What is the Healthy Gut Microbiota Composition? A Changing Ecosystem across Age, Environment, Diet, and Diseases

Emanuele Rinninella, Pauline Raoul, Marco Cintoni, Francesco Franceschi, Giacinto Abele Donato Miggiano, Antonio Gasbarrini, Maria Cristina Mele, Emanuele Rinninella, Pauline Raoul, Marco Cintoni, Francesco Franceschi, Giacinto Abele Donato Miggiano, Antonio Gasbarrini, Maria Cristina Mele

Abstract

Each individual is provided with a unique gut microbiota profile that plays many specific functions in host nutrient metabolism, maintenance of structural integrity of the gut mucosal barrier, immunomodulation, and protection against pathogens. Gut microbiota are composed of different bacteria species taxonomically classified by genus, family, order, and phyla. Each human's gut microbiota are shaped in early life as their composition depends on infant transitions (birth gestational date, type of delivery, methods of milk feeding, weaning period) and external factors such as antibiotic use. These personal and healthy core native microbiota remain relatively stable in adulthood but differ between individuals due to enterotypes, body mass index (BMI) level, exercise frequency, lifestyle, and cultural and dietary habits. Accordingly, there is not a unique optimal gut microbiota composition since it is different for each individual. However, a healthy host⁻microorganism balance must be respected in order to optimally perform metabolic and immune functions and prevent disease development. This review will provide an overview of the studies that focus on gut microbiota balances in the same individual and between individuals and highlight the close mutualistic relationship between gut microbiota variations and diseases. Indeed, dysbiosis of gut microbiota is associated not only with intestinal disorders but also with numerous extra-intestinal diseases such as metabolic and neurological disorders. Understanding the cause or consequence of these gut microbiota balances in health and disease and how to maintain or restore a healthy gut microbiota composition should be useful in developing promising therapeutic interventions.

Keywords: Alzheimer’s disease; Parkinson’s disease; age; autism spectrum disorders; celiac disease; colorectal cancer; diet; diversity; enterotypes; gut microbiota; health; hepatic encephalopathy; inflammatory bowel disease; irritable bowel syndrome; milk feeding; necrotizing enterocolitis; nutrition; obesity; personalized medicine; type 2 diabetes; weaning.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Examples of taxonomic gut microbiota composition. In the box are cited examples of bacteria belonging to Phyla Firmicutes and Bacteroidetes, representing 90% of gut microbiota.

References

    1. Thursby E., Juge N. Introduction to the human gut microbiota. Biochem. J. 2017;474:1823–1836. doi: 10.1042/BCJ20160510.
    1. Ley R.E., Turnbaugh P.J., Klein S., Gordon J.I. Microbial ecology: Human gut microbes associated with obesity. Nature. 2006;444:1022–1023. doi: 10.1038/4441022a.
    1. Valdes A.M., Walter J., Segal E., Spector T.D. Role of the gut microbiota in nutrition and health. BMJ. 2018;361:36–44. doi: 10.1136/bmj.k2179.
    1. Moore W.E., Holdeman L.V. Human fecal flora: The normal flora of 20 Japanese-Hawaiians. Appl. Microbiol. 1974;27:961–979.
    1. Poretsky R., Rodriguez-R L.M., Luo C., Tsementzi D., Konstantinidis K.T. Strengths and limitations of 16S rRNA gene amplicon sequencing in revealing temporal microbial community dynamics. PLoS ONE. 2014;9:e93827. doi: 10.1371/journal.pone.0093827.
    1. Mizrahi-Man O., Davenport E.R., Gilad Y. Taxonomic classification of bacterial 16S rRNA genes using short sequencing reads: Evaluation of effective study designs. PLoS ONE. 2013;8:e53608. doi: 10.1371/journal.pone.0053608.
    1. Human Microbiome Jumpstart Reference Strains Consortium. Nelson K.E., Weinstock G.M., Highlander S.K., Worley K.C., Creasy H.H., Wortman J.R., Rusch D.B., Mitreva M., Sodergren E., et al. A catalog of reference genomes from the human microbiome. Science. 2010;328:994–999. doi: 10.1126/science.1183605.
    1. 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. Metagenomic analysis of the human distal gut microbiome. Science. 2006;312:1355–1359. doi: 10.1126/science.1124234.
