Bifidobacteria and Butyrate-Producing Colon Bacteria: Importance and Strategies for Their Stimulation in the Human Gut

Audrey Rivière, Marija Selak, David Lantin, Frédéric Leroy, Luc De Vuyst, Audrey Rivière, Marija Selak, David Lantin, Frédéric Leroy, Luc De Vuyst

Abstract

With the increasing amount of evidence linking certain disorders of the human body to a disturbed gut microbiota, there is a growing interest for compounds that positively influence its composition and activity through diet. Besides the consumption of probiotics to stimulate favorable bacterial communities in the human gastrointestinal tract, prebiotics such as inulin-type fructans (ITF) and arabinoxylan-oligosaccharides (AXOS) can be consumed to increase the number of bifidobacteria in the colon. Several functions have been attributed to bifidobacteria, encompassing degradation of non-digestible carbohydrates, protection against pathogens, production of vitamin B, antioxidants, and conjugated linoleic acids, and stimulation of the immune system. During life, the numbers of bifidobacteria decrease from up to 90% of the total colon microbiota in vaginally delivered breast-fed infants to <5% in the colon of adults and they decrease even more in that of elderly as well as in patients with certain disorders such as antibiotic-associated diarrhea, inflammatory bowel disease, irritable bowel syndrome, obesity, allergies, and regressive autism. It has been suggested that the bifidogenic effects of ITF and AXOS are the result of strain-specific yet complementary carbohydrate degradation mechanisms within cooperating bifidobacterial consortia. Except for a bifidogenic effect, ITF and AXOS also have shown to cause a butyrogenic effect in the human colon, i.e., an enhancement of colon butyrate production. Butyrate is an essential metabolite in the human colon, as it is the preferred energy source for the colon epithelial cells, contributes to the maintenance of the gut barrier functions, and has immunomodulatory and anti-inflammatory properties. It has been shown that the butyrogenic effects of ITF and AXOS are the result of cross-feeding interactions between bifidobacteria and butyrate-producing colon bacteria, such as Faecalibacterium prausnitzii (clostridial cluster IV) and Anaerostipes, Eubacterium, and Roseburia species (clostridial cluster XIVa). These kinds of interactions possibly favor the co-existence of bifidobacterial strains with other bifidobacteria and with butyrate-producing colon bacteria in the human colon.

Keywords: arabinoxylan-oligosaccharides; bifidobacteria; butyrate-producing colon bacteria; cross-feeding; inulin-type fructans; prebiotics; probiotics.

Figures

Figure 1
Figure 1
Spatial distribution and concentrations of bacteria along the gastrointestinal tract of humans (Tuohy and Scott, 2015). The dominant genera in the stomach, small intestine, and colon are listed, based on 16S rRNA gene sequence studies (Tap et al., ; Zoetendal et al., ; Delgado et al., ; Walker et al., 2014).
Figure 2
Figure 2
(A) Schematic representation of the fermentation of hexoses (glucose and fructose) and pentoses (arabinose and xylose) by bifidobacteria through the fructose 6-phosphate phosphoketolase pathway or bifid shunt. (B) Schematic representation of the fermentation of hexoses (glucose and fructose) and pentoses (arabinose and xylose) by butyrate-producing colon bacteria through the Embden-Meyerhof-Parnas pathway and pentose-phosphate pathway, respectively, and of lactate. Dashed lines represent different steps. Underlined metabolites are excreted into the extracellular medium. Fdox, oxidized ferredoxin; Fdred, reduced ferredoxin; FAD, flavin adenine dinucleotide; enzymes: 1, fructose 6-phosphate phosphoketolase; 2, transaldolase; 3, transketolase; 4, xylulose 5-phosphate phosphoketolase; 5, acetate kinase; 6, lactate dehydrogenase; 7, formate acetyltransferase; 8, bifunctional aldehyde-alcohol dehydrogenase; 9, phosphotransacetylase; 10, phosphoenolpyruvate carboxylase; 11, malate dehydrogenase; 12, fumarase; 13, succinate dehydrogenase; 14, pyruvate:ferredoxin oxidoreductase; 15, pyruvate-formate lyase; 16, butyryl-CoA dehydrogenase/electron-transferring flavoprotein (Bcd/Etf) complex; 17, butyrate kinase; 18, butyryl-CoA:acetate CoA transferase; 19, ferredoxin hydrogenase; and 20, membrane-bound ferredoxin oxidoreductase (Rnf) complex.
Figure 3
Figure 3
Chemical structures [(A) and (C)] and schematic representations [(B) and (D)] of ITF, AX, and AXOS molecules. Glc, glucose; Fru, fructose; Xyl, xylose; Ara, arabinose; FeA, ferulic acid; Ac, acetyl group; GlA, glucuronic acid; CouA, p-coumaric acid. Arrows indicate possible hydrolysis of the carbohydrates by bacterial enzymes present in the human colon: 1, β-fructofuranosidase; 2, β-xylosidase; 3, β-endoxylanase; 4, exo-oligoxylanase; 5, α-arabinofuranosidase; 6, α-glucuronidase; and 7, esterase.
Figure 4
Figure 4
Different types of cross-feeding that can take place between Bifidobacterium spp. and species of butyrate-producing colon bacteria in the human colon. Arrows indicate consumption of oligofructose, inulin, and AXOS (…..), production of carbohydrate breakdown products and/or metabolic end-products (- - -), and cross-feeding interactions between the bifidobacterial and butyrate-producing strains (—).

References

    1. Al-Lahham S. H., Peppelenbosch M. P., Roelofsen H., Vonk R. J., Venema K. (2010). Biological effects of propionic acid in humans; metabolism, potential applications and underlying mechanisms. Biochim. Biophys. Acta 1801, 1175–1183. 10.1016/j.bbalip.2010.07.007
    1. Antoine C., Peyron S., Mabille F., Lapierre C., Bouchet B., Abecassis J., et al. . (2003). Individual contribution of grain outer layers and their cell wall structure to the mechanical properties of wheat bran. J. Agric. Food Chem. 51, 2026–2033. 10.1021/jf0261598
    1. Aroniadis O. C., Brandt L. J. (2014). Intestinal microbiota and the efficacy of fecal microbiota transplantation in gastrointestinal disease. Gastroenterol. Hepatol. 10, 230–237.
