Front Microbiol. 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.
Frontiers in microbiology
Audrey Rivière, Marija Selak, David Lantin, Frédéric Leroy, Luc De Vuyst
Affiliations
Affiliations
- Research Group of Industrial Microbiology and Food Biotechnology, Faculty of Sciences and Bioengineering Sciences, Vrije Universiteit Brussel Brussels, Belgium.
PMID: 27446020
PMCID: PMC4923077 DOI: 10.3389/fmicb.2016.00979
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
References
- BMC Microbiol. 2014 Nov 25;14:282 - PubMed
- Int J Food Microbiol. 2016 Aug 16;231:76-85 - PubMed
- Appl Environ Microbiol. 2006 Dec;72(12):7835-41 - PubMed
- Science. 2012 Jun 8;336(6086):1209 - PubMed
- Proc Natl Acad Sci U S A. 2002 Oct 29;99(22):14422-7 - PubMed
- J Mol Microbiol Biotechnol. 2007;12(1-2):9-19 - PubMed
- ISME J. 2013 May;7(5):949-61 - PubMed
- Environ Microbiol. 2009 Oct;11(10):2574-84 - PubMed
- Br J Nutr. 2014 Dec 14;112(11):1837-49 - PubMed
- Genome Biol. 2012 Apr 16;13(9):R79 - PubMed
- Appl Microbiol Biotechnol. 2014 Jan;98(2):563-77 - PubMed
- Nat Rev Microbiol. 2014 Oct;12(10):661-72 - PubMed
- EMBO Rep. 2006 Jul;7(7):688-93 - PubMed
- Nutr Diabetes. 2012 Jan 23;2:e28 - PubMed
- Sci Transl Med. 2014 Nov 19;6(263):263ra158 - PubMed
- Proc Natl Acad Sci U S A. 2011 Mar 15;108 Suppl 1:4672-9 - PubMed
- Curr Opin Gastroenterol. 2015 Mar;31(2):153-8 - PubMed
- Cell Metab. 2014 Nov 4;20(5):719-30 - PubMed
- Appl Environ Microbiol. 2003 Nov;69(11):6354-60 - PubMed
- J Agric Food Chem. 2003 Mar 26;51(7):2026-33 - PubMed
- Gut. 2014 Feb;63(2):367 - PubMed
- Curr Opin Biotechnol. 2015 Apr;32:21-7 - PubMed
- Appl Environ Microbiol. 2006 Aug;72(8):5204-10 - PubMed
- BMC Microbiol. 2015 Mar 21;15:67 - PubMed
- Nature. 2011 May 12;473(7346):174-80 - PubMed
- Nat Rev Gastroenterol Hepatol. 2014 Aug;11(8):506-14 - PubMed
- Crit Rev Food Sci Nutr. 2011 Feb;51(2):178-94 - PubMed
- Br J Nutr. 2005 Apr;93 Suppl 1:S13-25 - PubMed
- Microb Ecol Health Dis. 2012 Jun 18;23:null - PubMed
- FEMS Microbiol Rev. 2005 Aug;29(3):491-509 - PubMed
- J Proteome Res. 2007 Feb;6(2):546-51 - PubMed
- Science. 2016 Apr 29;352(6285):586-9 - PubMed
- Nature. 2013 Aug 29;500(7464):541-6 - PubMed
- Biol Psychiatry. 2013 Nov 15;74(10):720-6 - PubMed
- Clin Microbiol Infect. 2014 Nov;20(11):1098-105 - PubMed
- Int J Food Microbiol. 2011 Sep 1;149(1):73-80 - PubMed
- J Psychiatr Res. 2015 Apr;63:1-9 - PubMed
- Microb Ecol Health Dis. 2015 Feb 02;26:25877 - PubMed
- Nature. 2015 Feb 26;518(7540):S3-11 - PubMed
- J Appl Microbiol. 2008 Feb;104(2):305-44 - PubMed
- Appl Microbiol Biotechnol. 2010 Aug;87(6):2257-66 - PubMed
- Anaerobe. 2014 Dec;30:70-4 - PubMed
- Proc Natl Acad Sci U S A. 2009 Apr 7;106(14):5859-64 - PubMed
- Gastroenterol Hepatol (N Y). 2014 Apr;10(4):230-7 - PubMed
- Appl Environ Microbiol. 2014 Jan;80(1):204-17 - PubMed