    1. Luckey T.D. Introduction to intestinal microecology. Am. J. Clin. Nutr. 1972;25:1292–1294. doi: 10.1093/ajcn/25.12.1292.
    1. Khosravi A., Mazmanian S.K. Disruption of the gut microbiome as a risk factor for microbial infections. Curr. Opin. Microbiol. 2013;16:221–227. doi: 10.1016/j.mib.2013.03.009.
    1. Brestoff J.R., Artis D. Commensal bacteria at the interface of host metabolism and the immune system. Nat. Immunol. 2013;14:676–684. doi: 10.1038/ni.2640.
    1. Laterza L., Rizzatti G., Gaetani E., Chiusolo P., Gasbarrini A. The gut microbiota and immune system relationship in human graft-versus-host disease. Mediterr. J. Hematol. Infect. Dis. 2016;8:e2016025. doi: 10.4084/mjhid.2016.025.
    1. 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. Enterotypes of the human gut microbiome. Nature. 2011;473:174–180. doi: 10.1038/nature09944.
    1. Flint H.J., Scott K.P., Louis P., Duncan S.H. The role of the gut microbiota in nutrition and health. Nat. Rev. Gastroenterol. Hepatol. 2012;9:577–589. doi: 10.1038/nrgastro.2012.156.
    1. Arboleya S., Binetti A., Salazar N., Fernández N., Solís G., Hernández-Barranco A., Margolles A., de Los Reyes-Gavilán C.G., Gueimonde M. Establishment and development of intestinal microbiota in preterm neonates. FEMS Microbiol. Ecol. 2012;79:763–772. doi: 10.1111/j.1574-6941.2011.01261.x.
    1. Ren S., Hui Y., Obelitz-Ryom K., Brandt A.B., Kot W., Nielsen D.S., Thymann T., Sangild P.T., Nguyen D.N. Neonatal gut and immune maturation is determined more by postnatal age than by post-conceptional age in moderately preterm pigs. Am. J. Physiol. Gastrointest. Liver Physiol. 2018;315:855–867. doi: 10.1152/ajpgi.00169.2018.
    1. Butel M.J., Suau A., Campeotto F., Magne F., Aires J., Ferraris L., Kalach N., Leroux B., Dupont C. Conditions of bifidobacterial colonization in preterm infants: A prospective analysis. J. Pediatr. Gastroenterol. Nutr. 2007;44:577–582. doi: 10.1097/MPG.0b013e3180406b20.
    1. Gabrielli O., Zampini L., Galeazzi T., Padella L., Santoro L., Peila C., Giuliani F., Bertino E., Fabris C., Coppa G.V. Preterm milk oligosaccharides during the first month of lactation. Pediatrics. 2011;128:e1520–e1531. doi: 10.1542/peds.2011-1206.
    1. Underwood M.A., Gaerlan S., De Leoz M.L., Dimapasoc L., Kalanetra K.M., Lemay D.G., German J.B., Mills D.A., Lebrilla C.B. Human milk oligosaccharides in premature infants: Absorption, excretion, and influence on the intestinal microbiota. Pediatr. Res. 2015;78:670–677. doi: 10.1038/pr.2015.162.
    1. Praticò G., Capuani G., Tomassini A., Baldassarre M.E., Delfini M., Miccheli A. Exploring human breast milk composition by NMR-based metabolomics. Nat. Prod. Res. 2014;28:95–101. doi: 10.1080/14786419.2013.843180.
    1. Bering S.B. Human milk oligosaccharides to prevent gut dysfunction and necrotizing enterocolitis in preterm neonates. Nutrients. 2018;10:1461. doi: 10.3390/nu10101461.
    1. Mastromarino P., Capobianco D., Campagna G., Laforgia N., Drimaco P., Dileone A., Baldassarre M.E. Correlation between lactoferrin and beneficial microbiota in breast milk and infant’s feces. Biometals. 2014;27:1077–1086. doi: 10.1007/s10534-014-9762-3.
    1. Salminen S., Gibson G.R., McCartney A.L., Isolauri E. Influence of mode of delivery on gut microbiota composition in seven year old children. Gut. 2004;53:1388–1389. doi: 10.1136/gut.2004.041640.
    1. Dominguez-Bello M.G., Costello E.K., Contreras M., Magris M., Hidalgo G., Fierer N., Knight R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl. Acad. Sci. USA. 2010;107:11971–11975. doi: 10.1073/pnas.1002601107.