    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. 10.1038/nature09944
    1. Bäckhed 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. 10.1126/science.1104816
    1. Barron C., Surget A., Rouau X. (2007). Relative amounts of tissues in mature wheat (Triticum aestivum L.) grain and their carbohydrate and phenolic acid composition. J. Cereal Sci. 45, 88–96. 10.1016/j.jcs.2006.07.004
    1. Belenguer A., Duncan S. H., Calder A. G., Holtrop G., Louis P., Lobley G. E., et al. . (2006). Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Appl. Environ. Microbiol. 72, 3593–3599. 10.1128/AEM.72.5.3593-3599.2006
    1. Belenguer A., Holtrop G., Duncan S. H., Anderson S. E., Calder A. G., Flint H. J., et al. . (2011). Rates of production and utilization of lactate by microbial communities from the human colon. FEMS Microbiol. Ecol. 77, 107–119. 10.1111/j.1574-6941.2011.01086.x
    1. Benamrouche S., Crônier D., Debeire P., Chabbert B. A. (2002). A chemical and histological study on the effect of (1 → 4)-β-endo-xylanase treatment on wheat bran. J. Cereal Sci. 36, 253–260. 10.1006/jcrs.2001.0427
    1. Bindels L. B., Delzenne N. M., Cani P. D., Walter J. (2015). Towards a more comprehensive concept for prebiotics. Nat. Rev. Gastroenterol. Hepatol. 12, 303–310. 10.1038/nrgastro.2015.47
    1. Boets E., Houben E., Windey K., De Preter V., Moens F., Gomand S., et al. (2013). In vivo evaluation of bacterial cross-feeding in the colon using stable isotope techniques: a pilot study, in Digestive Disease Week, Orlando, FL: Gastroenterology 144.
    1. Bottacini F., Ventura M., van Sinderen D., O'Connell Motherway M. (2014). Diversity, ecology and intestinal function of bifidobacteria. Microb. Cell Fact. 13, S4. 10.1186/1475-2859-13-S1-S4
    1. Braniste V., Al-Asmakh M., Kowal C., Anuar F., Abbaspour A., Tóth M., et al. . (2014). The gut microbiota influences blood-brain barrier permeability in mice. Sci. Transl. Med. 6, 263ra158. 10.1126/scitranslmed.3009759
    1. Broekaert W. F., Courtin C., Delcour J. (2009). (Arabino)xylan Oligosaccharide Preparation. WO 2009117790 A2. PCT International Publication.
    1. Broekaert W. F., Courtin C. M., Verbeke K., Van de Wiele T., Verstraete W., Delcour J. A. (2011). Prebiotic and other health-related effects of cereal-derived arabinoxylans, arabinoxylan-oligosaccharides, and xylooligosaccharides. Crit. Rev. Food Sci. Nutr. 51, 178–194. 10.1080/10408390903044768
    1. Bunzel M., Ralph J., Marita J. M., Hatfield R. D., Steinhart H. (2001). Diferulates as structural components in soluble and insoluble cereal dietary fibre. J. Sci. Food Agric. 81, 653–660. 10.1002/jsfa.861
    1. Cani P. D., Bibiloni R., Knauf C., Waget A., Neyrinck A. M., Delzenne N. M., et al. . (2008). Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57, 1470–1481. 10.2337/db07-1403
    1. Cani P. D., Van Hul M. (2015). Novel opportunities for next-generation probiotics targeting metabolic syndrome. Curr. Opin. Biotechnol. 32, 21–27. 10.1016/j.copbio.2014.10.006
    1. Chang P. V., Hao L., Offermanns S., Medzhitov R. (2014). The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc. Natl. Acad. Sci. U.S.A. 111, 2247–2252. 10.1073/pnas.1322269111
    1. Chassard C., Goumy V., Leclerc M., Del'homme C., Bernalier-Donadille A. (2007). Characterization of the xylan-degrading microbial community from human faeces. FEMS Microbiol. Ecol. 61, 121–131. 10.1111/j.1574-6941.2007.00314.x
    1. Choi J. H., Lee K. M., Lee M. K., Cha C. J., Kim G. B. (2014). Bifidobacterium faecale sp. nov., isolated from human >faeces. Int. J. Syst. Evol. Microbiol. 64, 3134–3139. 10.1099/ijs.0.063479-0
    1. Cloetens L., Broekaert W. F., Delaedt Y., Ollevier F., Courtin C. M., Delcour J. A., et al. . (2010). Tolerance of arabinoxylan-oligosaccharides and their prebiotic activity in healthy subjects: a randomised, placebo-controlled cross-over study. Br. J. Nutr. 103, 703–713. 10.1017/S0007114509992248
    1. Collins S. M., Surette M., Bercik P. (2012). The interplay between the intestinal microbiota and the brain. Nat. Rev. Microbiol. 10, 735–742. 10.1038/nrmicro2876
    1. Courtin C. M., Broekaert W. F., Swennen K., Aerts G., Van Craeyveld V., Delcour J. A. (2009). Occurrence of arabinoxylo-oligosaccharides and arabinogalactan peptides in beer. J. Am. Soc. Brew. Chem. 67, 112–117. 10.1094/asbcj-2009-0323-01
    1. Crittenden R., Karppinen S., Ojanen S., Tenkanen M., Fagerstrom R., Matto J., et al. (2002). In vitro fermentation of cereal dietary fibre carbohydrates by probiotic and intestinal bacteria. J. Sci. Food Agric. 82, 781–789. 10.1002/jsfa.1095
    1. Cui B., Li P., Xu L., Peng Z., Xiang J., He Z., et al. . (2016). Step-up fecal microbiota transplantation (FMT) strategy. Gut Microbes. 10.1080/19490976.2016.1151608. [Epub ahead of print].