- Gastroenterology. 2012 Oct;143(4):913-6.e7 - PubMed
- Int J Syst Bacteriol. 1997 Apr;47(2):590-2 - PubMed
- Mol Microbiol. 2011 Jan;79(2):292-304 - PubMed
- Environ Microbiol. 2011 Oct;13(10):2667-80 - PubMed
- Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):6578-83 - PubMed
- Science. 2013 Sep 6;341(6150):1241214 - PubMed
- PLoS One. 2011;6(6):e20944 - PubMed
- Nature. 2012 Jun 13;486(7402):207-14 - PubMed
- Nutr J. 2012 Jun 01;11:36 - PubMed
- Mucosal Immunol. 2014 Mar;7(2):210-4 - PubMed
- Science. 2013 Jul 5;341(6141):1237439 - PubMed
- Gut. 2016 Mar;65(3):415-25 - PubMed
- FEMS Microbiol Ecol. 2007 Jul;61(1):121-31 - PubMed
- Mol Nutr Food Res. 2008 Jan;52(1):146-63 - PubMed
- Bioessays. 2013 Oct;35(10):913-23 - PubMed
- Appl Environ Microbiol. 2009 Apr;75(8):2312-9 - PubMed
- Gut Microbes. 2016 Jul 3;7(4):323-328 - PubMed
- Appl Environ Microbiol. 2009 Mar;75(6):1534-45 - PubMed
- Biochim Biophys Acta. 2010 Nov;1801(11):1175-83 - PubMed
- FEMS Microbiol Ecol. 2009 Aug;69(2):231-42 - PubMed
- Best Pract Res Clin Gastroenterol. 2013 Feb;27(1):73-83 - PubMed
- Trends Microbiol. 2014 May;22(5):267-74 - PubMed
- Lett Appl Microbiol. 2002;35(6):462-7 - PubMed
- Nutr Res Rev. 2004 Dec;17(2):259-75 - PubMed
- Maturitas. 2013 May;75(1):44-50 - PubMed
- Int J Syst Evol Microbiol. 2016 Jan 05;:null - PubMed
- J Sci Food Agric. 2014 Jan 30;94(2):163-8 - PubMed
- Front Microbiol. 2015 Sep 24;6:1030 - PubMed
- Nat Rev Microbiol. 2012 Nov;10(11):735-42 - PubMed
- Int J Syst Evol Microbiol. 2014 Sep;64(Pt 9):3134-9 - PubMed
- Appl Environ Microbiol. 2009 Sep;75(18):5884-92 - PubMed
- Anaerobe. 2013 Oct;23:74-81 - PubMed
- Nat Rev Microbiol. 2013 Apr;11(4):227-38 - PubMed
- Curr Opin Biotechnol. 2016 Feb;37:1-7 - PubMed
- Biomed Res Int. 2015;2015:169381 - PubMed
- Appl Environ Microbiol. 2006 Feb;72(2):1006-12 - PubMed
- Biotechnol Adv. 2014 Mar-Apr;32(2):316-32 - PubMed
- Glob Change Biol Bioenergy. 2009 Feb 18;1(1):2-17 - PubMed
- J Sci Food Agric. 2011 Jun;91(8):1341-8 - PubMed
- Nat Rev Gastroenterol Hepatol. 2015 May;12(5):303-10 - PubMed
- Nucleic Acids Res. 2014 Jan;42(Database issue):D7-17 - PubMed
- Biochem Biophys Res Commun. 2010 Nov 26;402(4):644-50 - PubMed
- Appl Environ Microbiol. 2014 Apr;80(8):2564-72 - PubMed
- Microb Biotechnol. 2013 Jul;6(4):335-40 - PubMed
- Biomed Res Int. 2014;2014:960826 - PubMed
- Nucleic Acids Res. 2014 Jan;42(Database issue):D490-5 - PubMed
- Diabetes. 2008 Jun;57(6):1470-81 - PubMed
- J Perinatol. 2014 Aug;34(8):599-605 - PubMed
- J Biosci Bioeng. 2013 Aug;116(2):265-70 - PubMed
- PLoS One. 2012;7(5):e36957 - PubMed
- Biomed Res Int. 2015;2015:505878 - PubMed
- J Appl Microbiol. 2005;98(6):1303-15 - PubMed
- Benef Microbes. 2011 Jun;2(2):103-14 - PubMed
- Aliment Pharmacol Ther. 2008 Jan 15;27(2):104-19 - PubMed
- Gut. 2013 Dec;62(12):1745-52 - PubMed