    1. Biasucci G., Benenati B., Morelli L., Bessi E., Boehm G. Cesarean delivery may affect the early biodiversity of intestinal bacteria. J. Nutr. 2008;138:1796S–1800S. doi: 10.1093/jn/138.9.1796S.
    1. Mueller N.T., Bakacs E., Combellick J., Grigoryan Z., Dominguez-Bello M.G. The infant microbiome development: Mom matters. Trends Mol. Med. 2015;21:109–117. doi: 10.1016/j.molmed.2014.12.002.
    1. Pantoja-Feliciano I.G., Clemente J.C., Costello E.K., Perez M.E., Blaser M.J., Knight R., Dominguez-Bello M.G. Biphasic assembly of the murine intestinal microbiota during early development. ISME J. 2013;7:1112–1115. doi: 10.1038/ismej.2013.15.
    1. Grönlund M.M., Lehtonen O.P., Eerola E., Kero P. Fecal microflora in healthy infants born by different methods of delivery: Permanent changes in intestinal flora after cesarean delivery. J. Pediatr. Gastroenterol. Nutr. 1999;28:19–25. doi: 10.1097/00005176-199901000-00007.
    1. Azad M.B., Konya T., Maughan H., Guttman D.S., Field C.J., Chari R.S., Sears M.R., Becker A.B., Scott J.A., Kozyrskyj A.L. Gut microbiota of healthy Canadian infants: Profiles by mode of delivery and infant diet at 4 months. CMAJ. 2013;185:385–394. doi: 10.1503/cmaj.121189.
    1. Sevelsted A., Stokholm J., Bønnelykke K., Bisgaard H. Cesarean section and chronic immune disorders. Pediatrics. 2015;135:e92–e98. doi: 10.1542/peds.2014-0596.
    1. Chen G., Chiang W.L., Shu B.C., Guo Y.L., Chiou S.T., Chiang T.L. Associations of caesarean delivery and the occurrence of neurodevelopmental disorders, asthma or obesity in childhood based on Taiwan birth cohort study. BMJ Open. 2017;7:e017086. doi: 10.1136/bmjopen-2017-017086.
    1. Penders J., Thijs C., Vink C., Stelma F.F., Snijders B., Kummeling I., van den Brandt P.A., Stobberingh E.E. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118:511–521. doi: 10.1542/peds.2005-2824.
    1. Bezirtzoglou E., Tsiotsias A., Welling G.W. Microbiota profile in feces of breast- and formula-fed newborns by using fluorescence in situ hybridization (FISH) Anaerobe. 2011;17:478–482. doi: 10.1016/j.anaerobe.2011.03.009.
    1. Roger L.C., Costabile A., Holland D.T., Hoyles L., McCartney A.L. Examination of faecal Bifidobacterium populations in breast- and formula-fed infants during the first 18 months of life. Microbiology. 2010;156:3329–3341. doi: 10.1099/mic.0.043224-0.
    1. Marcobal A., Barboza M., Froehlich J.W., Block D.E., German J.B., Lebrilla C.B., Mills D.A. Consumption of human milk oligosaccharides by gut-related microbes. J. Agric. Food Chem. 2010;58:5334–5340. doi: 10.1021/jf9044205.
    1. Sakurama H., Kiyohara M., Wada J., Honda Y., Yamaguchi M., Fukiya S., Yokota A., Ashida H., Kumagai H., Kitaoka M., et al. Lacto-N-biosidase encoded by a novel gene of Bifidobacterium longum subspecies longum shows unique substrate specificity and requires a designated chaperone for its active expression. J. Biol. Chem. 2013;288:25194–25206. doi: 10.1074/jbc.M113.484733.
    1. Matsuki T., Yahagi K., Mori H., Matsumoto H., Hara T., Tajima S., Ogawa E., Kodama H., Yamamoto K., Yamada T., et al. A key genetic factor for fucosyllactose utilization affects infant gut microbiota development. Nat. Commun. 2016;7:11939. doi: 10.1038/ncomms11939.
    1. Yaron S., Shachar D., Abramas L., Riskin A., Bader D., Litmanovitz I., Bar-Yoseph F., Cohen T., Levi L., Lifshitz Y., et al. Effect of high β-palmitate content in infant formula on the intestinal microbiota of term infants. J. Pediatr. Gastroenterol. Nutr. 2013;56:376–381. doi: 10.1097/MPG.0b013e31827e1ee2.