    1. Damen B., Verspreet J., Pollet A., Broekaert W. F., Delcour J. A., Courtin C. M. (2011). Prebiotic effects and intestinal fermentation of cereal arabinoxylans and arabinoxylan oligosaccharides in rats depend strongly on their structural properties and joint presence. Mol. Nutr. Food. Res. 55, 1862–1874. 10.1002/mnfr.201100377
    1. Delgado S., Cabrera-Rubio R., Mira A., Suárez A., Mayo B. (2013). Microbiological survey of the human gastric ecosystem using culturing and pyrosequencing methods. Microb. Ecol. 63, 763–772. 10.1007/s00248-013-0192-5
    1. de Vos W. M. (2013). Fame and future of faecal transplantations - developing next-generation therapies with synthetic microbiomes. Microb. Biotechnol. 6, 316–325. 10.1111/1751-7915.12047
    1. de Vos W. M., de Vos E. A. (2012). Role of the intestinal microbiome in health and disease: from correlation to causation. Nutr. Rev. 1, S45–S56. 10.1111/j.1753-4887.2012.00505.x
    1. De Vuyst L., Leroy F. (2011). Cross-feeding between bifidobacteria and butyrate-producing colon bacteria explains bifidobacterial competitiveness, butyrate production, and gas production. Int. J. Food Microbiol. 149, 73–80. 10.1016/j.ijfoodmicro.2011.03.003
    1. De Vuyst L., Moens F., Selak M., Rivière A., Leroy F. (2014). Summer meeting 2013: growth and physiology of bifidobacteria. J. Appl. Microbiol. 116, 477–491. 10.1111/jam.12415
    1. Di Gioia D., Aloisio I., Mazzola G., Biavati B. (2014). Bifidobacteria: their impact on gut microbiota composition and their applications as probiotics in infants. Appl. Microbiol. Biotechnol. 98, 563–577. 10.1007/s00253-013-5405-9
    1. Dinan T. G., Stanton C., Cryan J. F. (2013). Psychobiotics: a novel class of psychotropic. Biol. Psychiat. 74, 720–726. 10.1016/j.biopsych.2013.05.001
    1. Dinan T. G., Stilling R. M., Stanton C., Cryan J. F. (2015). Collective unconscious: how gut microbes shape human behavior. J. Psychiat. Res. 63, 1–9. 10.1016/j.jpsychires.2015.02.021
    1. Dodd D., Cann I. K. (2009). Enzymatic deconstruction of xylan for biofuel production. Glob. Change Biol. Bioenergy 18, 2–17. 10.1111/j.1757-1707.2009.01004.x
    1. Dodd D., Mackie R., Cann I. K. (2011). Xylan degradation, a metabolic property shared by rumen and human colonic Bacteroidetes. Mol. Microbiol. 79, 292–304. 10.1111/j.1365-2958.2010.07473.x
    1. Duncan S. H., Flint H. J. (2013). Probiotics and prebiotics and health in ageing populations. Maturitas 75, 44–50. 10.1016/j.maturitas.2013.02.004
    1. Duncan S. H., Louis P., 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. 10.1128/AEM.70.10.5810-5817.2004
    1. Duncan S. H., Louis P., Thomson J. M., Flint H. J. (2009). The role of pH in determining the species composition of the human colonic microbiota. Environ. Microbiol. 11, 2112–2122. 10.1111/j.1462-2920.2009.01931.x
    1. Eeckhaut V., Ducatelle R., Sas B., Vermeire S., Van Immerseel F. (2014). Progress towards butyrate-producing pharmabiotics: Butyricicoccus pullicaecorum capsule and efficacy in TNBS models in comparison with therapeutics. Gut 63, 367. 10.1136/gutjnl-2013-305293
    1. Eeckhaut V., Machiels K., Perrier C., Romero C., Maes S., Flahou B., et al. . (2013). Butyricicoccus pullicaecorum in inflammatory bowel disease. Gut 62, 1745–1752. 10.1136/gutjnl-2012-303611
    1. EFSA (2010). Scientific opinion on the substantiation of health claims related to live yoghurt cultures and improved lactose digestion (ID 1143, 2976), pursuant to Article 13 (1) of regulation (EC) No 1924/20061. EFSA J. 8, 1763 10.2903/j.efsa.2010.1763
    1. EFSA (2011a). Scientific opinion on the substantiation of health claims related to resistant starch and reduction of post-prandial glycaemic responses (ID 681), “digestive health benefits” (ID 682) and “favours a normal colon metabolism” (ID 783) pursuant to Article 13 (1) of Regulation (EC) No 1924/2006. EFSA J. 9, 2024 10.2903/j.efsa.2011.2024
    1. EFSA (2011b). Scientific opinion on the substantiation of health claims related to arabinoxylan produced from wheat endosperm and reduction of post-prandial glycaemic responses (ID 830) pursuant to Article 13 (1) of Regulation (EC) No 1924/2006. EFSA J. 9, 2205 10.2903/j.efsa.2011.2205
    1. EFSA (2015). Scientific opinion on the substantiation of a health claim related to “native chicory inulin” and maintenance of normal defecation by increasing stool frequency pursuant to Article 13.5 of Regulation (EC) No 1924/2006. EFSA J. 13, 3951 10.2903/j.efsa.2015.3951
    1. Egan M., O'Connell Motherway M., Kilcoyne M., Kane M., Joshi L., Ventura M., et al. . (2014). Cross-feeding by Bifidobacterium breve UCC2003 during co-cultivation with Bifidobacterium bifidum PRL2010 in a mucin-based medium. BMC Microbiol. 14:282. 10.1186/s12866-014-0282-7
    1. Ehrmann M. A., Korakli M., Vogel R. F. (2003). Identification of the gene for beta-fructofuranosidase of Bifidobacterium lactis DSM10140T and characterization of the enzyme expressed in Escherichia coli. Curr. Microbiol. 46, 391–397. 10.1007/s00284-002-3908-1
    1. El Aidy S., Van den Abbeele P., Van de Wiele T., Louis P., Kleerebezem M. (2013). Intestinal colonization: how key microbial players become established in this dynamic process. Bioessays 35, 913–923. 10.1002/bies.201300073
    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. 10.1038/nrmicro3050
    1. Eloe-Fadrosh E. A., Brady A., Crabtree J., Drabek E. F., Ma B., Mahurkar A., et al. . (2015). Functional dynamics of the gut microbiome in elderly people during probiotic consumption. MBio 6:e00231. 10.1128/mBio.00231-15
    1. European Commission (2008). Commission directive 2008/100/EC. Official Journal European Union, p. L 285/9.
    1. Euzéby J. P. (1997). List of bacterial names with standing in nomenclature: a folder available on the internet. Int. J. Syst. Bacteriol. 47, 590–592. 10.1099/00207713-47-2-590
    1. Euzéby J. P. (2016). Bifidobacterium. List of Prokaryotic Names with Standing in Nomenclature. Available online at: (Accessed May 19, 2016).
