Impact of pH on Lactate Formation and Utilization by Human Fecal Microbial Communities

Alvaro Belenguer, Sylvia H. Duncan, Grietje Holtrop, Susan E. Anderson, Gerald E. Lobley, Harry James Flint

Research output: Contribution to journalArticle

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Abstract

The human intestine harbors both lactate-producing and lactate-utilizing bacteria. Lactate is normally present at < 3 mmol liter(-1) in stool samples from healthy adults, but concentrations up to 100 mmol liter(-1) have been reported in gut disorders such as ulcerative colitis. The effect of different initial pH values (5.2, 5.9, and 6.4) upon lactate metabolism was studied with fecal inocula from healthy volunteers, in incubations performed with the addition Of DL-lactate, a mixture of polysaccharides (mainly starch), or both. Propionate and butyrate formation occurred at pH 6.4; both were curtailed at pH 5.2, while propionate but not butyrate formation was inhibited at pH 5.9. With the polysaccharide mix, lactate accumulation occurred only at pH 5.2, but lactate production, estimated using L-[U-C-13] lactate, occurred at all three pH values. Lactate was completely utilized within 24 h at pH 5.9 and 6.4 but not at pH 5.2. At pH 5.9, more butyrate than propionate was formed from L-[U-C-13] lactate in the presence of polysaccharides, but propionate, formed mostly by the acrylate pathway, was the predominant product with lactate alone. Fluorescent in situ hybridization demonstrated that populations of Bifidobacterium spp., major lactate producers, increased approximately 10-fold in incubations with polysaccharides. Populations of Eubacterium hallii, a lactate-utilizing butyrate-producing bacterium, increased 100-fold at pH 5.9 and 6.4. These experiments suggest that lactate is rapidly converted to acetate, butyrate, and propionate by the human intestinal microbiota at pH values as low as 5.9, but at pH 5.2 reduced utilization occurs while production is maintained, resulting in lactate accumulation.

Original languageEnglish
Pages (from-to)6526-6533
Number of pages8
JournalApplied and Environmental Microbiology
Volume73
Issue number20
Early online date31 Aug 2007
DOIs
Publication statusPublished - Oct 2007

Fingerprint

polysaccharide
lactates
microbial communities
microbial community
Lactic Acid
Butyrates
incubation
Propionates
butyrates
fold
propionates
bacterium
starch
Polysaccharides
polysaccharides
acetate
harbor
metabolism
Eubacterium hallii
pH-value

Keywords

  • adult
  • bacteria
  • carbon isotopes
  • culture media
  • ecosystem
  • feces
  • female
  • humans
  • hydrogen-ion concentration
  • in situ hybridization, fluorescence
  • lactates
  • male
  • middle aged
  • RNA, ribosomal, 16S

Cite this

Impact of pH on Lactate Formation and Utilization by Human Fecal Microbial Communities. / Belenguer, Alvaro; Duncan, Sylvia H.; Holtrop, Grietje; Anderson, Susan E.; Lobley, Gerald E.; Flint, Harry James.

In: Applied and Environmental Microbiology, Vol. 73, No. 20, 10.2007, p. 6526-6533.

Research output: Contribution to journalArticle

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abstract = "The human intestine harbors both lactate-producing and lactate-utilizing bacteria. Lactate is normally present at < 3 mmol liter(-1) in stool samples from healthy adults, but concentrations up to 100 mmol liter(-1) have been reported in gut disorders such as ulcerative colitis. The effect of different initial pH values (5.2, 5.9, and 6.4) upon lactate metabolism was studied with fecal inocula from healthy volunteers, in incubations performed with the addition Of DL-lactate, a mixture of polysaccharides (mainly starch), or both. Propionate and butyrate formation occurred at pH 6.4; both were curtailed at pH 5.2, while propionate but not butyrate formation was inhibited at pH 5.9. With the polysaccharide mix, lactate accumulation occurred only at pH 5.2, but lactate production, estimated using L-[U-C-13] lactate, occurred at all three pH values. Lactate was completely utilized within 24 h at pH 5.9 and 6.4 but not at pH 5.2. At pH 5.9, more butyrate than propionate was formed from L-[U-C-13] lactate in the presence of polysaccharides, but propionate, formed mostly by the acrylate pathway, was the predominant product with lactate alone. Fluorescent in situ hybridization demonstrated that populations of Bifidobacterium spp., major lactate producers, increased approximately 10-fold in incubations with polysaccharides. Populations of Eubacterium hallii, a lactate-utilizing butyrate-producing bacterium, increased 100-fold at pH 5.9 and 6.4. These experiments suggest that lactate is rapidly converted to acetate, butyrate, and propionate by the human intestinal microbiota at pH values as low as 5.9, but at pH 5.2 reduced utilization occurs while production is maintained, resulting in lactate accumulation.",
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T1 - Impact of pH on Lactate Formation and Utilization by Human Fecal Microbial Communities

AU - Belenguer, Alvaro

AU - Duncan, Sylvia H.

