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Review
. 2016 Jun 28:7:979.
doi: 10.3389/fmicb.2016.00979. eCollection 2016.

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

Audrey Rivière  1 , Marija Selak  1 , David Lantin  1 , Frédéric Leroy  1 , Luc De Vuyst  1
Affiliations
Review

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

Audrey Rivière et al. Front Microbiol. .

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.

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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 (—).
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