    1. Everard A., Cani P. D. (2013). Diabetes, obesity and gut microbiota. Best Pract. Res. Clin. Gastroenterol. 27, 73–78. 10.1016/j.bpg.2013.03.007
    1. Everard A., Lazarevic V., Derrien M., Girard M., Muccioli G. G., Neyrinck A. M., et al. . (2011). Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes 60, 2775–2786. 10.2337/db11-0227
    1. Faith J. J., Guruge J. L., Charbonneau M., Subramanian S., Seedorf H., Goodman A. L., et al. . (2013). The long-term stability of the human gut microbiota. Science 341:1237439. 10.1126/science.1237439
    1. Falony G., Calmeyn T., Leroy F., De Vuyst L. (2009a). Coculture fermentations of Bifidobacterium species and Bacteroides thetaiotaomicron reveal a mechanistic insight into the prebiotic effect of inulin-type fructans. Appl. Environ. Microbiol. 75, 2312–2319. 10.1128/AEM.02649-08
    1. Falony G., Lazidou K., Verschaeren A., Weckx S., Maes D., De Vuyst L. (2009b). In vitro kinetic analysis of fermentation of prebiotic inulin-type fructans by Bifidobacterium species reveals four different phenotypes. Appl. Environ. Microbiol. 75, 454–461. 10.1128/AEM.01488-08
    1. Falony G., Verschaeren A., De Bruycker F., De Preter V., Verbeke K., Leroy F., et al. . (2009c). In vitro kinetics of prebiotic inulin-type fructan fermentation by butyrate-producing colon bacteria: implementation of online gas chromatography for quantitative analysis of carbon dioxide and hydrogen gas production. Appl. Environ. Microbiol. 75, 5884–5892. 10.1128/AEM.00876-09
    1. Falony G., Vlachou A., Verbrugghe K., De Vuyst L. (2006). Cross-feeding between Bifidobacterium longum BB536 and acetate-converting, butyrate-producing colon bacteria during growth on oligofructose. Appl. Environ. Microbiol. 72, 7835–7841. 10.1128/AEM.01296-06
    1. Figueroa-González I., Quijano G., Ramírez G., Cruz-Guerrero A. (2011). Probiotics and prebiotics - perspectives and challenges. J. Sci. Food Agric. 91, 1341–1348. 10.1002/jsfa.4367
    1. Frei R., Akdis M., O'Mahony L. (2015). Prebiotics, probiotics, synbiotics, and the immune system: experimental data and clinical evidence. Curr. Opin. Gastroenterol. 31, 153–158. 10.1097/MOG.0000000000000151
    1. Gagnon M., Savard P., Rivière A., LaPointe G., Roy D. (2015). Bioaccessible antioxidants in milk fermented by Bifidobacterium longum subsp. longum strains. Biomed. Res. Int. 2015:169381. 10.1155/2015/169381
    1. Geirnaert A., Steyaert A., Eeckhaut V., Debruyne B., Arends J. B., Van Immerseel F., et al. . (2014). Butyricicoccus pullicaecorum, a butyrate producer with probiotic potential, is intrinsically tolerant to stomach and small intestine conditions. Anaerobe 30, 70–74. 10.1016/j.anaerobe.2014.08.010
    1. Gevers D., Kugathasan S., Denson L. A., Vázquez-Baeza Y., Van Treuren W., Ren B., et al. . (2014). The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe 15, 382–392. 10.1016/j.chom.2014.02.005
    1. Gibson G. R., Probert H. M., Loo J. V., Rastall R. A., Roberfroid M. B. (2004). Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr. Res. Rev. 17, 259–275. 10.1079/NRR200479
    1. Gibson G. R., Scott K. P., Rastall R. A., Tuohy K. M., Hotchkiss A., Dubert-Ferrandon A., et al. (2010). Dietary prebiotics: current status and new definition. Food Sci. Technol. Bull. 7, 1–19. 10.1616/1476-2137.15880
    1. Glanville J., King S., Guarner F., Hill C., Sanders M. E. (2015). A review of the systematic review process and its applicability for use in evaluating evidence for health claims on probiotic foods in the European Union. Nutr. J. 14, 16. 10.1186/s12937-015-0004-5
    1. Gorissen L., De Vuyst L., Raes K., De Smet S., Leroy F. (2012). Conjugated linoleic and linolenic acid production kinetics by bifidobacteria differ among strains. Int. J. Food Microbiol. 155, 234–240. 10.1016/j.ijfoodmicro.2012.02.012
    1. Gorissen L., Raes K., Weckx S., Dannenberger D., Leroy F., De Vuyst L., et al. . (2010). Production of conjugated linoleic acid and conjugated linolenic acid isomers by Bifidobacterium species. Appl. Microbiol. Biotechnol. 87, 2257–2266. 10.1007/s00253-010-2713-1
    1. Gosálbez L., Ramón D. (2015). Probiotics in transition: novel strategies. Trends Biotechnol. 33, 195–196. 10.1016/j.tibtech.2015.01.006
    1. Gråsten S., Liukkonen K. H., Chrevatidis A., El-Nezami H., Poutanen K., Mykkänen H. (2003). Effects of wheat pentosan and inulin on the metabolic activity of fecal microbiota and on bowel function in healthy humans. Nutr. Res. 23, 1503–1514. 10.1016/S0271-5317(03)00164-7
    1. Grimm V., Westermann C., Riedel C. U. (2014). Bifidobacteria-host interactions - an update on colonisation factors. Biomed. Res. Int. 2014:960826. 10.1155/2014/960826
    1. Grootaert C., Delcour J. A., Courtin C. M., Broekaert W. F., Verstraete W., Van de Wiele T. (2007). Microbial metabolism and prebiotic potency of arabinoxylan oligosaccharides in the human intestine. Trends Food Sci. Technol. 18, 64–71. 10.1016/j.tifs.2006.08.004
    1. Grootaert C., Van den Abbeele P., Marzorati M., Broekaert W. F., Courtin C. M., Delcour J. A., et al. . (2009). Comparison of prebiotic effects of arabinoxylan oligosaccharides and inulin in a simulator of the human intestinal microbial ecosystem. FEMS Microbiol. Ecol. 69, 231–242. 10.1111/j.1574-6941.2009.00712.x
    1. Gruppen H., Kormelink F. J. M., Voragen A. G. J. (1993). Enzymic degradation of water-unextractable cell wall material and arabinoxylans from wheat flour. J. Cereal Sci. 18, 129–143. 10.1006/jcrs.1993.1041
    1. Hamer H. M., Jonkers D., Venema K., Vanhoutvin S., Troost F. J., Brummer R. J. (2008). Review article: the role of butyrate on colonic function. Aliment. Pharmacol. Ther. 27, 104–119. 10.1111/j.1365-2036.2007.03562.x
    1. Havenaar R. (2011). Intestinal health functions of colonic microbial metabolites: a review. Benef. Microbes 2, 103–114. 10.3920/BM2011.0003
    1. Hill C., Guarner F., Reid G., Gibson G. R., Merenstein D. J., Pot B., et al. . (2014). Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 11, 506–514. 10.1038/nrgastro.2014.66
    1. Hood L. (2012). Tackling the microbiome. Science 336, 1209. 10.1126/science.1225475
    1. Hopkins M. J., Englyst H. N., Macfarlane S., Furrie E., Macfarlane G. T., McBain A. J. (2003). Degradation of cross-linked and non-cross-linked arabinoxylans by the intestinal microbiota in children. Appl. Environ. Microbiol. 69, 6354–6360. 10.1128/AEM.69.11.6354-6360.2003
    1. Hughes S. A., Shewry P. R., Li L., Gibson G. R., Sanz M. L., Rastall R. A. (2007). In vitro fermentation by human fecal microflora of wheat arabinoxylans. J. Agric. Food Chem. 55, 4589–4595. 10.1021/jf070293g
    1. Hutkins R. W., Krumbeck J. A., Bindels L. B., Cani P. D., Fahey G., Goh Y. J., et al. . (2016). Prebiotics: why definitions matter. Curr. Opin. Biotechnol. 37, 1–7. 10.1016/j.copbio.2015.09.001
    1. Ishikawa E., Matsuki T., Kubota H., Makino H., Sakai T., Oishi K., et al. . (2013). Ethnic diversity of gut microbiota: species characterization of Bacteroides fragilis group and genus Bifidobacterium in healthy Belgian adults, and comparison with data from Japanese subjects. J. Biosci. Bioeng. 116, 265–270. 10.1016/j.jbiosc.2013.02.010
    1. Izydorczyk M. S., Biliaderis C. G. (1995). Cereal arabinoxylans: advances in structure and physicochemical properties. Carbohydr. Polym. 28, 33–48. 10.1016/0144-8617(95)00077-1
    1. Izydorczyk M. S., Biliaderis C. G. (2006). Arabinoxylans: technology and nutritionally functional plant polysaccharides, in Functional Food Carbohydrates, eds Biliaderis C. G., Izydorczyk M. S. (Boca Raton, FL: CRC Press; ), 249–290.
