Introduction to the human gut microbiota

Elizabeth Thursby, Nathalie Juge, Elizabeth Thursby, Nathalie Juge

Abstract

The human gastrointestinal (GI) tract harbours a complex and dynamic population of microorganisms, the gut microbiota, which exert a marked influence on the host during homeostasis and disease. Multiple factors contribute to the establishment of the human gut microbiota during infancy. Diet is considered as one of the main drivers in shaping the gut microbiota across the life time. Intestinal bacteria play a crucial role in maintaining immune and metabolic homeostasis and protecting against pathogens. Altered gut bacterial composition (dysbiosis) has been associated with the pathogenesis of many inflammatory diseases and infections. The interpretation of these studies relies on a better understanding of inter-individual variations, heterogeneity of bacterial communities along and across the GI tract, functional redundancy and the need to distinguish cause from effect in states of dysbiosis. This review summarises our current understanding of the development and composition of the human GI microbiota, and its impact on gut integrity and host health, underlying the need for mechanistic studies focusing on host-microbe interactions.

Keywords: gastrointestinal tract; gut microbiota; symbiosis.

Conflict of interest statement

The Authors declare that there are no competing interests associated with the manuscript.

© 2017 The Author(s).

References

    1. Bengmark S. (1998) Ecological control of the gastrointestinal tract. The role of probiotic flora. Gut 42, 2–7 doi:10.1136/gut.42.1.2
    1. Backhed F. (2005) Host-bacterial mutualism in the human intestine. Science 307, 1915–1920 doi:10.1126/science.1104816
    1. Neish A.S. (2009) Microbes in gastrointestinal health and disease. Gastroenterology 136, 65–80 doi:10.1053/j.gastro.2008.10.080
    1. Gill S.R., Pop M., DeBoy R.T., Eckburg P.B., Turnbaugh P.J., Samuel B.S. et al. (2006) Metagenomic analysis of the human distal gut microbiome. Science 312, 1355–1359 doi:10.1126/science.1124234
    1. Sender R., Fuchs S. and Milo R. (2016) Revised estimates for the number of human and bacteria cells in the body. bioRxiv
    1. Luckey T.D. (1972) Introduction to intestinal microecology. Am. J. Clin. Nutr. 25, 1292–1294
    1. Natividad J.M.M. and Verdu E.F. (2013) Modulation of intestinal barrier by intestinal microbiota: Pathological and therapeutic implications. Pharmacol. Res. 69, 42–51 doi:10.1016/j.phrs.2012.10.007
    1. den Besten G., van Eunen K., Groen A.K., Venema K., Reijngoud D.-J., Bakker B.M. (2013) The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 54, 2325–2340 doi:10.1194/jlr.R036012
    1. Bäumler A.J. and Sperandio V. (2016) Interactions between the microbiota and pathogenic bacteria in the gut. Nature 535, 85–93 doi:10.1038/nature18849
    1. Gensollen T., Iyer S.S., Kasper D.L., Blumberg R.S. (2016) How colonization by microbiota in early life shapes the immune system. Science 352, 539–544 doi:10.1126/science.aad9378
    1. Chang C. and Lin H. (2016) Dysbiosis in gastrointestinal disorders. Best Pract. Res. Clin. Gastroenterol. 30, 3–15 doi:10.1016/j.bpg.2016.02.001
    1. Schroeder B.O. and Bäckhed F. (2016) Signals from the gut microbiota to distant organs in physiology and disease. Nat. Med. 22, 1079–1089 doi:10.1038/nm.4185
    1. Moore W.E.C. and Holdeman L.V. (1974) Human fecal flora - normal flora of 20 Japanese-hawaiians. Appl. Microbiol. 27, 961–979
    1. Poretsky R., Rodriguez-R L.M., Luo C., Tsementzi D., Konstantinidis K.T., Rodriguez-Valera F. (2014) Strengths and limitations of 16S rRNA gene amplicon sequencing in revealing temporal microbial community dynamics. PLoS ONE 9, e93827 doi:10.1371/journal.pone.0093827
    1. Mizrahi-Man O., Davenport E.R., Gilad Y., and White B.A. (2013) Taxonomic classification of bacterial 16S rRNA genes using short sequencing reads: evaluation of effective study designs. PLoS ONE 8, e53608 doi:10.1371/journal.pone.0053608
    1. Suau A., et al. (1999) Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl. Environ. Microbiol. 65, 4799–4807
    1. Hugon P., Dufour J.-C., Colson P., Fournier P.-E., Sallah K., Raoult D. (2015) A comprehensive repertoire of prokaryotic species identified in human beings. Lancet Infect. Dis. 15, 1211–1219 doi:10.1016/S1473-3099(15)00293-5
    1. Li J., Jia H., Cai X., Zhong H., Feng Q., Sunagawa S. et al. (2014) An integrated catalog of reference genes in the human gut microbiome. Nat. Biotechnol. 32, 834–841 doi:10.1038/nbt.2942
    1. Schluter J., Foster K.R., Ellner S.P. (2012) The evolution of mutualism in gut microbiota via host epithelial selection. PLoS Biol. 10, e1001424 doi:10.1371/journal.pbio.1001424
    1. Costello E.K., Lauber C.L., Hamady M., Fierer N., Gordon J.I., Knight R. (2009) Bacterial community variation in human body habitats across space and time. Science 326, 1694–1697 doi:10.1126/science.1177486
    1. Pérez-Cobas A.E., Gosalbes M.J., Friedrichs A., Knecht H., Artacho A., Eismann K. et al. (2013) Gut microbiota disturbance during antibiotic therapy: a multi-omic approach. Gut 62, 1591–1601 doi:10.1136/gutjnl-2012-303184
    1. Moya A. and Ferrer M. (2016) Functional redundancy-Induced stability of Gut microbiota subjected to disturbance. Trends Microbiol. 24, 402–413 doi:10.1016/j.tim.2016.02.002
    1. Aagaard K., Ma J., Antony K.M., Ganu R., Petrosino J., Versalovic J. (2014) The placenta harbors a unique microbiome. Sci. Transl. Med. 6, 237ra65 doi:10.1126/scitranslmed.3008599
    1. Rodriguez J.M., et al. (2015) The composition of the gut microbiota throughout life, with an emphasis on early life. Microb. Ecol. Health Dis. 26, 26050.
