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Contribution of acetate to butyrate formation by human faecal bacteria

Published online by Cambridge University Press:  09 March 2007

Sylvia H. Duncan ,
Grietje Holtrop ,
Gerald E. Lobley ,
A. Graham Calder ,
Colin S. Stewart  and
Harry J. Flint
Sylvia H. Duncan
Affiliation:
Gut Microbiology and Immunology Division, Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK
Grietje Holtrop
Affiliation:
Biomathematics and Statistics Scotland, Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK
Gerald E. Lobley
Affiliation:
Gut Microbiology and Immunology Division, Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK
A. Graham Calder
Affiliation:
Gut Microbiology and Immunology Division, Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK
Colin S. Stewart
Affiliation:
Gut Microbiology and Immunology Division, Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK
Harry J. Flint*
Affiliation:
Gut Microbiology and Immunology Division, Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK
*
*Corresponding author: Professor Harry J. Flint, fax +44 1224 716687, email [email protected]
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Abstract

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Acetate is normally regarded as an endproduct of anaerobic fermentation, but butyrate-producing bacteria found in the human colon can be net utilisers of acetate. The butyrate formed provides a fuel for epithelial cells of the large intestine and influences colonic health. [1-13C]Acetate was used to investigate the contribution of exogenous acetate to butyrate formation. Faecalibacterium prausnitzii and Roseburia spp. grown in the presence of 60 mm-acetate and 10 mm-glucose derived 85–90 % butyrate-C from external acetate. This was due to rapid interchange between extracellular acetate and intracellular acetyl-CoA, plus net acetate uptake. In contrast, a Coprococcus-related strain that is a net acetate producer derived only 28 % butyrate-C from external acetate. Different carbohydrate-derived energy sources affected butyrate formation by mixed human faecal bacteria growing in continuous or batch cultures. The ranking order of butyrate production rates was amylopectin > oat xylan > shredded wheat > inulin > pectin (continuous cultures), and inulin > amylopectin > oat xylan > shredded wheat > pectin (batch cultures). The contribution of external acetate to butyrate formation in these experiments ranged from 56 (pectin) to 90 % (xylan) in continuous cultures, and from 72 to 91 % in the batch cultures. This is consistent with a major role for bacteria related to F. prausnitzii and Roseburia spp. in butyrate formation from a range of substrates that are fermented in the large intestine. Variations in the dominant metabolic type of butyrate producer between individuals or with variations in diet are not ruled out, however, and could influence butyrate supply in the large intestine.

Keywords

Roseburia intestinalisFaecalibacterium prausnitziiButyrate synthesisAcetateStable isotopeColon
Type
Research Article
Information
British Journal of Nutrition , Volume 91 , Issue 6 , June 2004 , pp. 915 - 923
Copyright
Copyright © The Nutrition Society 2004