    1. Jedrzejczak-Krzepkowska M., Tkaczuk K. L., Bielecki S. (2011). Biosynthesis, purification and characterization of β-fructofuranosidase from Bifidobacterium longum KN29.1. Proc. Biochem. 46, 1963–1972. 10.1016/j.procbio.2011.07.005
    1. Kapel N., Thomas M., Corcos O., Mayeur C., Barbot-Trystram L., Bouhnik Y., et al. . (2014). Practical implementation of faecal transplantation. Clin. Microbiol. Infec. 20, 1098–1105. 10.1111/1469-0691.12796
    1. Khodayar-Pardo P., Mira-Pascual L., Collado M. C., Martínez-Costa C. (2014). Impact of lactation stage, gestational age and mode of delivery on breast milk microbiota. J. Perinatol. 34, 599–605. 10.1038/jp.2014.47
    1. Klijn A., Mercenier A., Arigoni F. (2005). Lessons from the genomes of bifidobacteria. FEMS Microbiol. Rev. 29, 491–509. 10.1016/j.fmrre.2005.04.010
    1. Kumar H., Salminen S., Verhagen H., Rowland I., Heimbach J., Bañares S., et al. . (2015). Novel probiotics and prebiotics: road to the market. Curr. Opin. Biotechnol. 32, 99–103. 10.1016/j.copbio.2014.11.021
    1. Lagaert S., Pollet A., Courtin C. M., Volckaert G. (2014). β-Xylosidases and α-L-arabinofuranosidases: accessory enzymes for arabinoxylan degradation. Biotechnol. Adv. 32, 316–332. 10.1016/j.biotechadv.2013.11.005
    1. Lagaert S., Pollet A., Delcour J. A., Lavigne R., Courtin C. M., Volckaert G. (2010). Substrate specificity of three recombinant α-L-arabinofuranosidases from Bifidobacterium adolescentis and their divergent action on arabinoxylan and arabinoxylan oligosaccharides. Biochem. Biophys. Res. Commun. 26, 644–650. 10.1016/j.bbrc.2010.10.075
    1. Lagaert S., Pollet A., Delcour J. A., Lavigne R., Courtin C. M., Volckaert G. (2011). Characterization of two β-xylosidases from Bifidobacterium adolescentis and their contribution to the hydrolysis of prebiotic xylooligosaccharides. Appl. Microbiol. Biotechnol. 92, 1179–1185. 10.1007/s00253-011-3396-y
    1. Laureys D., Cnockaert M., De Vuyst L., Vandamme P. (2016). Bifidobacterium aquikefiri sp. nov., isolated from water kefir. Int. J. Syst. Evolut. Microbiol. 66, 1281–1286. 10.1099/ijsem.0.000877
    1. Laureys D., De Vuyst L. (2014). Microbial species diversity, community dynamics, and metabolite kinetics of water kefir fermentation. Appl. Environ. Microbiol. 80, 2564–2572. 10.1128/AEM.03978-13
    1. Leahy S. C., Higgins D. G., Fitzgerald G. F., van Sinderen D. (2005). Getting better with bifidobacteria. J. Appl. Microbiol. 98, 1303–1315. 10.1111/j.1365-2672.2005.02600.x
    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. 10.1038/nature12506
    1. Li S., Zhu A., Benes V., Costea P. I., Hercog R., Hildebrand F., et al. . (2016). Durable coexistence of donor and recipient strains after fecal microbiota transplantation. Science 352, 586–589. 10.1126/science.aad8852
    1. Lombard V., Ramulu H. G., Drula E., Coutinho P. M., Henrissat B. (2014). The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42, D490–D495. 10.1093/nar/gkt1178
    1. Louis P., Flint H. J. (2009). Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol. Lett. 294, 1–8. 10.1111/j.1574-6968.2009.01514.x
    1. Louis P., Hold G. L., Flint H. J. (2014). The gut microbiota, bacterial metabolites and colorectal cancer. Nat. Rev. Microbiol. 12, 661–672. 10.1038/nrmicro3344
    1. Macfarlane G. T., Macfarlane S. (2012). Bacteria, colonic fermentation, and gastrointestinal health. J. AOAC Int. 95, 50–60. 10.5740/jaoacint.SGE_Macfarlane
    1. Macfarlane G. T., Steed H., Macfarlane S. (2008). Bacterial metabolism and health-related effects of galacto-oligosaccharides and other prebiotics. J. Appl. Microbiol. 104, 305–344. 10.1111/j.1365-2672.2007.03520.x
    1. Maes C., Delcour J. A. (2002). Structural characterisation of water-extractable and water-unextractable arabinoxylans in wheat bran. J. Cereal Sci. 35, 315–326. 10.1006/jcrs.2001.0439
    1. Mahowald M. A., Rey F. E., Seedorf H., Turnbaugh P. J., Fulton R. S., Wollam A., et al. . (2009). Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. Proc. Natl. Acad. Sci. U.S.A. 106, 5859–5864. 10.1073/pnas.0901529106
    1. Maki K. C., Gibson G. R., Dickmann R. S., Kendall C. W., Chen C. Y., Costabile A., et al. . (2012). Digestive and physiologic effects of a wheat bran extract, arabino-xylan-oligosaccharide, in breakfast cereal. Nutrition 28, 1115–1121. 10.1016/j.nut.2012.02.010
    1. Marchesi J. R., Holmes E., Khan F., Kochhar S., Scanlan P., Shanahan F., et al. . (2007). Rapid and noninvasive metabonomic characterization of inflammatory bowel disease. J. Proteome Res. 6, 546–551. 10.1021/pr060470d
    1. Marteau P. (2013). Butyrate-producing bacteria as pharmabiotics for inflammatory bowel disease. Gut 62, 1673. 10.1136/gutjnl-2012-304240
    1. Martín R., Miquel S., Chain F., Natividad J. M., Jury J., Lu J., et al. . (2015). Faecalibacterium prausnitzii prevents physiological damages in a chronic low-grade inflammation murine model. BMC Microbiol. 15:67. 10.1186/s12866-015-0400-1
    1. McLaughlin H. P., Motherway M. O., Lakshminarayanan B., Stanton C., Paul Ross R., Brulc J., et al. . (2015). Carbohydrate catabolic diversity of bifidobacteria and lactobacilli of human origin. Int. J. Food Microbiol. 203, 109–121. 10.1016/j.ijfoodmicro.2015.03.008
    1. Mendis M., Simsek S. (2013). Arabinoxylans and human health. Food Hydrocoll. 42, 239–243. 10.1016/j.foodhyd.2013.07.022
    1. Miquel S., Martín R., Bridonneau C., Robert V., Sokol H., Bermúdez-Humarán L. G., et al. . (2014). Ecology and metabolism of the beneficial intestinal commensal bacterium Faecalibacterium prausnitzii. Gut Microbes 5, 146–151. 10.4161/gmic.27651