    1. Mastromarino P., Capobianco D., Miccheli A., Praticò G., Campagna G., Laforgia N., Capursi T., Baldassarre M.E. Administration of a multistrain probiotic product (VSL#3) to women in the perinatal period differentially affects breast milk beneficial microbiota in relation to mode of delivery. Pharmacol. Res. 2015;95:63–70. doi: 10.1016/j.phrs.2015.03.013.
    1. Fallani M., Amarri S., Uusijarvi A., Adam R., Khanna S., Aguilera M., Gil A., Vieites J.M., Norin E., Young D., et al. Determinants of the human infant intestinal microbiota after the introduction of first complementary foods in infant samples from five European centres. Microbiology. 2011;157:1385–1392. doi: 10.1099/mic.0.042143-0.
    1. Tanaka M., Nakayama J. Development of the gut microbiota in infancy and its impact on health in later life. Allergol. Int. 2017;66:515–522. doi: 10.1016/j.alit.2017.07.010.
    1. Tidjani Alou M., Lagier J.C., Raoult D. Diet influence on the gut microbiota and dysbiosis related to nutritional disorders. Hum. Microbiome J. 2016;1:3–11. doi: 10.1016/j.humic.2016.09.001.
    1. Yatsunenko T., Rey F.E., Manary M.J., Trehan I., Dominguez-Bello M.G., Contreras M., Magris M., Hidalgo G., Baldassano R.N., Anokhin A.P., et al. Human gut microbiome viewed across age and geography. Nature. 2012;486:222–227. doi: 10.1038/nature11053.
    1. Toshitaka O., Kumiko K., Hirosuke S., Nanami H., Sachiko T., Jin-Zhong X., Fumiaki A., Ro O. Age-related changes in gut microbiota composition from newborn to centenarian: A cross-sectional study. BMC Microbiol. 2016;16:90.
    1. Guigoz Y., Doré J., Schiffrin E.J. The inflammatory status of old age can be nurtured from the intestinal environment. Curr. Opin. Clin. Nutr. Metab. Care. 2008;11:13–20. doi: 10.1097/MCO.0b013e3282f2bfdf.
    1. Pérez-Cobas A.E., Artacho A., Knecht H., Ferrús M.L., Friedrichs A., Ott S.J., Moya A., Latorre A., Gosalbes M.J. Differential effects of antibiotic therapy on the structure and function of human gut microbiota. PLoS ONE. 2013;8:e80201. doi: 10.1371/journal.pone.0080201.
    1. Iizumi T., Battaglia T., Ruiz V., Perez G.I. Gut microbiome and antibiotics. Arch. Med. Res. 2017;48:727–734. doi: 10.1016/j.arcmed.2017.11.004.
    1. Dethlefsen L., Relman D.A. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc. Natl. Acad. Sci. USA. 2011;108:4554–4561. doi: 10.1073/pnas.1000087107.
    1. Lozupone C.A., Stombaugh J.I., Gordon J.I., Jansson J.K., Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012;489:220–230. doi: 10.1038/nature11550.
    1. Bai J., Hu Y., Bruner D.W. Composition of gut microbiota and its association with body mass index and lifestyle factors in a cohort of 7–18 years old children from the American Gut Project. Pediatr. Obes. 2018 doi: 10.1111/ijpo.12480.
    1. Karlsson C.L., Onnerfält J., Xu J., Molin G., Ahrné S., Thorngren-Jerneck K. The microbiota of the gut in preschool children with normal and excessive body weight. Obesity. 2012;20:2257–2261. doi: 10.1038/oby.2012.110.
    1. Yun Y., Kim H.N., Kim S.E., Heo S.G., Chang Y., Ryu S., Shin H., Kim H.L. Comparative analysis of gut microbiota associated with body mass index in a large Korean cohort. BMC Microbiol. 2017;17:151. doi: 10.1186/s12866-017-1052-0.
    1. Bervoets L., Van Hoorenbeeck K., Kortleven I., Van Noten C., Hens N., Vael C., Goossens H., Desager K.N., Vankerckhoven V. Differences in gut microbiota composition between obese and lean children: A cross-sectional study. Gut Pathog. 2013;5:10. doi: 10.1186/1757-4749-5-10.