    1. Koenig J.E., Spor A., Scalfone N., Fricker A.D., Stombaugh J., Knight R. et al. (2011) Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl. Acad. Sci. U.S.A. 108(Suppl 1), 4578–4585 doi:10.1073/pnas.1000081107
    1. Avershina E., Storrø O., Øien T., Johnsen R., Pope P., Rudi K. (2014) Major faecal microbiota shifts in composition and diversity with age in a geographically restricted cohort of mothers and their children. FEMS Microbiol. Ecol. 87, 280–290 doi:10.1111/1574-6941.12223
    1. Aagaard K., Riehle K., Ma J., Segata N., Mistretta T.-A., Coarfa C. et al. (2012) A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLoS ONE 7, e36466 doi:10.1371/journal.pone.0036466
    1. Jakobsson H.E., Abrahamsson T.R., Jenmalm M.C., Harris K., Quince C., Jernberg C. et al. (2014) Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut 63, 559–566 doi:10.1136/gutjnl-2012-303249
    1. Salminen S. (2004) Influence of mode of delivery on gut microbiota composition in seven year old children. Gut 53, 1388–1389 doi:10.1136/gut.2004.041640
    1. Backhed F., Roswall J., Peng Y., Feng Q., Jia H., Kovatcheva-Datchary P. et al. (2015) Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17, 852 doi:10.1016/j.chom.2015.05.012
    1. Bäckhed F. (2011) Programming of host metabolism by the gut microbiota. Ann. Nutr. Metab. 58(Suppl 2), 44–52 doi:10.1159/000328042
    1. Palmer C., Bik E.M., DiGiulio D.B., Relman D.A., Brown P.O., Ruan Y. (2007) Development of the human infant intestinal microbiota. PLoS Biol. 5, e177 doi:10.1371/journal.pbio.0050177
    1. Dethlefsen L. and Relman D.A. (2011) Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc. Natl. Acad. Sci. U.S.A. 108, 4554–4561 doi:10.1073/pnas.1000087107
    1. Claesson M.J., Cusack S., O'Sullivan O., Greene-Diniz R., de Weerd H., Flannery E. et al. (2011) Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc. Natl. Acad. Sci. U.S.A. 108(Supplement 1), 4586–4591 doi:10.1073/pnas.1000097107
    1. Biagi E., Nylund L., Candela M., Ostan R., Bucci L., Pini E. et al. (2010) Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLoS ONE 5, e10667 doi:10.1371/journal.pone.0010667
    1. Claesson M.J., et al. (2012) Gut microbiota composition correlates with diet and health in the elderly. Nature 488, 178–+
    1. Woodmansey E.J., McMurdo M.E.T., Macfarlane G.T., Macfarlane S. (2004) Comparison of compositions and metabolic activities of fecal microbiotas in young adults and in antibiotic-treated and non-antibiotic-treated elderly subjects. Appl. Environ. Microbiol. 70, 6113–6122 doi:10.1128/AEM.70.10.6113-6122.2004
    1. Biagi E., Candela M., Turroni S., Garagnani P., Franceschi C., Brigidi P. (2013) Ageing and gut microbes: perspectives for health maintenance and longevity. Pharmacol. Res. 69, 11–20 doi:10.1016/j.phrs.2012.10.005
    1. Macpherson A.J. and McCoy K.D. (2013) Stratification and compartmentalisation of immunoglobulin responses to commensal intestinal microbes. Semin. Immunol. 25, 358–363 doi:10.1016/j.smim.2013.09.004
    1. Donaldson G.P., Lee S.M. and Mazmanian S.K. (2015) Gut biogeography of the bacterial microbiota. Nat. Rev. Microbiol. 14, 20–32 doi:10.1038/nrmicro3552
    1. Gu S., Chen D., Zhang J.-N., Lv X., Wang K., Duan L.-P. et al. (2013) Bacterial community mapping of the mouse gastrointestinal tract. PLoS ONE 8, e74957 doi:10.1371/journal.pone.0074957
    1. Eckburg P.B. (2005) Diversity of the human intestinal microbial flora. Science 308, 1635–1638 doi:10.1126/science.1110591
    1. Lavelle A., et al. (2015) Spatial variation of the colonic microbiota in patients with ulcerative colitis and control volunteers. Gut
    1. Van den Abbeele P., Belzer C., Goossens M., Kleerebezem M., De Vos W.M., Thas O. et al. (2013) Butyrate-producing Clostridium cluster XIVa species specifically colonize mucins in an in vitro gut model. ISME J. 7, 949–961 doi:10.1038/ismej.2012.158
    1. Li H., Limenitakis J.P., Fuhrer T., Geuking M.B., Lawson M.A., Wyss M. et al. (2015) The outer mucus layer hosts a distinct intestinal microbial niche. Nat. Commun. 6, 8292 doi:10.1038/ncomms9292
    1. Turnbaugh P.J., Hamady M., Yatsunenko T., Cantarel B.L., Duncan A., Ley R.E. et al. (2009) A core gut microbiome in obese and lean twins. Nature 457, 480–484 doi:10.1038/nature07540
    1. Jakobsson H.E., Jernberg C., Andersson A.F., Sjölund-Karlsson M., Jansson J.K., Engstrand L. et al. (2010) Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PLoS ONE 5 doi:10.1371/journal.pone.0009836