    1. Moens F., Weckx S., De Vuyst L. (2016). Bifidobacterial inulin-type fructan degradation capacity determines cross-feeding interactions between bifidobacteria and Faecalibacterium prausnitzii. Int. J. Food Microbiol. 231, 76–85 10.1016/j.ijfoodmicro.2016.05.015
    1. Morgan X. C., Tickle T. L., Sokol H., Gevers D., Devaney K. L., Ward D. V., et al. . (2012). Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 13:R79. 10.1186/gb-2012-13-9-r79
    1. NCBI Resource Coordinators (2014). Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 42, D7–D17. 10.1093/nar/gkt1146
    1. Nemoto H., Kataoka K., Ishikawa H., Ikata K., Arimochi H., Iwasaki T., et al. . (2012). Reduced diversity and imbalance of fecal microbiota in patients with ulcerative colitis. Dig. Dis. Sci. 57, 2955–2964. 10.1007/s10620-012-2236-y
    1. Neyrinck A. M., Possemiers S., Druart C., van de Wiele T., De Backer F., Cani P. D., et al. . (2011). Prebiotic effects of wheat arabinoxylan related to the increase in bifidobacteria, Roseburia and Bacteroides/Prevotella in diet-induced obese mice. PLoS ONE 6:e20944. 10.1371/journal.pone.0020944
    1. Neyrinck A. M., Van Hée V. F., Piront N., De Backer F., Toussaint O., Cani P. D., et al. . (2012). Wheat-derived arabinoxylan oligosaccharides with prebiotic effect increase satietogenic gut peptides and reduce metabolic endotoxemia in diet-induced obese mice. Nutr. Diabetes 2, e28. 10.1038/nutd.2011.24
    1. Nielsen T. S., Lærke H. N., Theil P. K., Sørensen J. F., Saarinen M., Forssten S., et al. . (2014). Diets high in resistant starch and arabinoxylan modulate digestion processes and SCFA pool size in the large intestine and faecal microbial composition in pigs. Br. J. Nutr. 112, 1837–1849. 10.1017/S000711451400302X
    1. O'Hara A. M., Shanahan F. (2006). The gut flora as a forgotten organ. EMBO Rep. 7, 688–693. 10.1038/sj.embor.7400731
    1. Omori T., Ueno K., Muramatsu K., Kikuchi M., Onodera S., Shiomi N. (2010). Characterization of recombinant β-fructofuranosidase from Bifidobacterium adolescentis G1. Chem. Centr. J. 4:9. 10.1186/1752-153X-4-9
    1. Ou J., Sun Z. (2014). Feruloylated oligosaccharides: structure, metabolism and function. J. Funct. Foods 7, 90–100. 10.1016/j.jff.2013.09.028
    1. Palframan R. J., Gibson G. R., Rastall R. A. (2003). Carbohydrate preferences of Bifidobacterium species isolated from the human gut. Curr. Issues Intest. Microbiol. 4, 71–75.
    1. Pamer E. G. (2014). Fecal microbiota transplantation: effectiveness, complexities, and lingering concerns. Mucosal Immunol. 7, 210–214. 10.1038/mi.2013.117
    1. Parche S., Amon J., Jankovic I., Rezzonico E., Beleut M., Barutcu H., et al. . (2007). Sugar transport systems of Bifidobacterium longum NCC2705. J. Mol. Microbiol. Biotechnol. 12, 9–19. 10.1159/000096455
    1. Pastell H., Westermann P., Meyer A. S., Tuomainen P., Tenkanen M. (2009). In vitro fermentation of arabinoxylan-derived carbohydrates by bifidobacteria and mixed faecal microbiota. J. Agric. Food Chem. 57, 8598–8606. 10.1021/jf901397b
    1. Pokusaeva K., Fitzgerald G. F., van Sinderen D. (2011). Carbohydrate metabolism in Bifidobacteria. Genes Nutr. 6, 285–306. 10.1007/s12263-010-0206-6
    1. Pollet A., Van Craeyveld V., Van de Wiele T., Verstraete W., Delcour J. A., Courtin C. M. (2012). In vitro fermentation of arabinoxylan oligosaccharides and low molecular mass arabinoxylans with different structural properties from wheat (Triticum aestivum L.) bran and psyllium (Plantago ovata Forsk) seed husk. J. Agric. Food Chem. 60, 946–954. 10.1021/jf203820j
    1. The Human Microbiome Project Consortium (2012). Structure, function and diversity of the healthy human microbiome. Nature 486, 207–214. 10.1038/nature11234
    1. Qiu X., Zhang M., Yang X., Hong N., Yu C. (2013). Faecalibacterium prausnitzii upregulates regulatory T cells and anti-inflammatory cytokines in treating TNBS-induced colitis. J. Crohns Colitis 7, e558–e568. 10.1016/j.crohns.2013.04.002
    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. 10.1136/gutjnl-2014-307649
    1. Richards L. B., Li M., van Esch B. C. A. M., Garssen J., Folkerts G. (2016). The effects of short-chain fatty acids on the cardiovascular system. Pharma Nutr. 4, 68–111. 10.1016/j.phanu.2016.02.001
    1. Ridaura V. K., Faith J. J., Rey F. E., Cheng J., Duncan A. E., Kau A. L., et al. . (2013). Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341:1241214. 10.1126/science.1241214
    1. Rivière A., Gagnon M., Weckx S., Roy D., De Vuyst L. (2015). Mutual cross-feeding interactions between Bifidobacterium longum NCC2705 and Eubacterium rectale ATCC 33656 explain the bifidogenic and butyrogenic effects of arabinoxylan-oligosaccharides. Appl. Environ. Microbiol. 81, 7767–7781. 10.1128/AEM.02089-15
    1. Rivière A., Moens F., Selak M., Maes D., Weckx S., De Vuyst L. (2014). The ability of bifidobacteria to degrade arabinoxylan oligosaccharide constituents and derived oligosaccharides is strain dependent. Appl. Environ. Microbiol. 80, 204–217. 10.1128/AEM.02853-13
    1. Roberfroid M. B. (2005). Introducing inulin-type fructans. Br. J. Nutr. 93, S13–S25. 10.1079/bjn20041350
    1. Roberfroid M. B. (2007). Inulin-type fructans: functional food ingredients. J. Nutr. 137, 2493–2502. 10.1201/9780203504932
    1. Rossi M., Amaretti A. (2011). Probiotic properties of bifidobacteria in Bifidobacteria, Genomics and Molecular Aspects, eds Mayo B., van Sinderen D. (Norwich: Caister Academic Press; ), 97–123.