    1. Riva A., Borgo F., Lassandro C., Verduci E., Morace G., Borghi E., Berry D. Pediatric obesity is associated with an altered gut microbiota and discordant shifts in Firmicutes populations. Environ. Microbiol. 2017;19:95–105. doi: 10.1111/1462-2920.13463.
    1. Borgo F., Riva A., Benetti A., Casiraghi M.C., Bertelli S., Garbossa S., Anselmetti S., Scarone S., Pontiroli A.E., Morace G., et al. Microbiota in anorexia nervosa: The triangle between bacterial species, metabolites and psychological tests. PLoS ONE. 2017;12:e0179739. doi: 10.1371/journal.pone.0179739.
    1. 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. Linking long-term dietary patterns with gut microbial enterotypes. Science. 2011;334:105–108. doi: 10.1126/science.1208344.
    1. De Filippo C., Cavalieri D., Di Paola M., Ramazzotti M., Poullet J.B., Massart S., Collini S., Pieraccini G., Lionetti P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. USA. 2010;107:14691–14696. doi: 10.1073/pnas.1005963107.
    1. Schnorr S.L., Candela M., Rampelli S., Centanni M., Consolandi C., Basaglia G., Turroni S., Biagi E., Peano C., Severgnini M., et al. Gut microbiome of the Hadza hunter-gatherers. Nat. Commun. 2014;5:3654. doi: 10.1038/ncomms4654.
    1. David L.A., Maurice C.F., Carmody R.N., Gootenberg D.B., Button J.E., Wolfe B.E., Ling A.V., Devlin A.S., Varma Y., Fischbach M.A., et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–563. doi: 10.1038/nature12820.
    1. Monda V., Villano I., Messina A., Valenzano A., Esposito T., Moscatelli F., Viggiano A., Cibelli G., Chieffi S., Monda M., et al. Exercise modifies the gut microbiota with positive health effects. Oxid. Med. Cell. Longev. 2017:3831972. doi: 10.1155/2017/3831972.
    1. Clarke S.F., Murphy E.F., O’Sullivan O., Lucey A.J., Humphreys M., Hogan A., Hayes P., O’Reilly M., Jeffery I.B., Wood-Martin R., et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut. 2014;63:1913–1920. doi: 10.1136/gutjnl-2013-306541.
    1. Bhattarai Y., Muniz Pedrogo D.A., Kashyap P.C. Irritable bowel syndrome: A gut microbiota-related disorder? Am. J. Physiol. Gastrointest. Liver Physiol. 2017;312:52–62. doi: 10.1152/ajpgi.00338.2016.
    1. Carroll I.M., Chang Y.H., Park J., Sartor R.B., Ringel Y. Luminal and mucosal-associated intestinal microbiota in patients with diarrhea-predominant irritable bowel syndrome. Gut Pathog. 2010;2:19. doi: 10.1186/1757-4749-2-19.
    1. Krogius-Kurikka L., Lyra A., Malinen E., Aarnikunnas J., Tuimala J., Paulin L., Mäkivuokko H., Kajander K., Palva A. Microbial community analysis reveals high level phylogenetic alterations in the overall gastrointestinal microbiota of diarrhoea-predominant irritable bowel syndrome sufferers. BMC Gastroenterol. 2009;9:95. doi: 10.1186/1471-230X-9-95.
    1. Salonen A., de Vos W.M., Palva A. Gastrointestinal microbiota in irritable bowel syndrome: Present state and perspectives. Microbiology. 2010;156:3205–3215. doi: 10.1099/mic.0.043257-0.
    1. Frank D.N., St Amand A.L., Feldman R.A., Boedeker E.C., Harpaz N., Pace N.R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. USA. 2007;104:13780–13785. doi: 10.1073/pnas.0706625104.
    1. Machiels K., Joossens M., Sabino J., De Preter V., Arijs I., Eeckhaut V., Ballet V., Claes K., Van Immerseel F., Verbeke K., et al. A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut. 2014;63:1275–1283. doi: 10.1136/gutjnl-2013-304833.
    1. Hansen R., Russell R.K., Reiff C., Louis P., McIntosh F., Berry S.H., Mukhopadhya I., Bisset W.M., Barclay A.R., Bishop J., et al. Microbiota of de-novo pediatric IBD: Increased Faecalibacterium prausnitzii and reduced bacterial diversity in Crohn’s but not in ulcerative colitis. Am. J. Gastroenterol. 2012;107:1913–1922. doi: 10.1038/ajg.2012.335.