- Diabetes. 2011 Nov;60(11):2775-86 - PubMed
- Int J Food Microbiol. 2015 Jun 16;203:109-21 - PubMed
- Gut Microbes. 2014 Mar-Apr;5(2):146-51 - PubMed
- Chem Cent J. 2010 Apr 12;4:9 - PubMed
- Microb Ecol. 2013 Apr;65(3):763-72 - PubMed
- Annu Rev Food Sci Technol. 2016;7:167-90 - PubMed
- J Crohns Colitis. 2013 Dec;7(11):e558-68 - PubMed
- Br J Nutr. 2010 Mar;103(5):703-13 - PubMed
- Curr Issues Intest Microbiol. 2003 Sep;4(2):71-5 - PubMed
- MBio. 2014 Apr 22;5(2):e00889 - PubMed
- FEMS Microbiol Ecol. 2014 Jan;87(1):30-40 - PubMed
- Microb Cell Fact. 2014 Aug 29;13 Suppl 1:S4 - PubMed
- J Appl Microbiol. 2014 Mar;116(3):477-91 - PubMed
- Curr Opin Biotechnol. 2015 Apr;32:99-103 - PubMed
- J Agric Food Chem. 2012 Feb 1;60(4):946-54 - PubMed
- Science. 2005 Mar 25;307(5717):1915-20 - PubMed
- Proc Natl Acad Sci U S A. 2009 Mar 10;106(10):3698-703 - PubMed
- Appl Environ Microbiol. 2015 Nov;81(22):7767-81 - PubMed
- Trends Biotechnol. 2015 Apr;33(4):195-6 - PubMed
- Appl Environ Microbiol. 2004 Oct;70(10):5810-7 - PubMed
- J Agric Food Chem. 2009 Sep 23;57(18):8598-606 - PubMed
- Microb Biotechnol. 2013 Jul;6(4):316-25 - PubMed
- MBio. 2015 Apr 14;6(2):null - PubMed
- Proc Natl Acad Sci U S A. 2014 Feb 11;111(6):2247-52 - PubMed
- J Agric Food Chem. 2007 May 30;55(11):4589-95 - PubMed
- Curr Microbiol. 2003 Jun;46(6):391-7 - PubMed
- Int J Food Microbiol. 2012 Apr 16;155(3):234-40 - PubMed
- J Nutr. 2008 Dec;138(12):2348-55 - PubMed
- World J Gastroenterol. 2015 Jan 7;21(1):102-11 - PubMed
- Environ Microbiol. 2009 Aug;11(8):2112-22 - PubMed
- Nat Rev Microbiol. 2013 Jul;11(7):497-504 - PubMed
- FEMS Microbiol Ecol. 2011 Jul;77(1):107-19 - PubMed
- FEMS Microbiol Lett. 2009 May;294(1):1-8 - PubMed
- ISME J. 2012 Jul;6(7):1415-26 - PubMed
- Dig Dis Sci. 2012 Nov;57(11):2955-64 - PubMed
- Appl Microbiol Biotechnol. 2011 Dec;92(6):1179-85 - PubMed
- Genes Nutr. 2011 Aug;6(3):285-306 - PubMed
- Microb Biotechnol. 2009 Jan;2(1):101-13 - PubMed
- Nutr Rev. 2012 Aug;70 Suppl 1:S45-56 - PubMed
- J Agric Food Chem. 2000 May;48(5):1644-52 - PubMed
- Nat Rev Microbiol. 2009 Jan;7(1):61-71 - PubMed
- Gut. 2013 Dec;62(12):1673 - PubMed
- World J Gastroenterol. 2014 Nov 7;20(41):15163-76 - PubMed
- Appl Environ Microbiol. 2009 Jan;75(2):454-61 - PubMed
- Appl Environ Microbiol. 2006 May;72(5):3593-9 - PubMed
- Cell Host Microbe. 2014 Mar 12;15(3):382-92 - PubMed
- Nutr J. 2015 Feb 08;14:16 - PubMed
- Nutrition. 2012 Nov-Dec;28(11-12):1115-21 - PubMed
- Appl Microbiol Biotechnol. 2016 May;100(9):4097-107 - PubMed
- Nutrients. 2013 Apr 22;5(4):1417-35 - PubMed
- Appl Environ Microbiol. 2004 Apr;70(4):1923-30 - PubMed
- Microb Ecol. 2013 Aug;66(2):462-70 - PubMed
- J AOAC Int. 2012 Jan-Feb;95(1):50-60 - PubMed
- Mol Nutr Food Res. 2011 Dec;55(12):1862-74 - PubMed
- J Nutr. 2007 Nov;137(11 Suppl):2493S-2502S - PubMed
Publication Types