    1. Ding T. and Schloss P.D. (2014) Dynamics and associations of microbial community types across the human body. Nature 509, 357–360 doi:10.1038/nature13178
    1. Arumugam M., Raes J., Pelletier E., Le Paslier D., Yamada T., Mende D.R. et al. (2011) Enterotypes of the human gut microbiome. Nature 473, 174–180 doi:10.1038/nature09944
    1. Jeffery I.B., Claesson M.J., O'Toole P.W., Shanahan F. (2012) Categorization of the gut microbiota: enterotypes or gradients? Nat. Rev. Microbiol. 10, 591–592 doi:10.1038/nrmicro2859
    1. Hooper L.V. and Macpherson A.J. (2010) Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat. Rev. Immunol. 10, 159–169 doi:10.1038/nri2710
    1. Ley R.E., Peterson D.A. and Gordon J.I. (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124, 837–848 doi:10.1016/j.cell.2006.02.017
    1. Travisano M. and Velicer G.J. (2004) Strategies of microbial cheater control. Trends Microbiol. 12, 72–78 doi:10.1016/j.tim.2003.12.009
    1. Zoetendal E.G. Raes J., van den Bogert B., Arumugam M., Booijink C.C.G.M., Troost F.J. et al. (2012) The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J. 6, 1415–1426 doi:10.1038/ismej.2011.212
    1. David L.A., Maurice C.F., Carmody R.N., Gootenberg D.B., Button J.E., Wolfe B.E. et al. (2013) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559–563 doi:10.1038/nature12820
    1. Walker A.W., Ince J., Duncan S.H., Webster L.M., Holtrop G., Ze X. et al. (2011) Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 5, 220–230 doi:10.1038/ismej.2010.118
    1. Yu Z.T., Chen C., Kling D.E., Liu B., McCoy J.M., Merighi M. et al. (2013) The principal fucosylated oligosaccharides of human milk exhibit prebiotic properties on cultured infant microbiota. Glycobiology 23, 169–177 doi:10.1093/glycob/cws138
    1. Marcobal A., Barboza M., Sonnenburg E.D., Pudlo N., Martens E.C., Desai P. et al. (2011) Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host Microbe 10, 507–514 doi:10.1016/j.chom.2011.10.007
    1. Bezirtzoglou E., Tsiotsias A. and Welling G.W. (2011) Microbiota profile in feces of breast- and formula-fed newborns by using fluorescence in situ hybridization (FISH). Anaerobe 17, 478–482 doi:10.1016/j.anaerobe.2011.03.009
    1. Penders J., Thijs C., Vink C., Stelma F.F., Snijders B., Kummeling I. et al. (2006) Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118, 511–521 doi:10.1542/peds.2005-2824
    1. Favier C.F., Vaughan E.E., De Vos W.M., Akkermans A.D.L. (2002) Molecular monitoring of succession of bacterial communities in human neonates. Appl. Environ. Microbiol. 68, 219–226 doi:10.1128/AEM.68.1.219-226.2002
    1. Kau A.L., et al. (2015) Functional characterization of IgA-targeted bacterial taxa from undernourished Malawian children that produce diet-dependent enteropathy. Sci. Transl. Med. 7, 276ra24
    1. De Filippo C., Cavalieri D., Di Paola M., Ramazzotti M., Poullet J.B., Massart S. 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. U.S.A. 107, 14691–14696 doi:10.1073/pnas.1005963107
    1. Wu G.D., Chen J., Hoffmann C., Bittinger K., Chen Y.-Y., Keilbaugh S.A. et al. (2011) Linking long-term dietary patterns with gut microbial enterotypes. Science 334, 105–108 doi:10.1126/science.1208344
    1. Sonnenburg E.D. and Sonnenburg J.L. (2014) Starving our microbial self: the deleterious consequences of a diet deficient in microbiota-accessible carbohydrates. Cell Metab. 20, 779–786 doi:10.1016/j.cmet.2014.07.003
    1. 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 doi:10.1038/nature16504
    1. Blanton L.V., Charbonneau M.R., Salih T., Barratt M.J., Venkatesh S., Ilkaveya O. et al. (2016) Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science 351, aad3311 doi:10.1126/science.aad3311
    1. Charbonneau M.R., O'Donnell D., Blanton L.V., Totten S.M., Davis J.C.C., Barratt M.J. et al. (2016) Sialylated milk oligosaccharides promote microbiota-Dependent growth in models of infant undernutrition. Cell 164, 859–871 doi:10.1016/j.cell.2016.01.024
    1. Schwarzer M., Makki K., Storelli G., Machuca-Gayet I., Srutkova D., Hermanova P. et al. (2016) Lactobacillus plantarum strain maintains growth of infant mice during chronic undernutrition. Science 351, 854–857 doi:10.1126/science.aad8588
    1. Tailford L.E., Owen C.D., Walshaw J., Crost E.H., Hardy-Goddard J., Le Gall G. et al. (2015) Discovery of intramolecular trans-sialidases in human gut microbiota suggests novel mechanisms of mucosal adaptation. Nat. Commun. 6, 7624 doi:10.1038/ncomms8624
