The role of pH in determining the species composition of the human colonic microbiota

Environmental Microbiology

Volumn 11, Issue 8, 2009, Pages 2112-2122

  Duncan, Sylvia H ^a   Louis, Petra ^a   Thomson, John M ^b   Flint, Harry J ^a  

^a ROWETT RESEARCH INSTITUTE   (United Kingdom)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

STARCH; VOLATILE FATTY ACID;

ARTICLE; CARBOHYDRATE DIET; CLASSIFICATION; COLON; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; GROWTH, DEVELOPMENT AND AGING; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PH;

BASE SEQUENCE; COLON; DIETARY CARBOHYDRATES; FATTY ACIDS, VOLATILE; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIA; HUMANS; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; STARCH;

BACTERIA (MICROORGANISMS); BACTEROIDES; BACTEROIDES SP.; BACTEROIDES THETAIOTAOMICRON; ESCHERICHIA COLI; EUBACTERIUM RECTALE; NEGIBACTERIA; POSIBACTERIA;

EID: 68249110221     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2009.01931.x     Document Type: Article

References (51)

1. Abell, G.C.J., Conlon, M.A. McOrist, A.L. (2006) Methanogenic archaea in adult human faecal samples are inversely related to butyrate concentration. Microb Ecol Heal Dis 18 : 154 160.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215 : 403 410.
3. Aminov, R.I., Walker, A.W., Duncan, S.H., Harmsen, H.J.M., Welling, G.W. Flint, H.J. (2006) Molecular diversity, cultivation, and improved FISH detection of a dominant group of human gut bacteria related to Roseburia and Eubacterium rectale. Appl Environ Microbiol 72 : 6371 6376.
4. Barcenilla, A., Pryde, S.E., Martin, J.C., Duncan, S.H., Stewart, C.S. Flint, H.J. (2000) Phylogenetic relationships of dominant butyrate producing bacteria from the human gut. Appl Environ Microbiol 66 : 1654 1661.
5. Belenguer, A., Duncan, S.H., Holtrop, G., Anderson, S.E., Lobley, G.E. Flint, H.J. (2007) Impact of pH on lactate formation and utilization by human fecal microbial communities. Appl Environ Microbiol 73 : 6526 6533.
6. Bird, A.R., Vuaran, M.S., King, R.A., Noakes, M., Morell, M.K. Topping, D.L. (2008) Wholegrain foods made from novel high-amylose barley variety (Himalaya 292) improve indices of bowel health in human subjects. Br J Nutr 99 : 1032 1040.
7. Bongers, A. van den Heuvel, E.G.H.M. (2003) Prebiotics and the bioavailability of minerals and trace elements. Food Rev Internat 19 : 397 422.
8. Booth, I.R., Cash, P. O'Byrne, C. (2002) Sensing and adapting to acid stress. Ant Van Leeuwenhoek Int J Gen Mol Microbiol 81 : 33 42.
9. Bown, R.L., Gibson, J.A., Sladen, G.E., Hicks, B. Dawson, A.M. (1974) Effects of lactulose and other laxatives on ileal and colonic pH as measured by radiotelemetry device. Gut 1 : 999 1004.
10. Brosius, J., Palmer, M.L., Kennedy, P.J. Noller, H.F. (1978) Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci USA 75 : 4801 4805.
11. Chassard, C., Goumy, V., LeClerc, M., Del'Homme, C. Bernalier Donadille, A. (2007) Characterisation of the xylan-degrading microbial community from human faeces. FEMS Microbiol Letts 242 : 339 344.
12. Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T.J., Higgins, D.G. Thompson, J.D. (2003) Multiple sequence alignment with the Clustal series of programs. Nucl Acids Res 31 : 3497 3500.
13. Chung, Y.C., Hsu, C.K., Ko, C.Y. Chan, Y.C. (2007) Dietary intake of xylooligosaccharides improves the intestinal microbiota, fecal moisture, and pH value in the elderly. Nutr Res 27 : 756 761.