    1. Saez-Lara M. J., Gomez-Llorente C., Plaza-Diaz J., Gil A. (2015). The role of probiotic lactic acid bacteria and bifidobacteria in the prevention and treatment of inflammatory bowel disease and other related diseases: a systematic review of randomized human clinical trials. Biomed. Res. Int. 2015:505878. 10.1155/2015/505878
    1. Salminen S., van Loveren H. (2012). Probiotics and prebiotics: health claim substantiation. Microb. Ecol. Health Dis. 23:18568. 10.3402/mehd.v23i0.18568
    1. Sanchez J. I., Marzorati M., Grootaert C., Baran M., Van Craeyveld V., Courtin C. M., et al. . (2009). Arabinoxylan-oligosaccharides (AXOS) affect the protein/carbohydrate fermentation balance and microbial population dynamics of the simulator of human intestinal microbial ecosystem. Microb. Biotechnol. 2, 101–113. 10.1111/j.1751-7915.2008.00064.x
    1. Schaafsma G., Slavin J. L. (2015). Significance of inulin fructans in the human diet. Compr. Rev. Food Sci. Food Saf. 14, 37–47. 10.1111/1541-4337.12119
    1. Schell M. A., Karmirantzou M., Snel B., Vilanova D., Berger B., Pessi G., et al. . (2002). The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc. Natl. Acad. Sci. U.S.A. 99, 14422–14427. 10.1073/pnas.212527599
    1. Scott K. P., Antoine J. M., Midtvedt T., van Hemert S. (2015). Manipulating the gut microbiota to maintain health and treat disease. Microb. Ecol. Health Dis. 26, 25877. 10.3402/mehd.v26.25877
    1. Scott K. P., Martin J. C., Chassard C., Clerget M., Potrykus J., Campbell G., et al. (2011). Substrate-driven gene expression in Roseburia inulinivorans: importance of inducible enzymes in the utilization of inulin and starch. Proc. Natl. Acad. Sci. U.S.A. 1, 4672–4679. 10.1073/pnas.1000091107
    1. Scott K. P., Martin J. C., Duncan S. H., Flint H. J. (2014). Prebiotic stimulation of human colonic butyrate-producing bacteria and bifidobacteria, in vitro. FEMS Microbiol. Ecol. 87, 30–40. 10.1111/1574-6941.12186
    1. Selak M., Rivière A., Moens F., Van den Abbeele P., Geirnaert A., Rogelj I., et al. . (2016). Inulin-type fructan fermentation by bifidobacteria depends on the strain rather than the species and region in the human intestine. Appl. Microbiol. Biotechnol. 100, 4097–4107. 10.1007/s00253-016-7351-9
    1. Sharon G., Garg N., Debelius J., Knight R., Dorrestein P. C., Mazmanian S. K. (2014). Specialized metabolites from the microbiome in health and disease. Cell Metab. 20, 719–730. 10.1016/j.cmet.2014.10.016
    1. Slavin J. (2013). Fiber and prebiotics: mechanisms and health benefits. Nutrients 5, 1417–1435. 10.3390/nu5041417
    1. Snelders J., Olaerts H., Dornez E., Van de Wiele T., Aura A. M., Vanhaecke L., et al. (2014). Structural features and feruloylation modulate the fermentability and evolution of antioxidant properties of arabinoxylanoligosaccharides during in vitro fermentation by human gut derived microbiota. J. Funct. Foods 10, 1–12. 10.1016/j.jff.2014.05.011
    1. Sommer F., Bäckhed F. (2013). The gut microbiota - masters of host development and physiology. Nat. Rev. Microbiol. 11, 227–238. 10.1038/nrmicro2974
    1. Swennen K., Courtin C. M., Lindemans G. C. J. E., Delcour J. A. (2006). Large-scale production and characterisation of wheat bran arabinoxylooligosaccharides. J. Sci. Food Agric. 86, 1722–1731. 10.1002/jsfa.2470
    1. Tannock G. W. (2010). Analysis of bifidobacterial populations in bowel ecology studies in Bifidobacteria, Genomics and Molecular Aspects, eds Mayo B., van Sinderen D. (Norwich: Caister Academic Press; ), 1–15.
    1. Tap J., Mondot S., Levenez F., Pelletier E., Caron C., Furet J. P., et al. . (2009). Towards the human intestinal microbiota phylogenetic core. Environ. Microbiol. 11, 2574–2584. 10.1111/j.1462-2920.2009.01982.x
    1. Tojo R., Suárez A., Clemente M. G., de los Reyes-Gavilán C. G., Margolles A., Gueimonde M., et al. . (2014). Intestinal microbiota in health and disease: role of bifidobacteria in gut homeostasis. World J. Gastroenterol. 20, 15163–15176. 10.3748/wjg.v20.i41.15163
    1. Tralongo P., Tomasello G., Sinagra E., Damiani P., Leone A., Palumbo V. D., et al. (2014). The role of butyric acid as a protective agent against inflammatory bowel diseases. Euromediterranean Biomed. J. 9, 24–35. 10.3269/1970-5492.2014.9.4
    1. Tuohy K. M., Scott K. P. (2015). The microbiota of the human gastrointestinal tract: a molecular view in Diet-Microbe Interactions in the Gut, eds Tuohy K. M., Del Rio D. (London: Elsevier; ), 1–15.