    1. Arike L. and Hansson G.C. (2016) The densely O-glycosylated MUC2 mucin protects the intestine and provides food for the commensal bacteria. J. Mol. Biol
    1. Ouwerkerk J.P., de Vos W.M., Belzer B. (2013) Glycobiome: Bacteria and mucus at the epithelial interface. Best Pract. Res. Clin. Gastroenterol. 27, 25–38 doi:10.1016/j.bpg.2013.03.001
    1. Johansson M.E.V., Larsson J.M.H. and Hansson G.C. (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. U.S.A. 108(Suppl 1), 4659–4665 doi:10.1073/pnas.1006451107
    1. Gustafsson J.K., Ermund A., Johansson M.E.V., Schutte A., Hansson G.C., Sjovall H. (2012) An ex vivo method for studying mucus formation, properties, and thickness in human colonic biopsies and mouse small and large intestinal explants. Am. J. Physiol. Gastrointest. Liver Physiol. 302, G430–G438 doi:10.1152/ajpgi.00405.2011
    1. Johansson M.E., Jakobsson H.E., Holmén-Larsson J., Schütte A., Ermund A., Rodríguez-Piñeiro A.M. et al. (2015) Normalization of host intestinal mucus layers requires long-Term microbial colonization. Cell Host Microbe 18, 582–592 doi:10.1016/j.chom.2015.10.007
    1. Juge N. (2012) Microbial adhesins to gastrointestinal mucus. Trends Microbiol. 20, 30–39 doi:10.1016/j.tim.2011.10.001
    1. Tailford L.E., Crost E.H., Kavanaugh D., Juge N. (2015) Mucin glycan foraging in the human gut microbiome. Frontiers in Genetics. 6, 131 doi:10.3389/fgene.2015.00081
    1. Rausch P., Rehman A., Kunzel S., Hasler R., Ott S.J., Schreiber S. et al. (2011) Colonic mucosa-associated microbiota is influenced by an interaction of crohn disease and FUT2 (Secretor) genotype. Proc Natl Acad Sci U.S.A. 108, 19030–19035 doi:10.1073/pnas.1106408108
    1. Arpaia N., Campbell C., Fan X., Dikiy S., van der Veeken J., deRoos P. et al. (2013) Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 504, 451–455 doi:10.1038/nature12726
    1. Furusawa Y., Obata Y., Fukuda S., Endo T.A., Nakato G., Takahashi D. et al. (2013) Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 504, 446–450 doi:10.1038/nature12721
    1. Zarepour M., Bhullar K., Montero M., Ma C., Huang T., Velcich A. et al. (2013) The mucin MUC2 limits pathogen burdens and epithelial barrier dysfunction during salmonella enterica serovar typhimurium colitis. Infect Immun. 81, 3672–3683 doi:10.1128/IAI.00854-13
    1. Earle K.A., Billings G., Sigal M., Lichtman J.S., Hansson G.C., Elias J.E. et al. (2015) Quantitative imaging of gut microbiota spatial organization. Cell Host Microbe 18, 478–488 doi:10.1016/j.chom.2015.09.002
    1. Desai M.S., Seekatz A.M., Koropatkin N.M., Kamada N., Hickey C.A., Wolter M. et al. (2016) A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell. 167, 1339–1353.e21 doi:10.1016/j.cell.2016.10.043
    1. Everard A., Belzer C., Geurts L., Ouwerkerk J.P., Druart C., Bindels L.B. et al. (2013) Cross-talk between akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U.S.A. 110, 9066–9071 doi:10.1073/pnas.1219451110
    1. Li J., Lin S., Vanhoutte P.M., Woo C.W., Xu A. (2016) Akkermansia muciniphila protects against atherosclerosis by preventing metabolic endotoxemia-induced inflammation in apoe-/- mice. Circulation. 133, 2434–2446 doi:10.1161/CIRCULATIONAHA.115.019645
    1. Plovier H., Everard A., Druart C., Depommier C., Van Hul M., Geurts L. et al. (2016) A purified membrane protein from akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nat Med. 23, 107–113 doi:10.1038/nm.4236
    1. Zhao S., Liu W., Wang J., Shi J., Sun Y., Wang W. et al. (2017) Akkermansia muciniphila improves metabolic profiles by reducing inflammation in chow diet-fed mice. J Mol Endocrinol. 58, 1–14 doi:10.1530/JME-16-0054
    1. Cockburn D.W. and Koropatkin N.M. (2016) Polysaccharide degradation by the intestinal microbiota and its influence on human health and disease. J Mol Biol. 428, 3230–3252 doi:10.1016/j.jmb.2016.06.021
    1. El Kaoutari A., Armougom F., Gordon J.I., Raoult D., Henrissat B. (2013) The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nat Rev Microbiol. 11, 497–504 doi:10.1038/nrmicro3050
    1. Cantarel B.L., Lombard V., Henrissat B. and Appanna V.D. (2012) Complex carbohydrate utilization by the healthy human microbiome. PLoS One. 7, e28742 doi:10.1371/journal.pone.0028742
    1. Larsbrink J., Rogers T.E., Hemsworth G.R., McKee L.S., Tauzin A.S., Spadiut O. et al. (2014) A discrete genetic locus confers xyloglucan metabolism in select human gut bacteroidetes. Nature. 506, 498–502 doi:10.1038/nature12907
    1. Rogowski A., Briggs J.A., Mortimer J.C., Tryfona T., Terrapon N., Lowe E.C. et al. (2015) Glycan complexity dictates microbial resource allocation in the large intestine. Nat Commun. 6, 7481 doi:10.1038/ncomms8481
    1. Cuskin F., Lowe E.C., Temple M.J., Zhu Y., Cameron E.A., Pudlo N.A. et al. (2015) Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism. Nature. 517, 165–169 doi:10.1038/nature13995
    1. Tauzin A.S., Kwiatkowski K.J., Orlovsky N.I., Smith C.J., Creagh A.L., Haynes C.A. et al. (2016) Molecular dissection of xyloglucan recognition in a prominent human Gut symbiont. MBio. 7, e02134–15 doi:10.1128/mBio.02134-15
    1. Foley M.H., Cockburn D.W. and Koropatkin N.M. (2016) The Sus operon: a model system for starch uptake by the human gut bacteroidetes. Cell Mol Life Sci. 73, 2603–2617 doi:10.1007/s00018-016-2242-x
    1. Glenwright A.J., Pothula K.R., Bhamidimarri S.P., Chorev D.S., Baslé A., Firbank S.J. et al. (2017) Structural basis for nutrient acquisition by dominant members of the human gut microbiota. Nature. 541, 407–411 doi:10.1038/nature20828
    1. Ze X., et al. (2015) Unique organization of extracellular amylases into amylosomes in the resistant starch-utilizing human colonic firmicutes bacterium Ruminococcus bromii. MBio. 6, e01058–15
    1. Bjedov I. (2003) Stress-induced mutagenesis in bacteria. Science. 300, 1404–1409 doi:10.1126/science.1082240
    1. Xu J., et al. (2007) Evolution of symbiotic bacteria in the distal human intestine. PLoS Biol. 5, 1574–1586
    1. Svanback R. and Bolnick D.I. (2007) Intraspecific competition drives increased resource use diversity within a natural population. Proceedings of the Royal Society B-Biological Sciences. 274, 839–844 doi:10.1098/rspb.2006.0198
    1. Emerson B.C. and Kolm N. (2005) Species diversity can drive speciation. Nature 434, 1015–1017 doi:10.1038/nature03450
    1. Louis P. and Flint H.J. (2016) Formation of propionate and butyrate by the human colonic microbiota. Environ Microbiol
    1. 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. ISME J 6, 1535–1543 doi:10.1038/ismej.2012.4
    1. Louis P., Scott K.P., Duncan S.H. and Flint H.J. (2007) Understanding the effects of diet on bacterial metabolism in the large intestine. Journal of Applied Microbiology 102, 1197–1208 doi:10.1111/j.1365-2672.2007.03322.x
    1. Duncan S.H., Louis P. and Flint H.J. (2004) Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl Environ Microbiol 70, 5810–5817 doi:10.1128/AEM.70.10.5810-5817.2004
    1. Rakoff-Nahoum S., Foster K.R. and Comstock L.E. (2016) The evolution of cooperation within the gut microbiota. Nature 533, 255–259 doi:10.1038/nature17626
    1. Juge N., Tailford L. and Owen C.D. (2016) Sialidases from gut bacteria: a mini-review. Biochem Soc Trans 44, 166–175 doi:10.1042/BST20150226
    1. Crost E.H., Tailford L.E., Le Gall G., Fons M., Henrissat B., Juge N. et al. (2013) Utilisation of mucin glycans by the human Gut symbiont ruminococcus gnavus Is strain-Dependent. PLoS One 8, e76341 doi:10.1371/journal.pone.0076341
    1. Crost E.H., et al. (2016) The mucin-degradation strategy of ruminococcus gnavus: The importance of intramolecular trans-sialidases. Gut Microbes 1–11
    1. Larsson J.M.H., Karlsson H., Crespo J.G., Johansson M.E.V., Eklund L., Sjövall H. et al. (2011) Altered o-glycosylation profile of MUC2 mucin occurs in active ulcerative colitis and is associated with increased inflammation. Inflamm Bowel Dis 17, 2299–2307 doi:10.1002/ibd.21625
    1. 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. Front Physiol 3, 448 doi:10.3389/fphys.2012.00448
    1. Ridlon J.M., Kang D.J., Hylemon P.B., Bajaj J.S. (2014) Bile acids and the gut microbiome. Curr Opin Gastroenterol 30, 332–338 doi:10.1097/MOG.0000000000000057
    1. Staley C., Weingarden A.R., Khoruts A., Sadowsky M.J. (2017) Interaction of gut microbiota with bile acid metabolism and its influence on disease states. Appl Microbiol Biotechnol 101, 47–64 doi:10.1007/s00253-016-8006-6
    1. Browne H.P., Forster S.C., Anonye B.O., Kumar N., Neville B.A., Stares M.D. et al. (2016) Culturing of 'unculturable' human microbiota reveals novel taxa and extensive sporulation. Nature 533, 543–546 doi:10.1038/nature17645
    1. Kakiyama G., Pandak W.M., Gillevet P.M., Hylemon P.B., Heuman D.M., Daita K. et al. (2013) Modulation of the fecal bile acid profile by gut microbiota in cirrhosis. J Hepatol 58, 949–955 doi:10.1016/j.jhep.2013.01.003
    1. Hooper L.V., Littman D.R. and Macpherson A.J. (2012) Interactions between the microbiota and the immune system. Science 336, 1268–1273 doi:10.1126/science.1223490