    1. Joossens M., Huys G., Cnockaert M., De Preter V., Verbeke K., Rutgeerts P., Vandamme P., Vermeire S. Dysbiosis of the faecal microbiota in patients with Crohn’s disease and their unaffected relatives. Gut. 2011;60:631–637. doi: 10.1136/gut.2010.223263.
    1. Sokol H., Pigneur B., Watterlot L., Lakhdari O., Bermúdez-Humarán L.G., Gratadoux J.J., Blugeon S., Bridonneau C., Furet J.P., Corthier G., et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. USA. 2008;105:16731–16736. doi: 10.1073/pnas.0804812105.
    1. Marasco G., Di Biase A.R., Schiumerini R., Eusebi L.H., Iughetti L., Ravaioli F., Scaioli E., Colecchia A., Festi D. Gut microbiota and celiac disease. Dig. Dis. Sci. 2016;61:1461–1472. doi: 10.1007/s10620-015-4020-2.
    1. Chander A.M., Yadav H., Jain S., Bhadada S.K., Dhawan D.K. Cross-talk between gluten, intestinal microbiota and intestinal mucosa in celiac disease: Recent advances and basis of autoimmunity. Front. Microbiol. 2018;9:2597. doi: 10.3389/fmicb.2018.02597.
    1. De Palma G., Nadal I., Medina M., Donat E., Ribes-Koninckx C., Calabuig M., Sanz Y. Intestinal dysbiosis and reduced immunoglobulin-coated bacteria associated with coeliac disease in children. BMC Microbiol. 2010;10:63. doi: 10.1186/1471-2180-10-63.
    1. Nadal I., Donat E., Ribes-Koninckx C., Calabuig M., Sanz Y. Imbalance in the composition of the duodenal microbiota of children with coeliac disease. J. Med. Microbiol. 2007;56:1669–1674. doi: 10.1099/jmm.0.47410-0.
    1. Collado M.C., Donat E., Ribes-Koninckx C., Calabuig M., Sanz Y. Imbalances in faecal and duodenal Bifidobacterium species composition inactive and non-active coeliac disease. BMC Microbiol. 2008;8:232. doi: 10.1186/1471-2180-8-232.
    1. Collado M.C., Donat E., Ribes-Koninckx C., Calabuig M., Sanz Y. Specific duodenal and faecal bacterial groups associated with paediatric coeliac disease. J. Clin. Pathol. 2009;62:264–269. doi: 10.1136/jcp.2008.061366.
    1. Jemal A., Bray F., Center M.M., Ferlay J., Ward E., Forman D. Global cancer statistics. CA Cancer J. Clin. 2011;61:69–90. doi: 10.3322/caac.20107.
    1. Wang T., Cai G., Qiu Y., Fei N., Zhang M., Pang X., Jia W., Cai S., Zhao L. Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J. 2012;6:320–329. doi: 10.1038/ismej.2011.109.
    1. Shen X.J., Rawls J.F., Randall T., Burcal L., Mpande C.N., Jenkins N., Jovov B., Abdo Z., Sandler R.S., Keku T.O. Molecular characterization of mucosal adherent bacteria and associations with colorectal adenomas. Gut Microbes. 2010;1:138–147. doi: 10.4161/gmic.1.3.12360.
    1. Kostic A.D., Gevers D., Pedamallu C.S., Michaud M., Duke F., Earl A.M., Ojesina A.I., Jung J., Bass A.J., Tabernero J., et al. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res. 2012;22:292–298. doi: 10.1101/gr.126573.111.
    1. Mayer E.A., Tillisch K., Gupta A. Gut/brain axis and the microbiota. J. Clin. Investig. 2015;125:926–938. doi: 10.1172/JCI76304.
    1. Rinninella E., Mele M.C., Merendino N., Cintoni M., Anselmi G., Caporossi A., Gasbarrini A., Minnella A.M. The role of diet, micronutrients and the gut microbiota in age-related macular degeneration: New perspectives from the gut-retina axis. Nutrients. 2018;10:1677. doi: 10.3390/nu10111677.