References

Avivi-Green, C, Polak-Charson, S, Madar, Z & Schwartz, B (2000) Apoptosis cascade proteins are regulated in vivo by high intracolonic butyrate concentration: correlation with colon cancer inhibition. Oncol Res 12, 83–95.CrossRefGoogle ScholarPubMed
Barcenilla, A, Pryde, SE, Martin, JC, Duncan, SH, Stewart, CS, Henderson, C & Flint, HJ (2000) Phylogenetic relationships of dominant butyrate producing bacteria from the human gut. Appl Environ Microbiol 66, 1654–1661.CrossRefGoogle Scholar
Bryant, MP (1972) Commentary on the Hungate technique for cultivation of anaerobic bacteria. Am J Clin Nutr 25, 1324–1328.CrossRefGoogle Scholar
Calder, AG, Garden, KE, Anderson, SE & Lobley, GE (1999) Quantitation of blood and plasma amino acids using isotope dilution electron impact gas chromotography/mass spectrometry with U-13C amino acids as internal standards. Rapid Commun Mass Spectrom 13, 2080–2083.3.0.CO;2-O>CrossRefGoogle Scholar
Cavaglieri, C, Nishiyama, A, Fernandes, LC, Curi, R, Miles, EA & Calder, PC (2003) Differential effects of short chain fatty acids on proliferation and production of pro- and anti-inflammatory cytokines by cultured lymphocytes. Life Sci 73, 1683–1690.CrossRefGoogle ScholarPubMed
Csordas, A (1996) Butyrate, aspirin and colorectal cancer. Eur J Cancer Prev 5, 221–231.CrossRefGoogle ScholarPubMed
Cummings, HJ (1995) Short chain fatty acids. In Human Colonic Bacteria: Role in Nutrition, Physiology and Pathology, pp. 101–130 [Gibson, GR and Macfarlane, GT]. Boca Raton, FL: CRC Press.Google Scholar
Duncan, SH, Barcenilla, A, Stewart, CS, Pryde, SE & Flint, HJ (2002 a) Acetate utilization and butyryl coenzyme A (CoA): acetate-CoA transferase in butyrate-producing bacteria from the human large intestine. Appl Environ Microbiol 68, 5186–5190.CrossRefGoogle ScholarPubMed
Duncan, SH, Hold, GL, Barcenilla, A, Stewart, CS & Flint, HJ (2002 b) Roseburia intestinalis sp. nov., a novel saccharolytic, butyrate-producing bacterium from human faeces. Int J Syst Evol Microbiol 52, 1615–1620.Google Scholar
Duncan, SH, Hold, GL, Harmsen, HJM, Stewart, CS & Flint, HJ (2002 c) Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as Faecalibacterium prausnitzii gen. nov., comb. nov. Int J Syst Evol Microbiol 52, 2141–2146.Google Scholar
Duncan, SH, Scott, KP, Ramsay, AG, Harmsen, HJM, Welling, GW, Stewart, CS & Flint, HJ (2003) Effects of alternative dietary substrates on competition between human colonic bacteria in an anaerobic fermentor system. Appl Environ Microbiol 69, 1136–1142.CrossRefGoogle Scholar
Englyst, HN, Hay, S & Macfarlane, GT (1987) Polysaccharide breakdown by mixed populations of human fecal bacteria. FEMS Microbiol Ecol 95, 163–171.CrossRefGoogle Scholar
Hague, A, Elder, DJE, Hicks, DJ & Paraskeva, AC (1995) Apoptosis in colorectal tumour cells – induction by the short chain fatty acids butyrate, propionate and acetate and acetate by the bile salt deoxycholate. Int J Cancer 60, 400–406.CrossRefGoogle ScholarPubMed
Hillman, K, Murdoch, TA, Spencer, RJ & Stewart, CS (1994) Inhibition of enterotoxigenic Escherichia coli by the microflora of the porcine ileum, in an in vitro semi-continuous culture system. J Appl Bacteriol 76, 294–300.CrossRefGoogle Scholar
Hold, GL, Schwiertz, A, Aminov, RI, Blaut, M & Flint, HJ (2003) Oligonucleotide probes that detect quantitatively significant groups of butyrate-producing bacteria in human feces. Appl Environ Microbiol 69, 4320–4324.CrossRefGoogle ScholarPubMed
Kleessen, B, Hartmann, L & Blaut, M (2001) Oligofructose and long chain inulin: influence on the gut microbial ecology of rats associated with a human faecal flora. Br J Nutr 86, 291–300.CrossRefGoogle ScholarPubMed
Macfarlane, GT & Gibson, GR (1997) Carbohydrate fermentation, energy transduction and gas metabolism in the human large intestine. In Gastrointestinal Microbiology, vol. 1. pp. 269–318 [Mackie, RI and White, BA, editors]. New York: B. A. Chapman and Hall Microbiology Series.CrossRefGoogle Scholar
Macfarlane, GT, Hay, S & Gibson, GR (1989) Influence of mucin on glycosidase, protease and arylamidase activities of human gut bacteria grown in a 3-stage continuous culture system. J Appl Bacteriol 66, 407–417.CrossRefGoogle Scholar
McIntyre, A, Gibson, PR & Young, GP (1993) Butyrate production from dietary fiber and protection against large bowel cancer in a rat model. Gut 34, 386–391.CrossRefGoogle ScholarPubMed
Mariadason, JM, Corner, GA & Augenlight, LH (2000) Genetic reprogramming in pathways of colonic cell maturation induced by short chain fatty acids: comparison with trichostatin A, sulindac, and curcurmin and implications for chemoprevention of colon cancer. Cancer Res 60, 4561–4572.Google Scholar
Miller, TL & Wolin, MJ (1996) Pathways of acetate, propionate, and butyrate formation by the human fecal microbial flora. Appl Environ Microbiol 62, 1589–1592.CrossRefGoogle ScholarPubMed
Miyazaki, K, Martin, JC, Marinsek-Logar, R & Flint, HJ (1997) Degradation and utilisation of xylans by the rumen anaerobe Prevotella bryantii (formerly P. ruminicola subsp. brevis) B 1 4. Anaerobe 3, 373–381.CrossRefGoogle ScholarPubMed
Pryde, SE, Duncan, SH, Hold, GL, Stewart, CS & Flint, HJ (2002) The microbiology of butyrate formation in the human colon. FEMS Microbiol Letts 217, 133–139.CrossRefGoogle ScholarPubMed
Richardson, AJ, Calder, GC, Stewart, CS & Smith, A (1989) Simultaneous determination of volatile and non-volatile fermentation products of anaerobes by capillary gas chromatography. Lett Appl Microbiol 9, 5–8.CrossRefGoogle Scholar
Scheppach, W, Luehrs, H & Menzel, T (2001) Beneficial health effects of low digestible carbohydrate consumption. Br J Nutr 85, S23–S30.CrossRefGoogle ScholarPubMed
Shipley, RA & Clark, RE (1972) Tracer Methods for In Vivo Kinetics, Theory and Applications. New York: Academic Press, New York.Google Scholar
Suau, A, Rochet, V, Sghir, A, Gramet, G, Breways, S, Sutern, M, Rigottier-Gois, L & Dore, J (2001) Fusobacterium prausnitzii and related species represent a dominant group within the human fecal flora. Syst Appl Microbiol 24, 139–145.CrossRefGoogle ScholarPubMed
Titgemeyer, EC, Bourquin, LD, Fahey, GC Jr & Garleb, KA (1991) Fermentability of various fiber sources by human fecal bacteria in vitro. Am J Clin Nutr 53, 1418–1424.CrossRefGoogle ScholarPubMed
Topping, DL & Clifton, PM (2001) Short chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev 81, 1031–1064.CrossRefGoogle ScholarPubMed
Wachtershauser, A & Stein, J (2000) Rationale for the luminal provision of butyrate in intestinal disease. Eur J Nutr 39, 164–171.Google Scholar
Weaver, GA, Krause, JA, Miller, TL & Wolin, MJ (1992) Cornstarch fermentation by the colonic microbial community yields more butyrate than does cabbage fibre fermentation – cornstarch fermentation rates correlate negatively with methanogenesis. Am J Clin Nutr 55, 70–77.CrossRefGoogle ScholarPubMed
Wolin, MJ, Miller, TJ, Yerry, S, Zhang, YC, Bank, S & Weaver, GA (1999) Changes in fermentation pattern of fecal microbial communities associated with a drug treatment that increases dietary starch in the human colon. Appl Environ Microbiol 65, 2807–2812.CrossRefGoogle Scholar