    1. Macpherson A.J. (2000) A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 288, 2222–2226 doi:10.1126/science.288.5474.2222
    1. Macpherson A.J. and Uhr T. (2004) Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 303, 1662–1665 doi:10.1126/science.1091334
    1. Cash H.L. (2006) Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313, 1126–1130 doi:10.1126/science.1127119
    1. McGuckin M.A., Lindén S.K., Sutton P. and Florin T.H. (2011) Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9, 265–278 doi:10.1038/nrmicro2538
    1. Meyer-Hoffert U., Hornef M.W., Henriques-Normark B., Axelsson L.-G., Midtvedt T., Putsep K. et al. (2008) Secreted enteric antimicrobial activity localises to the mucus surface layer. Gut 57, 764–771 doi:10.1136/gut.2007.141481
    1. Wehkamp J. (2004) NOD2 (CARD15) mutations in crohn's disease are associated with diminished mucosal alpha-defensin expression. Gut 53, 1658–1664 doi:10.1136/gut.2003.032805
    1. Wehkamp J., Salzman N.H., Porter E., Nuding S., Weichenthal M., Petras R.E. et al. (2005) Reduced paneth cell alpha-defensins in ileal crohn's disease. Proc Natl Acad Sci U.S.A 102, 18129–18134 doi:10.1073/pnas.0505256102
    1. Rogier E.W., Frantz A., Bruno M. and Kaetzel C. (2014) Secretory IgA is concentrated in the outer layer of colonic mucus along with gut bacteria. Pathogens 3, 390–403 doi:10.3390/pathogens3020390
    1. Bollinger R.R.., Everett M.L., Palestrant D., Love S.D., Lin S.S. and Parker W. (2003) Human secretory immunoglobulin A May contribute to biofilm formation in the gut. Immunology 109, 580–587 doi:10.1046/j.1365-2567.2003.01700.x
    1. Friman V., et al. (1996) Decreased expression of mannose-specific adhesins by Escherichia coli in the colonic microflora of immunoglobulin A-deficient individuals. Infect Immun 64, 2794–2798
    1. Suzuki K., Meek B., Doi Y., Muramatsu M., Chiba T., Honjo T. et al. (2004) Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut. Proc Natl Acad Sci U.S.A. 101, 1981–1986 doi:10.1073/pnas.0307317101
    1. Biedermann L., Zeitz J., Mwinyi J., Sutter-Minder E., Rehman A., Ott S.J. et al. (2013) Smoking cessation induces profound changes in the composition of the intestinal microbiota in humans. PLoS One 8, e59260 doi:10.1371/journal.pone.0059260
    1. Jiang H., Ling Z., Zhang Y., Mao H., Ma Z., Yin Y. et al. (2015) Altered fecal microbiota composition in patients with major depressive disorder. Brain Behavior and Immunity 48, 186–194 doi:10.1016/j.bbi.2015.03.016
    1. Tyakht A.V., Kostryukova E.S., Popenko A.S., Belenikin M.S., Pavlenko A.V., Larin A.K. et al. (2013) Human gut microbiota community structures in urban and rural populations in russia. Nature Commun 4, 2469 doi:10.1038/ncomms3469
    1. Maurice C.F., Haiser H.J. and Turnbaugh P.J. (2013) Xenobiotics shape the physiology and gene expression of the active human gut microbiome. Cell 152, 39–50 doi:10.1016/j.cell.2012.10.052
    1. Jernberg C., Löfmark S., Edlund C. and Jansson J.K. (2007) Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J 1, 56–66 doi:10.1038/ismej.2007.3
    1. Ferrer M., Martins dos Santos V.A.P., Ott S.J. and Moya A. (2014) Gut microbiota disturbance during antibiotic therapy: a multi-omic approach. Gut Microbes 5, 64–70 doi:10.4161/gmic.27128
    1. Ge X., Ding C., Zhao W., Xu L., Tian H., Gong J. et al. (2017) Antibiotics-induced depletion of mice microbiota induces changes in host serotonin biosynthesis and intestinal motility. J Transl Med 15, 13 doi:10.1186/s12967-016-1105-4
    1. Ng K.M., Ferreyra J.A., Higginbottom S.K., Lynch J.B., Kashyap P.C., Gopinath S. et al. (2013) Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502, 96–99 doi:10.1038/nature12503
    1. Musso G., Gambino R. and Cassader M. (2010) Obesity, diabetes, and gut microbiota: The hygiene hypothesis expanded? Diabetes Care 33, 2277–2284 doi:10.2337/dc10-0556
    1. Louis P., Hold G.L. and Flint H.J. (2014) The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol 12, 661–672 doi:10.1038/nrmicro3344
    1. Corrêa-Oliveira R., Fachi J.L., Vieira A., Sato F.T. and Vinolo M.A.R. (2016) Regulation of immune cell function by short-chain fatty acids. Clin Transl Immunol 5, e73 doi:10.1038/cti.2016.17
    1. Macfarlane S. and Macfarlane G.T. (2003) Regulation of short-chain fatty acid production. Proc Nutr Soc 62, 67–72 doi:10.1079/PNS2002207
    1. Morrison D.J. and Preston T. (2016) Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes 7, 189–200 doi:10.1080/19490976.2015.1134082
    1. Derrien M. (2004) Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 54(Pt 5), 1469–1476 doi:10.1099/ijs.0.02873-0
    1. Guarner F. and Malagelada J.R. (2003) Gut flora in health and disease. Lancet 361, 512–519 doi:10.1016/S0140-6736(03)12489-0
    1. Lin L. and Zhang J. (2017) Role of intestinal microbiota and metabolites on gut homeostasis and human diseases. BMC Immunol. 18
    1. Donohoe D.R., Collins L.B., Wali A., Bigler R., Sun W. and Bultman S.J. (2012) The warburg effect dictates the mechanism of butyrate-mediated histone acetylation and cell proliferation. Mol Cell. 48, 612–626 doi:10.1016/j.molcel.2012.08.033
    1. Chambers E.S., Morrison D.J. and Frost G. (2015) Control of appetite and energy intake by SCFA: what are the potential underlying mechanisms? Proc Nutr Soc. 74, 328–336 doi:10.1017/S0029665114001657
    1. Pingitore A., et al. (2016) The diet-derived short chain fatty acid propionate improves beta-cell function in humans and stimulates insulin secretion from human islets in vitro. Diabetes Obes. Metab. 19, 257–265 doi:10.1111/dom.12811
    1. Byrne C.S., Chambers E.S., Alhabeeb H., Chhina N., Morrison D.J., Preston T. et al. (2016) Increased colonic propionate reduces anticipatory reward responses in the human striatum to high-energy foods. Am J Clin Nutr. 104, 5–14 doi:10.3945/ajcn.115.126706
    1. Nagai M., Obata Y., Takahashi D. and Hase K. (2016) Fine-tuning of the mucosal barrier and metabolic systems using the diet-microbial metabolite axis. Int Immunopharmacol. 37, 79–86 doi:10.1016/j.intimp.2016.04.001
    1. LeBlanc J.G., Milani C., de Giori G.S., Sesma F., van Sinderen D. and Ventura M. (2013) Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Current Opinion in Biotechnology. 24, 160–168 doi:10.1016/j.copbio.2012.08.005
    1. Martens J.H., Barg H., Warren M. and Jahn D. (2002) Microbial production of vitamin B-12. Applied Microbiology and Biotechnology. 58, 275–285 doi:10.1007/s00253-001-0902-7
    1. Pompei A., Cordisco L., Amaretti A., Zanoni S., Matteuzzi D. and Rossi M. (2007) Folate production by bifidobacteria as a potential probiotic property. Appl Environ Microbiol. 73, 179–185 doi:10.1128/AEM.01763-06
    1. Hill M.J. (1997) Intestinal flora and endogenous vitamin synthesis. European Journal of Cancer Prevention. 6, S43–S45 doi:10.1097/00008469-199703001-00009
    1. Palau-Rodriguez M., Tulipani S., Isabel Queipo-Ortuño M., Urpi-Sarda M., Tinahones F.J. and Andres-Lacueva C. (2015) Metabolomic insights into the intricate gut microbial-host interaction in the development of obesity and type 2 diabetes. Front Microbiol. 6, 1151 doi:10.3389/fmicb.2015.01151
    1. Smith K., McCoy K.D. and Macpherson A.J. (2007) Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Seminars in Immunology. 19, 59–69 doi:10.1016/j.smim.2006.10.002
    1. Swanson P.A. II, Kumar A., Samarin S., Vijay-Kumar M., Kundu K., Murthy N. et al. (2011) Enteric commensal bacteria potentiate epithelial restitution via reactive oxygen species-mediated inactivation of focal adhesion kinase phosphatases. Proc Natl Acad Sci U.S.A. 108, 8803–8808 doi:10.1073/pnas.1010042108
    1. Reunanen J., et al. (2015) Akkermansia muciniphila adheres to enterocytes and strengthens the integrity of epithelial cell layer. Appl Environ Microbiol
    1. Chen H.Q., Yang J., Zhang M., Zhou Y.-K., Shen T.-Y., Chu Z.-X. et al. (2010) Lactobacillus plantarum ameliorates colonic epithelial barrier dysfunction by modulating the apical junctional complex and PepT1 in IL-10 knockout mice. Am J Physiol Gastrointest Liver Physiol. 299, G1287–G1297 doi:10.1152/ajpgi.00196.2010
    1. Petersson J., Schreiber O., Hansson G.C., Gendler S.J., Velcich A., Lundberg J.O. et al. (2011) Importance and regulation of the colonic mucus barrier in a mouse model of colitis. Am J Physiol Gastrointest Liver Physiol. 300, G327–G333 doi:10.1152/ajpgi.00422.2010
    1. Wrzosek L., Miquel S., Noordine M.-L., Bouet S., Chevalier-Curt M., Robert V. et al. (2013) Bacteroides thetaiotaomicron and faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent. BMC Biol. 11, 61 doi:10.1186/1741-7007-11-61
    1. Graziani F., Pujol A., Nicoletti C., Dou S., Maresca M., Giardina T. et al. (2016) Ruminococcus gnavus E1 modulates mucin expression and intestinal glycosylation. J Appl Microbiol. 120, 1403–1417 doi:10.1111/jam.13095
    1. Varyukhina S., Freitas M., Bardin S., Robillard E., Tavan E., Sapin C. et al. (2012) Glycan-modifying bacteria-derived soluble factors from bacteroides thetaiotaomicron and lactobacillus casei inhibit rotavirus infection in human intestinal cells. Microbes Infect. 14, 273–278 doi:10.1016/j.micinf.2011.10.007
