pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon

Alan W Walker, Sylvia H Duncan, E Carol McWilliam Leitch, Matthew W Child, Harry James Flint

Research output: Contribution to journalArticle

321 Citations (Scopus)

Abstract

The effects of changes in the gut environment upon the human colonic microbiota. are poorly understood. The response of human fecal microbial communities from two donors to alterations in pH (5.5 or 6.5) and peptides (0.6 or 0.1%) was studied here in anaerobic continuous cultures supplied with a mixed carbohydrate source. Final butyrate concentrations were markedly higher at pH 5.5 (0.6% peptide mean, 24.9 mM; 0.1% peptide mean, 13.8 mM) than at pH 6.5 (0.6% peptide mean, 5.3 mM; 0.1% peptide mean, 7.6 mM). At pH 5.5 and 0.6% peptide input, a high butyrate production coincided with decreasing acetate concentrations. The highest propionate concentrations (mean, 20.6 mM) occurred at pH 6.5 and 0.6% peptide input. In parallel, major bacterial groups were monitored by using fluorescence in situ hybridization with a panel of specific 16S rRNA probes. Bacteroides levels increased from ca. 20 to 75% of total eubacteria after a shift from pH 5.5 to 6.5, at 0.6% peptide, coinciding with high propionate formation. Conversely, populations of the butyrate-producing Roseburia group were highest (11 to 19%) at pH 5.5 but fell at pH 6.5, a finding that correlates with butyrate formation. When tested in batch culture, three Bacteroides species grew well at pH 6.7 but poorly at pH 5.5, which is consistent with the behavior observed for the mixed community. Two Roseburia isolates grew equally well at pH 6.7 and 5.5. These findings suggest that a lowering of pH resulting from substrate fermentation in the colon may boost butyrate production and populations of butyrate-producing bacteria, while at the same time curtailing the growth of Bacteroides spp.

Original languageEnglish
Pages (from-to)3692-3700
Number of pages9
JournalApplied and Environmental Microbiology
Volume71
Issue number7
DOIs
Publication statusPublished - Jul 2005

Keywords

  • 16S ribosomal-RNA
  • butyrate-producing bacteria
  • in-situ hybridization
  • human fecal flora
  • targeted oligonucleotide probes
  • inflammatory bowel disease
  • continuous culture system
  • human large intestine
  • human feces
  • resistant starch

Cite this

@article{0e60e9ab28fd42adb13946489728112e,
title = "pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon",
abstract = "The effects of changes in the gut environment upon the human colonic microbiota. are poorly understood. The response of human fecal microbial communities from two donors to alterations in pH (5.5 or 6.5) and peptides (0.6 or 0.1{\%}) was studied here in anaerobic continuous cultures supplied with a mixed carbohydrate source. Final butyrate concentrations were markedly higher at pH 5.5 (0.6{\%} peptide mean, 24.9 mM; 0.1{\%} peptide mean, 13.8 mM) than at pH 6.5 (0.6{\%} peptide mean, 5.3 mM; 0.1{\%} peptide mean, 7.6 mM). At pH 5.5 and 0.6{\%} peptide input, a high butyrate production coincided with decreasing acetate concentrations. The highest propionate concentrations (mean, 20.6 mM) occurred at pH 6.5 and 0.6{\%} peptide input. In parallel, major bacterial groups were monitored by using fluorescence in situ hybridization with a panel of specific 16S rRNA probes. Bacteroides levels increased from ca. 20 to 75{\%} of total eubacteria after a shift from pH 5.5 to 6.5, at 0.6{\%} peptide, coinciding with high propionate formation. Conversely, populations of the butyrate-producing Roseburia group were highest (11 to 19{\%}) at pH 5.5 but fell at pH 6.5, a finding that correlates with butyrate formation. When tested in batch culture, three Bacteroides species grew well at pH 6.7 but poorly at pH 5.5, which is consistent with the behavior observed for the mixed community. Two Roseburia isolates grew equally well at pH 6.7 and 5.5. These findings suggest that a lowering of pH resulting from substrate fermentation in the colon may boost butyrate production and populations of butyrate-producing bacteria, while at the same time curtailing the growth of Bacteroides spp.",
keywords = "16S ribosomal-RNA, butyrate-producing bacteria, in-situ hybridization, human fecal flora, targeted oligonucleotide probes, inflammatory bowel disease, continuous culture system, human large intestine, human feces, resistant starch",
author = "Walker, {Alan W} and Duncan, {Sylvia H} and {McWilliam Leitch}, {E Carol} and Child, {Matthew W} and Flint, {Harry James}",
year = "2005",
month = "7",
doi = "10.1128/AEM.71.7.3692-3700.2005",
language = "English",
volume = "71",
pages = "3692--3700",
journal = "Applied and Environmental Microbiology",
issn = "0099-2240",
publisher = "American Society for Microbiology",
number = "7",