14. Clamp, M., Cuff, J., Searle, S.M. Barton, J. (2004) The jalview java alignment editor. Bioinformatics 20 : 426 427.
15. Cummings, J.H. Macfarlane, G.T. (1991) The control and consequences of bacterial fermentation in the human colon. J Appl Bacteriol 70 : 443 459.
16. Duncan, S.H. (2001) Effects of rumen and gut microorganisms and their metabolites on the growth and survival of Escherichia coli O157. PhD Thesis. Scotland, UK: University of Aberdeen.
17. Duncan, S.H., Hold, G.L., Barcenilla, A., Stewart, C.S. Flint, H.J. (2002) Roseburia intestinalis sp. nov., a novel saccharolytic, butyrate-producing bacterium from human faeces. Int J Syst Evol Microbiol 52 : 1 6.
18. Duncan, S.H., Scott, K.P., Ramsay, A.G., Harmsen, H.J.M., Welling, G.W., Stewart, C.S. Flint, H.J. (2003) Effects of alternative dietary substrates on competition between human colonic bacteria in an anaerobic fermentor system. Appl Environ Microbiol 69 : 1136 1142.
19. 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.
20. Duncan, S.H., Aminov, R.I., Scott, K.P., Louis, P., Stanton, T.B. Flint, H.J. (2006) Proposal of Roseburia faecis sp. nov., Roseburia hominis sp. nov., and Roseburia inulinivorans sp. nov., based on isolates from human faeces. Int J Syst Evol Microbiol 56 : 247 2441.
21. Duncan, S.H., Belenguer, A., Holtrop, G., Johnstone, A.M., Flint, H.J. Lobley, G.E. (2007) Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl Environ Microbiol 73 : 1073 1078.
22. Flint, H.J., Duncan, S.H., Scott, K.P. Louis, P. (2007a) Interactions and competition within the microbial community of the human colon: links between diet and health. Environ Microbiol 9 : 1101 1111.
23. Flint, H.J., Louis, P., Scott, K.P. Duncan, S.H. (2007b) Commensal bacteria in health and disease. In Virulence Mechanisms of Bacterial Pathogens. Brogden, K.A., Minion, C.F., Cornick, N., Stanton, T.B., Zhang, Q., Nolan L.K. Wannemuehler, M.J. (eds). Washington, DC, USA : ASM Press, pp. 101 115.
24. Flint, H.J., Bayer, E.A., Rincon, M.T., Lamed, R. White, B.A. (2008) Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol 6 : 121 131.
25. Gill, C.I.R. Rowland, I.R. (2002) Diet and cancer: assessing the risk. Br J Nutr 88 (Suppl. 1 S73 S87.
26. 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.
27. Kleesen, 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.
28. Lane, D.J. (1991) 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics. Stackebrandt, E. Goodfellow, M. (eds). New York, USA : John Wiley and sons, pp. 115 175.
29. Leitch, E.C.M., Walker, A.W., Duncan, S.H., Holtrop, G. Flint, H.J. (2007) Selective colonization of insoluble substrates by human faecal bacteria. Env Microbiol 9 : 667 679.
30. Lewis, S.J. Heaton, K.W. (1997) Increasing butyrate concentration in the distal colon by accelerating intestinal transit. Gut 41 : 245 225.
31. Louis, P., Duncan, S.H., McCrae, S.I., Millar, J., Jackson, M.S. Flint, H.J. (2004) Restricted distribution of the butyrate kinase pathway among butyrate-producing bacteria from the human colon. J Bacteriol 186 : 2099 2106.
32. Macfarlane, G.T. Englyst, H.N. (1986) Starch utilization by the human large intestinal microflora. J Appl Bacteriol 60 : 195 201.
33. Macfarlane, G.T. Gibson, G.R. (1995) Carbohydrate fermentation, energy transduction and gas metabolism in the human large intestine. In Gastrointestinal Microbiology, Vol. 1. Mackie, R.I. White, B.A. (eds). New York, USA : Chapman & Hall, pp. 269 318.
34. Macfarlane, G.T., Gibson, G.R. Cummings, J.H. (1992) Comparison of fermentation reactions in different regions of the human colon. J Appl Bacteriol 72 : 57 64.
35. Miller, T.L. Wolin, M.J. (1985) Methanosphaera stadtmaniae gen. nov., sp. nov.: a species that forms methane by reducing methanol with hydrogen. Arch Microbiol 141 : 116 122.
36. Nugent, S.G., Kumar, D., Rampton, D.S. Evans, D.F. (2001) Intestinal luminal pH in inflammatory bowel disease: possible determinants and implications for therapy with aminosalicylates and other drugs. Gut 48 : 571 577.
37. Pryde, S.E., Duncan, S.H., Hold, G.L., Stewart, C.S. Flint, H.J. (2002) The microbiology of butyrate formation in the human colon. FEMS Microbiol Letts 217 : 133 139.
38. Ramsay, A.G., Scott, K.P., Martin, J.C., Rincon, M.T. Flint. H.J. (2006) Cell associated α-amylases of butyrate-producing Firmicute bacteria from the human colon. Microbiol 152 : 3281 3290.
39. Richardson, A.J., Calder, G.C., Stewart, C.S. Smith, A. (1989) Simultaneous determination of volatile and non-volatile fermentation products of anaerobes by capillary gas chromatography. Letts Appl Microbiol 9 : 5 8.
40. Roe, A.J., McLaggan, D., Davidson, I., O'Byrne, C. Booth, I.R. (1998) Perturbation of anion balance during inhibition of growth of Escherichia coli by weak acids. Bacteriol 180 : 767 772.
41. Russell, J.B. (1992) Another explanation for the low toxicity of fermentation acids at low pH- anion accumulation versus uncoupling. J Appl Bacteriol 73 : 363 370.
42. Salyers, A.A., West, S.E.H., Vercellotti, J.R. Wilkins, T.D. (1977) Fermentation of mucins and plant polysaccharides by anaerobic bacteria from the human colon. Appl Environ Microbiol 34 : 529 533.
43. Schloss, P.D. Handelsman, J. (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71 : 1501 1506.
44. Scholz-Aherns, K.E. Schrezenmeir, J. (2007) Inulin and oligofructose and mineral metabolism: the evidence from animal trials. J Nutr 137 : 2513S 2523S.
45. Scott, K.P. Flint, H.J. (1995) Transfer of plasmids between strains of Escherichia coli under rumen conditions. J Appl Bacteriol 78 : 189 193.
46. Swidsinski, A., Loening-Baucke, V., Vaneechoutte, M. Doerffel, Y. (2008) Active Crohn's disease and ulcerative colitis can be specifically diagnosed and monitored based on the biostructure of the fecal flora. Inflamm Bowel Dis 14 : 147 161.
47. Tamura, K., Dudley, J., Nei, M. Kumar, S. (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24 : 1596 1599.
48. Walker, A.W., Duncan, S.H., McWilliam Leitch, E.C., Child, M.W. Flint, H.J. (2005) pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl Environ Microbiol 71 : 3692 3700.
49. Walker, A.W., Duncan, S.H., Harmsen, H.J.M., Holtrop, G., Welling, G.W. Flint, H.J. (2008) The species composition of the human intestinal microbiota differs between particle-associated and liquid phase communities. Environ Microbiol 10 : 3275 3283.
50. Wolin, M. (1969) Volatile fatty acids and the inhibition of Escherichia coli growth by rumen fluid. App Environ Microbiol 17 : 83 87.
51. Xu, J., Mahowald, M.A., Ley, R.E., Lozupone, C.A., Hamady, M., Marten, E.C., et al. (2007) Evolution of symbiotic bacteria in the distal human intestine. PLOS Biol 5 : 1574 1586.