    1. Turroni F., Özcan E., Milani C., Mancabelli L., Viappiani A., van Sinderen D., et al. . (2015). Glycan cross-feeding activities between bifidobacteria under in vitro conditions. Front. Microbiol. 6:1030. 10.3389/fmicb.2015.01030
    1. Turroni F., Foroni E., Pizzetti P., Giubellini V., Ribbera A., Merusi P., et al. . (2009). Exploring the diversity of the bifidobacterial population in the human intestinal tract. Appl. Environ. Microbiol. 75, 1534–1545. 10.1128/AEM.02216-08
    1. Turroni F., Peano C., Pass D. A., Foroni E., Severgnini M., Claesson M. J., et al. . (2012). Diversity of bifidobacteria within the infant gut microbiota. PLoS ONE 7:e36957. 10.1371/journal.pone.0036957
    1. Van Craeyveld V., Swennen K., Dornez E., Van de Wiele T., Marzorati M., Verstraete W., et al. . (2008). Structurally different wheat-derived arabinoxylooligosaccharides have different prebiotic and fermentation properties in rats. J. Nutr. 138, 2348–2355. 10.3945/jn.108.094367
    1. Van den Abbeele P., Belzer C., Goossens M., Kleerebezem M., De Vos W. M., Thas O., et al. . (2013a). Butyrate-producing Clostridium cluster XIVa species specifically colonize mucins in an in vitro gut model. ISME J. 7, 949–961. 10.1038/ismej.2012.158
    1. Van den Abbeele P., Gerard P., Rabot S., Bruneau A., El Aidy S., Derrien M., et al. . (2011). Arabinoxylans and inulin differentially modulate the mucosal and luminal gut microbiota and mucin-degradation in humanized rats. Environ. Microbiol. 13, 2667–2680. 10.1111/j.1462-2920.2011.02533.x
    1. Van den Abbeele P., Verstraete W., El Aidy S., Geirnaert A., Van de Wiele T. (2013b). Prebiotics, faecal transplants and microbial network units to stimulate biodiversity of the human gut microbiome. Microb. Biotechnol. 6, 335–340. 10.1111/1751-7915.12049
    1. van den Broek L. A. M., Hinz S. W. A., Beldman G., Vincken J. P., Voragen A. G. J. (2008). Bifidobacterium carbohydrases - their role in breakdown and synthesis of (potential) prebiotics. Nutr. Food. Res. 52, 146–163. 10.1002/mnfr.200700121
    1. van den Broek L. A. M., Voragen A. G. J. (2008). Bifidobacterium glycoside hydrolases and (potential) prebiotics. Innov. Food Sci. Emerg. Technol. 9, 401–407. 10.1016/j.ifset.2007.12.006
    1. Van der Meulen R., Adriany T., Verbrugghe K., De Vuyst L. (2006a). Kinetic analysis of bifidobacterial metabolism reveals a minor role for succinic acid in the regeneration of NAD+ through its growth-associated production. Appl. Environ. Microbiol. 72, 5204–5210. 10.1128/AEM.00146-06
    1. Van der Meulen R., Avonts L., De Vuyst L. (2004). Short fractions of oligofructose are preferentially metabolized by Bifidobacterium animalis DN-173 010. Appl. Environ. Microbiol. 70, 1923–1930. 10.1128/AEM.70.4.1923-1930.2004
    1. Van der Meulen R., Makras L., Verbrugghe K., Adriany T., De Vuyst L. (2006b). In vitro kinetic analysis of oligofructose consumption by Bacteroides and Bifidobacterium spp. indicates different degradation mechanisms. Appl. Environ. Microbiol. 72, 1006–1012. 10.1128/AEM.72.2.1006-1012.2006
    1. Van Laere K. M. J., Hartemink R., Bosveld M., Schols H. A., Voragen A. G. J. (2000). Fermentation of plant cell wall derived polysaccharides and their corresponding oligosaccharides by intestinal bacteria. J. Agric. Food Chem. 48, 1644–1652. 10.1021/jf990519i
    1. Velasquez-Manoff M. (2015). Gut microbiome: the peacekeepers. Nature 518, S3–S11. 10.1038/518S3a
    1. Ventura M., O'Flaherty S., Claesson M. J., Turroni F., Klaenhammer T. R., van Sinderen D., et al. . (2009). Genome-scale analyses of health-promoting bacteria: probiogenomics. Nat. Rev. Microbiol. 7, 61–71. 10.1038/nrmicro2047
    1. Ventura M., Turroni F., Bottacini F., Giubellini V., van Sinderen D. (2011). Bifidobacterial ecology and comparative genomics: perspectives and prospects, in Bifidobacteria, Genomics and Molecular Aspects, eds Mayo B., van Sinderen D. (Norwich: Caister Academic Press; ), 31–44.
    1. Ventura M., Turroni F., Lugli G. A., van Sinderen D. (2014). Bifidobacteria and humans: our special friends, from ecological to genomics perspectives. J. Sci. Food Agric. 94, 163–168. 10.1002/jsfa.6356
    1. Verbeke K. (2014). Prebiotics and synbiotics: how do they affect health? in Clinical Insights: Probiotics, Prebiotics and Gut Health, eds Floch M. H., Kim A. (London: Future Medicine Ltd.), 47–61.
    1. Verspreet J., Damen D., Broekaert W. F., Verbeke K., Delcour J. A., Courtin C. M. (2016). A critical look at prebiotics within the dietary fiber concept. Annu. Rev. Food Sci. Technol. 7, 167–190. 10.1146/annurev-food-081315-032749
    1. Vital M., Howe A. C., Tiedje J. M. (2014). Revealing the bacterial butyrate synthesis pathways by analyzing (meta)genomic data. MBio 5, e00889–e00814. 10.1128/mBio.00889-14
    1. Vrieze A., Van Nood E., Holleman F., Salojärvi J., Kootte R. S., Bartelsman J. F., et al. . (2012). Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143, 913–916. 10.1053/j.gastro.2012.06.031
    1. Walker A. W., Duncan S. H., Louis P., Flint H. J. (2014). Phylogeny, culturing, and metagenomics of the human gut microbiota. Trends Microbiol. 22, 267–274. 10.1016/j.tim.2014.03.001
    1. Walton G. E., Lu C., Trogh I., Arnaut F., Gibson G. R. (2012). A randomised, double-blind, placebo controlled cross-over study to determine the gastrointestinal effects of consumption of arabinoxylan-oligosaccharides enriched bread in healthy volunteers. Nutr. J. 11:36. 10.1186/1475-2891-11-36
    1. Warchol M., Perrin S., Grill J. P., Schneider F. (2002). Characterization of a purified beta-fructofuranosidase from Bifidobacterium infantis ATCC 15697. Lett. Appl. Microbiol. 35, 462–467. 10.1046/j.1472-765X.2002.01224.x
    1. Whitman W. B., Coleman D. C., Wiebe W. J. (1998). Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. U.S.A. 95, 6578–6583. 10.1073/pnas.95.12.6578
    1. Wikoff W. R., Anfora A. T., Liu J., Schultz P. G., Lesley S. A., Peters E. C., et al. . (2009). Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc. Natl. Acad. Sci. U.S.A. 106, 3698–3703. 10.1073/pnas.0812874106
    1. Wu N., Yang X., Zhang R., Li J., Xiao X., Hu Y., et al. . (2013). Dysbiosis signature of fecal microbiota in colorectal cancer patients. Microb. Ecol. 66, 462–470. 10.1007/s00248-013-0245-9
    1. Xu M. Q., Cao H. L., Wang W. Q., Wang S., Cao X. C., Yan F., et al. . (2015). Fecal microbiota transplantation broadening its application beyond intestinal disorders. World J. Gastroenterol. 21, 102–111. 10.3748/wjg.v21.i1.102
    1. Yang J., Martínez I., Walter J., Keshavarzian A., Rose D. J. (2013). In vitro characterization of the impact of selected dietary fibers on fecal microbiota composition and short chain fatty acid production. Anaerobe 23, 74–81. 10.1016/j.anaerobe.2013.06.012
    1. Zoetendal E. G., Raes J., van den Bogert B., Arumugam M., Booijink C. C., 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. 10.1038/ismej.2011.212

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe