Major phenylpropanoid-derived metabolites in the human gut can arise from microbial fermentation of protein

Wendy R Russell, Sylvia Helen Duncan, Lorraine Scobbie, Gary Duncan, Louise Cantlay, A Graham Calder, Susan E Anderson, Harry James Flint

Research output: Contribution to journalArticle

79 Citations (Scopus)

Abstract

SCOPE: Plant secondary metabolites, such as phenolic acids are commonly associated with benefits for human health. Two of the most abundant phenylpropanoid-derived compounds detected in human faecal samples are phenylacetic acid (PAA) and 4-hydroxylphenylacetic acid (4-hydroxyPAA). Although they have the potential to be derived from diets rich in plant-based foods, evidence suggests that these compounds can be derived from the microbial fermentation of aromatic amino acids (AAAs) in the colon.

METHODS AND RESULTS: To identify the bacteria responsible, 26 strains representing 25 of the dominant human colonic species were screened for phenyl metabolite formation. Seven strains produced significant amounts of both PAA and 4-hydroxyPAA. These included five out of seven Bacteroidetes (Bacteroides thetaiotaomicron, Bacteroides eggerthii, Bacteroides ovatus, Bacteroides fragilis, Parabacteroides distasonis), and two out of 17 Firmicutes (Eubacterium hallii and Clostridium bartlettii). These species also produced indole-3-acetic acid (IAA), the corresponding tryptophan metabolite, but C. bartlettii showed 100 times higher IAA production than the other six strains. Four strains were further tested and PAA formation was substantially increased by phenylalanine, 4-hydroxyPAA by tyrosine and IAA by tryptophan.

CONCLUSION: This study demonstrates that certain microbial species have the ability to ferment all three AAAs and that protein fermentation is the likely source of major phenylpropanoid-derived metabolites in the colon.

Original languageEnglish
Pages (from-to)523-535
Number of pages13
JournalMolecular Nutrition & Food Research
Volume57
Issue number3
Early online date24 Jan 2013
DOIs
Publication statusPublished - Mar 2013

Fingerprint

phenylpropanoids
phenylacetic acid
Fermentation
Aromatic Amino Acids
Bacteroides
digestive system
fermentation
indole acetic acid
metabolites
Tryptophan
Acids
Colon
Bacteroides eggerthii
Eubacterium hallii
tryptophan
Eubacterium
Bacteroidetes
colon
aromatic compounds
Bacteroides ovatus

Keywords

  • Amino Acids
  • Amino Acids, Aromatic
  • Bacteroides
  • Colon
  • Eubacterium
  • Fermentation
  • Humans
  • Indoleacetic Acids
  • Microbiota
  • Phenylacetates
  • Tryptophan

Cite this

Major phenylpropanoid-derived metabolites in the human gut can arise from microbial fermentation of protein. / Russell, Wendy R; Duncan, Sylvia Helen; Scobbie, Lorraine; Duncan, Gary; Cantlay, Louise; Calder, A Graham; Anderson, Susan E; Flint, Harry James.

In: Molecular Nutrition & Food Research, Vol. 57, No. 3, 03.2013, p. 523-535.

Research output: Contribution to journalArticle

Russell, Wendy R ; Duncan, Sylvia Helen ; Scobbie, Lorraine ; Duncan, Gary ; Cantlay, Louise ; Calder, A Graham ; Anderson, Susan E ; Flint, Harry James. / Major phenylpropanoid-derived metabolites in the human gut can arise from microbial fermentation of protein. In: Molecular Nutrition & Food Research. 2013 ; Vol. 57, No. 3. pp. 523-535.
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T1 - Major phenylpropanoid-derived metabolites in the human gut can arise from microbial fermentation of protein

AU - Russell, Wendy R

AU - Duncan, Sylvia Helen

AU - Scobbie, Lorraine

AU - Duncan, Gary

AU - Cantlay, Louise

AU - Calder, A Graham

AU - Anderson, Susan E

AU - Flint, Harry James

N1 - © 2013 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.

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N2 - SCOPE: Plant secondary metabolites, such as phenolic acids are commonly associated with benefits for human health. Two of the most abundant phenylpropanoid-derived compounds detected in human faecal samples are phenylacetic acid (PAA) and 4-hydroxylphenylacetic acid (4-hydroxyPAA). Although they have the potential to be derived from diets rich in plant-based foods, evidence suggests that these compounds can be derived from the microbial fermentation of aromatic amino acids (AAAs) in the colon.METHODS AND RESULTS: To identify the bacteria responsible, 26 strains representing 25 of the dominant human colonic species were screened for phenyl metabolite formation. Seven strains produced significant amounts of both PAA and 4-hydroxyPAA. These included five out of seven Bacteroidetes (Bacteroides thetaiotaomicron, Bacteroides eggerthii, Bacteroides ovatus, Bacteroides fragilis, Parabacteroides distasonis), and two out of 17 Firmicutes (Eubacterium hallii and Clostridium bartlettii). These species also produced indole-3-acetic acid (IAA), the corresponding tryptophan metabolite, but C. bartlettii showed 100 times higher IAA production than the other six strains. Four strains were further tested and PAA formation was substantially increased by phenylalanine, 4-hydroxyPAA by tyrosine and IAA by tryptophan.CONCLUSION: This study demonstrates that certain microbial species have the ability to ferment all three AAAs and that protein fermentation is the likely source of major phenylpropanoid-derived metabolites in the colon.

AB - SCOPE: Plant secondary metabolites, such as phenolic acids are commonly associated with benefits for human health. Two of the most abundant phenylpropanoid-derived compounds detected in human faecal samples are phenylacetic acid (PAA) and 4-hydroxylphenylacetic acid (4-hydroxyPAA). Although they have the potential to be derived from diets rich in plant-based foods, evidence suggests that these compounds can be derived from the microbial fermentation of aromatic amino acids (AAAs) in the colon.METHODS AND RESULTS: To identify the bacteria responsible, 26 strains representing 25 of the dominant human colonic species were screened for phenyl metabolite formation. Seven strains produced significant amounts of both PAA and 4-hydroxyPAA. These included five out of seven Bacteroidetes (Bacteroides thetaiotaomicron, Bacteroides eggerthii, Bacteroides ovatus, Bacteroides fragilis, Parabacteroides distasonis), and two out of 17 Firmicutes (Eubacterium hallii and Clostridium bartlettii). These species also produced indole-3-acetic acid (IAA), the corresponding tryptophan metabolite, but C. bartlettii showed 100 times higher IAA production than the other six strains. Four strains were further tested and PAA formation was substantially increased by phenylalanine, 4-hydroxyPAA by tyrosine and IAA by tryptophan.CONCLUSION: This study demonstrates that certain microbial species have the ability to ferment all three AAAs and that protein fermentation is the likely source of major phenylpropanoid-derived metabolites in the colon.

KW - Amino Acids

KW - Amino Acids, Aromatic

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KW - Humans

KW - Indoleacetic Acids

KW - Microbiota

KW - Phenylacetates

KW - Tryptophan

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JO - Molecular Nutrition & Food Research

JF - Molecular Nutrition & Food Research

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