    1. Ley R.E., Bäckhed F., Turnbaugh P., Lozupone C.A., Knight R.D., Gordon J.I. Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. USA. 2005;102:11070–11075. doi: 10.1073/pnas.0504978102.
    1. Geurts L., Lazarevic V., Derrien M., Everard A., Van Roye M., Knauf C., Valet P., Girard M., Muccioli G.G., François P. Altered gut microbiota and endocannabinoid system tone in obese and diabetic leptin-resistant mice: Impact on apelin regulation in adipose tissue. Front. Microbiol. 2011;2:149. doi: 10.3389/fmicb.2011.00149.
    1. Kim K.A., Gu W., Lee I.A., Joh E.H., Kim D.H. High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. PLoS ONE. 2012;7:e47713. doi: 10.1371/journal.pone.0047713.
    1. Cani P.D. Gut microbiota and obesity: Lessons from the microbiome. Brief. Funct. Genom. 2013;12:381–387. doi: 10.1093/bfgp/elt014.
    1. Zhang C., Zhang M., Wang S., Han R., Cao Y., Hua W., Mao Y., Zhang X., Pang X., Wei C., et al. Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. SME J. 2010;4:232–241. doi: 10.1038/ismej.2009.112.
    1. Rizzatti G., Lopetuso L.R., Gibiino G., Binda C., Gasbarrini A. Proteobacteria: A common factor in human diseases. Biomed. Res. Int. 2017:9351507. doi: 10.1155/2017/9351507.
    1. Everard A., Belzer C., Geurts L., Ouwerkerk J.P., Druart C., Bindels L.B., Guiot Y., Derrien M., Muccioli G.G., Delzenne N.M., et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. USA. 2013;110:9066–9071. doi: 10.1073/pnas.1219451110.
    1. Derrien M., Vaughan E.E., Plugge C.M., de Vos W.M. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int. J. Syst. Evol. Microbiol. 2004;54:1469–1476. doi: 10.1099/ijs.0.02873-0.
    1. Turnbaugh P.J., Ley R.E., Mahowald M.A., Magrini V., Mardis E.R., Gordon J.I. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–1031. doi: 10.1038/nature05414.
    1. Larsen N., Vogensen F.K., van den Berg F.W., Nielsen D.S., Andreasen A.S., Pedersen B.K., Al-Soud W.A., Sørensen S.J., Hansen L.H., Jakobsen M. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS ONE. 2010;5:e9085. doi: 10.1371/journal.pone.0009085.
    1. Walsh C.J., Guinane C.M., O’Toole P.W., Cotter P.D. Beneficial modulation of the gut microbiota. FEBS Lett. 2014;588:4120–4130. doi: 10.1016/j.febslet.2014.03.035.
    1. Qin J., Li Y., Cai Z., Li S., Zhu J., Zhang F., Liang S., Zhang W., Guan Y., Shen D., et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490:55–60. doi: 10.1038/nature11450.
    1. Li X., Watanabe K., Kimura I. Gut microbiota dysbiosis drives and implies novel therapeutic strategies for diabetes mellitus and related metabolic diseases. Front. Immunol. 2017;8:1882. doi: 10.3389/fimmu.2017.01882.
    1. Prince M., Wimo A., Guerchet M., Ali G.C., Wu Y.T., Prina M. World Alzheimer Report 2015: The Global Impact of Dementia: An Analysis of Prevalence, Incidence, Cost and Trends. [(accessed on 1 November 2018)]; Available online: .
    1. Cattaneo A., Cattane N., Galluzzi S., Provasi S., Lopizzo N., Festari C., Ferrari C., Guerra U.P., Paghera B., Muscio C., et al. Association of brain amyloidosis with pro-inflammatory gut bacterial taxa and peripheral inflammation markers in cognitively impaired elderly. Neurobiol. Aging. 2017;49:60–68. doi: 10.1016/j.neurobiolaging.2016.08.019.
    1. Vogt N.M., Kerby R.L., Dill-McFarland K.A., Harding S.J., Merluzzi A.P., Johnson S.C., Carlsson C.M., Asthana S., Zetterberg H., Blennow K., et al. Gut microbiome alterations in Alzheimer’s disease. Sci. Rep. 2017;7:13537. doi: 10.1038/s41598-017-13601-y.