    1. Freitas M., Cayuela C., Antoine J.-M., Piller F., Sapin C. and Trugnan G. (2001) A heat labile soluble factor from bacteroides thetaiotaomicron VPI-5482 specifically increases the galactosylation pattern of HT29-MTX cells. Cell Microbiol. 3, 289–300 doi:10.1046/j.1462-5822.2001.00113.x
    1. Mazmanian S.K., Liu C.H., Tzianabos A.O. and Kasper D.L. (2005) An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell. 122, 107–118 doi:10.1016/j.cell.2005.05.007
    1. Hevia A., Delgado S., Sánchez B. and Margolles A. (2015) Molecular players involved in the interaction between beneficial bacteria and the immune system. Front Microbiol. 6, 1285 doi:10.3389/fmicb.2015.01285
    1. Schnupf P., Gaboriau-Routhiau V., Gros M., Friedman R., Moya-Nilges M., Nigro G. et al. (2015) Growth and host interaction of mouse segmented filamentous bacteria in vitro. Nature. 520, 99–103 doi:10.1038/nature14027
    1. Candela M., Biagi E., Maccaferri S., Turroni S. and Brigidi P. (2012) Intestinal microbiota is a plastic factor responding to environmental changes. Trends Microbiol. 20, 385–391 doi:10.1016/j.tim.2012.05.003
    1. Ellekilde M., Krych L., Hansen C.H.F., Hufeldt M.R., Dahl K., Hansen L.H. et al. (2014) Characterization of the gut microbiota in leptin deficient obese mice - correlation to inflammatory and diabetic parameters. Res Vet Sci. 96, 241–250 doi:10.1016/j.rvsc.2014.01.007
    1. Hansen C.H., Krych L., Nielsen D.S., Vogensen F.K., Hansen L.H., Sørensen S.J. et al. (2012) Early life treatment with vancomycin propagates akkermansia muciniphila and reduces diabetes incidence in the NOD mouse. Diabetologia. 55, 2285–2294 doi:10.1007/s00125-012-2564-7
    1. Le Chatelier E., Nielsen T., Qin J., Prifti E., Hildebrand F., Falony G. et al. (2013) Richness of human gut microbiome correlates with metabolic markers. Nature. 500, 541–546 doi:10.1038/nature12506
    1. Wang L., Christophersen C.T., Sorich M.J., Gerber J.P., Angley M.T. and Conlon M.A. (2011) Low relative abundances of the mucolytic bacterium akkermansia muciniphila and bifidobacterium spp. in feces of children with autism. Appl Environ Microbiol. 77, 6718–6721 doi:10.1128/AEM.05212-11
    1. Derrien M., Belzer C. and de Vos W.M. (2016) Akkermansia muciniphila and its role in regulating host functions. Microb. Pathog. doi:10.1016/j.micpath.2016.02.005
    1. Sokol H., Seksik P., Furet J.P., Firmesse O., Nion-Larmurier I., Beaugerie L. et al. (2009) Low counts of faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis. 15, 1183–1189 doi:10.1002/ibd.20903
    1. Lopez-Siles M., et al. (2017) Faecalibacterium prausnitzii: from microbiology to diagnostics and prognostics. ISME J. doi:10.1038/ismej.2016.176
    1. Quévrain E., Maubert M.A., Michon C., Chain F., Marquant R., Tailhades J. et al. (2016) Identification of an anti-inflammatory protein from faecalibacterium prausnitzii, a commensal bacterium deficient in crohn's disease. Gut. 65, 415–425 doi:10.1136/gutjnl-2014-307649
    1. Ferreyra J.A., Wu K.J., Hryckowian A.J., Bouley D.M., Weimer B.C., Sonnenburg J.L. et al. (2014) Gut microbiota-produced succinate promotes C. difficile infection after antibiotic treatment or motility disturbance. Cell Host Microbe 16, 770–777 doi:10.1016/j.chom.2014.11.003
    1. Huang Y.L., Chassard C., Hausmann M., von Itzstein M. and Hennet T. (2015) Sialic acid catabolism drives intestinal inflammation and microbial dysbiosis in mice. Nat Commun. 6, 8141 doi:10.1038/ncomms9141
    1. Mathias A., Pais B., Favre L., Benyacoub J. and Corthésy B. (2014) Role of secretory IgA in the mucosal sensing of commensal bacteria. Gut Microbes. 5, 688–695 doi:10.4161/19490976.2014.983763
    1. Rios D., Wood M.B., Li J., Chassaing B., Gewirtz A.T. and Williams I.R. (2016) Antigen sampling by intestinal M cells is the principal pathway initiating mucosal IgA production to commensal enteric bacteria. Mucosal Immunol. 9, 907–916 doi:10.1038/mi.2015.121
    1. Jandhyala S.M. (2015) Role of the normal gut microbiota. World J Gastroenterol. 21, 8787–8803 doi:10.3748/wjg.v21.i29.8787
    1. Guinane C.M. and Cotter P.D. (2013) Role of the gut microbiota in health and chronic gastrointestinal disease: understanding a hidden metabolic organ. Therap Adv Gastroenterol. 6, 295–308 doi:10.1177/1756283X13482996

Source: PubMed

Sponzoři a spolupracovníci

Zdravotní podmínky

Drogové intervence

3
Předplatit