AU - Holtrop, Grietje

AU - Anderson, Susan E.

AU - Lobley, Gerald E.

AU - Flint, Harry James

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N2 - The human intestine harbors both lactate-producing and lactate-utilizing bacteria. Lactate is normally present at < 3 mmol liter(-1) in stool samples from healthy adults, but concentrations up to 100 mmol liter(-1) have been reported in gut disorders such as ulcerative colitis. The effect of different initial pH values (5.2, 5.9, and 6.4) upon lactate metabolism was studied with fecal inocula from healthy volunteers, in incubations performed with the addition Of DL-lactate, a mixture of polysaccharides (mainly starch), or both. Propionate and butyrate formation occurred at pH 6.4; both were curtailed at pH 5.2, while propionate but not butyrate formation was inhibited at pH 5.9. With the polysaccharide mix, lactate accumulation occurred only at pH 5.2, but lactate production, estimated using L-[U-C-13] lactate, occurred at all three pH values. Lactate was completely utilized within 24 h at pH 5.9 and 6.4 but not at pH 5.2. At pH 5.9, more butyrate than propionate was formed from L-[U-C-13] lactate in the presence of polysaccharides, but propionate, formed mostly by the acrylate pathway, was the predominant product with lactate alone. Fluorescent in situ hybridization demonstrated that populations of Bifidobacterium spp., major lactate producers, increased approximately 10-fold in incubations with polysaccharides. Populations of Eubacterium hallii, a lactate-utilizing butyrate-producing bacterium, increased 100-fold at pH 5.9 and 6.4. These experiments suggest that lactate is rapidly converted to acetate, butyrate, and propionate by the human intestinal microbiota at pH values as low as 5.9, but at pH 5.2 reduced utilization occurs while production is maintained, resulting in lactate accumulation.

AB - The human intestine harbors both lactate-producing and lactate-utilizing bacteria. Lactate is normally present at < 3 mmol liter(-1) in stool samples from healthy adults, but concentrations up to 100 mmol liter(-1) have been reported in gut disorders such as ulcerative colitis. The effect of different initial pH values (5.2, 5.9, and 6.4) upon lactate metabolism was studied with fecal inocula from healthy volunteers, in incubations performed with the addition Of DL-lactate, a mixture of polysaccharides (mainly starch), or both. Propionate and butyrate formation occurred at pH 6.4; both were curtailed at pH 5.2, while propionate but not butyrate formation was inhibited at pH 5.9. With the polysaccharide mix, lactate accumulation occurred only at pH 5.2, but lactate production, estimated using L-[U-C-13] lactate, occurred at all three pH values. Lactate was completely utilized within 24 h at pH 5.9 and 6.4 but not at pH 5.2. At pH 5.9, more butyrate than propionate was formed from L-[U-C-13] lactate in the presence of polysaccharides, but propionate, formed mostly by the acrylate pathway, was the predominant product with lactate alone. Fluorescent in situ hybridization demonstrated that populations of Bifidobacterium spp., major lactate producers, increased approximately 10-fold in incubations with polysaccharides. Populations of Eubacterium hallii, a lactate-utilizing butyrate-producing bacterium, increased 100-fold at pH 5.9 and 6.4. These experiments suggest that lactate is rapidly converted to acetate, butyrate, and propionate by the human intestinal microbiota at pH values as low as 5.9, but at pH 5.2 reduced utilization occurs while production is maintained, resulting in lactate accumulation.

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KW - bacteria

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KW - culture media

KW - ecosystem

KW - feces

KW - female

KW - humans

KW - hydrogen-ion concentration

KW - in situ hybridization, fluorescence

KW - lactates

KW - male

KW - middle aged

KW - RNA, ribosomal, 16S

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