    1. Hopfner F., Künstner A., Müller S.H., Künzel S., Zeuner K.E., Margraf N.G., Deuschl G., Baines J.F., Kuhlenbäumer G. Gut microbiota in Parkinson disease in a northern German cohort. Brain Res. 2017;1667:41–45. doi: 10.1016/j.brainres.2017.04.019.
    1. Hill-Burns E.M., Debelius J.W., Morton J.T., Wissemann W.T., Lewis M.R., Wallen Z.D., Peddada S.D., Factor S.A., Molho E., Zabetian C.P., et al. Parkinson’s disease and Parkinson’s disease medications have distinct signatures of the gut microbiome. Mov. Disord. 2017;32:739–749. doi: 10.1002/mds.26942.
    1. Keshavarzian A., Green S.J., Engen P.A., Voigt R.M., Naqib A., Forsyth C.B., Mutlu E., Shannon K.M. Colonic bacterial composition in Parkinson’s disease. Mov. Disord. 2015;30:1351–1360. doi: 10.1002/mds.26307.
    1. Scheperjans F., Aho V., Pereira P.A., Koskinen K., Paulin L., Pekkonen E., Haapaniemi E., Kaakkola S., Eerola-Rautio J., Pohja M., et al. Gut microbiota are related to Parkinson’s disease and clinical phenotype. Mov. Disord. 2015;30:350–358. doi: 10.1002/mds.26069.
    1. Bajaj J.S., Ridlon J.M., Hylemon P.B., Thacker L.R., Heuman D.M., Smith S., Sikaroodi M., Gillevet P.M. Linkage of gut microbiome with cognition in hepatic encephalopathy. Am. J. Physiol. Gastrointest. Liver Physiol. 2012;302:168–175. doi: 10.1152/ajpgi.00190.2011.
    1. Finegold S.M., Molitoris D., Song Y., Liu C., Vaisanen M.L., Bolte E., McTeague M., Sandler R., Wexler H., Marlowe E.M., et al. Gastrointestinal microflora studies in late-onset autism. Clin. Infect. Dis. 2002;35:S6–S16. doi: 10.1086/341914.
    1. Finegold S.M. Desulfovibrio species are potentially important in regressive autism. Med. Hypotheses. 2011;77:270–274. doi: 10.1016/j.mehy.2011.04.032.
    1. Finegold S.M., Downes J., Summanen P.H. Microbiology of regressive autism. Anaerobe. 2012;18:260–262. doi: 10.1016/j.anaerobe.2011.12.018.
    1. Li Q., Han Y., Dy A.B.C., Hagerman R.J. The gut microbiota and autism spectrum disorders. Front. Cell. Neurosci. 2017;11:120. doi: 10.3389/fncel.2017.00120.
    1. Wang L., Christophersen C.T., Sorich M.J., Gerber J.P., Angley M.T., Conlon M.A. Low relative abundances of the mucolytic bacterium Akkermansia muciniphila and Bifidobacterium spp. in feces of children with autism. Appl. Environ. Microbiol. 2011;77:6718–6721. doi: 10.1128/AEM.05212-11.
    1. Williams B.L., Hornig M., Parekh T., Lipkin W.I. Application of novel PCR-based methods for detection, quantitation, and phylogenetic characterization of Sutterella species in intestinal biopsy samples from children with autism and gastrointestinal disturbances. MBio. 2012;3:e00261-11. doi: 10.1128/mBio.00261-11.
    1. Collins S.M., Surette M., Bercik P. The interplay between the intestinal microbiota and the brain. Nat. Rev. Microbiol. 2012;10:735–742. doi: 10.1038/nrmicro2876.
    1. Bailey M.T., Dowd S.E., Galley J.D., Hufnagle A.R., Allen R.G., Lyte M. Exposure to a social stressor alters the structure of the intestinal microbiota: Implications for stressor-induced immunomodulation. Brain Behav. Immun. 2011;25:397–407. doi: 10.1016/j.bbi.2010.10.023.
    1. Lee Y.K., Menezes J.S., Umesaki Y., Mazmanian S.K. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA. 2011;108:4615–4622. doi: 10.1073/pnas.1000082107.
    1. Patterson E., Cryan J.F., Fitzgerald G.F., Ross R.P., Dinan T.G., Stanton C. Gut microbiota, the pharmabiotics they produce and host health. Proc. Nutr. Soc. 2014;73:477–489. doi: 10.1017/S0029665114001426.

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