}

TY - JOUR

T1 - pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon

AU - Walker, Alan W

AU - Duncan, Sylvia H

AU - McWilliam Leitch, E Carol

AU - Child, Matthew W

AU - Flint, Harry James

PY - 2005/7

Y1 - 2005/7

N2 - The effects of changes in the gut environment upon the human colonic microbiota. are poorly understood. The response of human fecal microbial communities from two donors to alterations in pH (5.5 or 6.5) and peptides (0.6 or 0.1%) was studied here in anaerobic continuous cultures supplied with a mixed carbohydrate source. Final butyrate concentrations were markedly higher at pH 5.5 (0.6% peptide mean, 24.9 mM; 0.1% peptide mean, 13.8 mM) than at pH 6.5 (0.6% peptide mean, 5.3 mM; 0.1% peptide mean, 7.6 mM). At pH 5.5 and 0.6% peptide input, a high butyrate production coincided with decreasing acetate concentrations. The highest propionate concentrations (mean, 20.6 mM) occurred at pH 6.5 and 0.6% peptide input. In parallel, major bacterial groups were monitored by using fluorescence in situ hybridization with a panel of specific 16S rRNA probes. Bacteroides levels increased from ca. 20 to 75% of total eubacteria after a shift from pH 5.5 to 6.5, at 0.6% peptide, coinciding with high propionate formation. Conversely, populations of the butyrate-producing Roseburia group were highest (11 to 19%) at pH 5.5 but fell at pH 6.5, a finding that correlates with butyrate formation. When tested in batch culture, three Bacteroides species grew well at pH 6.7 but poorly at pH 5.5, which is consistent with the behavior observed for the mixed community. Two Roseburia isolates grew equally well at pH 6.7 and 5.5. These findings suggest that a lowering of pH resulting from substrate fermentation in the colon may boost butyrate production and populations of butyrate-producing bacteria, while at the same time curtailing the growth of Bacteroides spp.

AB - The effects of changes in the gut environment upon the human colonic microbiota. are poorly understood. The response of human fecal microbial communities from two donors to alterations in pH (5.5 or 6.5) and peptides (0.6 or 0.1%) was studied here in anaerobic continuous cultures supplied with a mixed carbohydrate source. Final butyrate concentrations were markedly higher at pH 5.5 (0.6% peptide mean, 24.9 mM; 0.1% peptide mean, 13.8 mM) than at pH 6.5 (0.6% peptide mean, 5.3 mM; 0.1% peptide mean, 7.6 mM). At pH 5.5 and 0.6% peptide input, a high butyrate production coincided with decreasing acetate concentrations. The highest propionate concentrations (mean, 20.6 mM) occurred at pH 6.5 and 0.6% peptide input. In parallel, major bacterial groups were monitored by using fluorescence in situ hybridization with a panel of specific 16S rRNA probes. Bacteroides levels increased from ca. 20 to 75% of total eubacteria after a shift from pH 5.5 to 6.5, at 0.6% peptide, coinciding with high propionate formation. Conversely, populations of the butyrate-producing Roseburia group were highest (11 to 19%) at pH 5.5 but fell at pH 6.5, a finding that correlates with butyrate formation. When tested in batch culture, three Bacteroides species grew well at pH 6.7 but poorly at pH 5.5, which is consistent with the behavior observed for the mixed community. Two Roseburia isolates grew equally well at pH 6.7 and 5.5. These findings suggest that a lowering of pH resulting from substrate fermentation in the colon may boost butyrate production and populations of butyrate-producing bacteria, while at the same time curtailing the growth of Bacteroides spp.

KW - 16S ribosomal-RNA

KW - butyrate-producing bacteria

KW - in-situ hybridization

KW - human fecal flora

KW - targeted oligonucleotide probes

KW - inflammatory bowel disease

KW - continuous culture system

KW - human large intestine

KW - human feces

KW - resistant starch

U2 - 10.1128/AEM.71.7.3692-3700.2005

DO - 10.1128/AEM.71.7.3692-3700.2005

M3 - Article

VL - 71

SP - 3692

EP - 3700

JO - Applied and Environmental Microbiology

JF - Applied and Environmental Microbiology

SN - 0099-2240

IS - 7

ER -