wels, M., de Vos, W. M., & Kleerebezem, M. (2012). The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. The ISME Journal, 6, 1415–1426.PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Gastrointestinal MicrobiologyGerman Institute of Human Nutrition Potsdam-Rehbruecke (DIfE)NuthetalGermany

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