Modulation of the human gut microbiota by dietary fibres occurs at the species level

Wing Sun Faith Chung, Alan W. Walker, Petra Louis, Julian Parkhill, Joan Vermeiren, Douwina Bosscher, Sylvia H. Duncan, Harry J. Flint*

*Corresponding author for this work

Research output: Contribution to journalArticle

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Abstract

Background: Dietary intake of specific non-digestible carbohydrates (including prebiotics) is increasingly seen as a highly effective approach for manipulating the composition and activities of the human gut microbiota to benefit health. Nevertheless, surprisingly little is known about the global response of the microbial community to particular carbohydrates. Recent in vivo dietary studies have demonstrated that the species composition of the human faecal microbiota is influenced by dietary intake. There is now potential to gain insights into the mechanisms involved by using in vitro systems that produce highly controlled conditions of pH and substrate supply.

Results: We supplied two alternative non-digestible polysaccharides as energy sources to three different human gut microbial communities in anaerobic, pH-controlled continuous-flow fermentors. Community analysis showed that supply of apple pectin or inulin resulted in the highly specific enrichment of particular bacterial operational taxonomic units (OTUs; based on 16S rRNA gene sequences). Of the eight most abundant Bacteroides OTUs detected, two were promoted specifically by inulin and six by pectin. Among the Firmicutes, Eubacterium eligens in particular was strongly promoted by pectin, while several species were stimulated by inulin. Responses were influenced by pH, which was stepped up, and down, between 5.5, 6.0, 6.4 and 6.9 in parallel vessels within each experiment. In particular, several experiments involving downshifts to pH 5.5 resulted in Faecalibacterium prausnitzii replacing Bacteroides spp. as the dominant sequences observed. Community diversity was greater in the pectin-fed than in the inulin-fed fermentors, presumably reflecting the differing complexity of the two substrates.

Conclusions: We have shown that particular non-digestible dietary carbohydrates have enormous potential for modifying the gut microbiota, but these modifications occur at the level of individual strains and species and are not easily predicted a priori. Furthermore, the gut environment, especially pH, plays a key role in determining the outcome of interspecies competition. This makes it crucial to put greater effort into identifying the range of bacteria that may be stimulated by a given prebiotic approach. Both for reasons of efficacy and of safety, the development of prebiotics intended to benefit human health has to take account of the highly individual species profiles that may result.

Original languageEnglish
Article number3
JournalBMC Biology
Volume14
DOIs
Publication statusPublished - 11 Jan 2016

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Inulin
Dietary Fiber
intestinal microorganisms
Prebiotics
inulin
dietary fiber
pectins
Modulation
carbohydrate
prebiotics
Otus
Bacteroides
fermenters
Bioreactors
microbial community
Insurance Benefits
Eubacterium eligens
Carbohydrates
Health
microbial communities

Keywords

  • Bacteroidetes
  • Prebiotic
  • Colonic anaerobes
  • Faecalibacterium prausnitzii
  • Firmicutes
  • Inulin
  • Pectin
  • Propionate
  • Butyrate-producing bacteria
  • Human colonic microbiota
  • Double-blind
  • In-vitro
  • Fermentation
  • PH
  • Bifidobacteria
  • Health
  • Consequences

Cite this

Modulation of the human gut microbiota by dietary fibres occurs at the species level. / Chung, Wing Sun Faith; Walker, Alan W.; Louis, Petra; Parkhill, Julian; Vermeiren, Joan; Bosscher, Douwina; Duncan, Sylvia H.; Flint, Harry J.

In: BMC Biology, Vol. 14, 3, 11.01.2016.

Research output: Contribution to journalArticle

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abstract = "Background: Dietary intake of specific non-digestible carbohydrates (including prebiotics) is increasingly seen as a highly effective approach for manipulating the composition and activities of the human gut microbiota to benefit health. Nevertheless, surprisingly little is known about the global response of the microbial community to particular carbohydrates. Recent in vivo dietary studies have demonstrated that the species composition of the human faecal microbiota is influenced by dietary intake. There is now potential to gain insights into the mechanisms involved by using in vitro systems that produce highly controlled conditions of pH and substrate supply.Results: We supplied two alternative non-digestible polysaccharides as energy sources to three different human gut microbial communities in anaerobic, pH-controlled continuous-flow fermentors. Community analysis showed that supply of apple pectin or inulin resulted in the highly specific enrichment of particular bacterial operational taxonomic units (OTUs; based on 16S rRNA gene sequences). Of the eight most abundant Bacteroides OTUs detected, two were promoted specifically by inulin and six by pectin. Among the Firmicutes, Eubacterium eligens in particular was strongly promoted by pectin, while several species were stimulated by inulin. Responses were influenced by pH, which was stepped up, and down, between 5.5, 6.0, 6.4 and 6.9 in parallel vessels within each experiment. In particular, several experiments involving downshifts to pH 5.5 resulted in Faecalibacterium prausnitzii replacing Bacteroides spp. as the dominant sequences observed. Community diversity was greater in the pectin-fed than in the inulin-fed fermentors, presumably reflecting the differing complexity of the two substrates.Conclusions: We have shown that particular non-digestible dietary carbohydrates have enormous potential for modifying the gut microbiota, but these modifications occur at the level of individual strains and species and are not easily predicted a priori. Furthermore, the gut environment, especially pH, plays a key role in determining the outcome of interspecies competition. This makes it crucial to put greater effort into identifying the range of bacteria that may be stimulated by a given prebiotic approach. Both for reasons of efficacy and of safety, the development of prebiotics intended to benefit human health has to take account of the highly individual species profiles that may result.",
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author = "Chung, {Wing Sun Faith} and Walker, {Alan W.} and Petra Louis and Julian Parkhill and Joan Vermeiren and Douwina Bosscher and Duncan, {Sylvia H.} and Flint, {Harry J.}",
note = "Acknowledgements We would like to thank Donna Henderson for carrying out GC analysis, and Paul Scott, Iraad Bronner and the Wellcome Trust Sanger Institute’s core sequencing team for carrying out the Illumina MiSeq sequencing of 16S rRNA genes. We are grateful to Grietje Holtrop (BioSS) for advice on statistical analysis. Freda Farquharson kindly contributed her expertise with training on qPCR. The Rowett Institute of Nutrition and Health receives financial support from the Scottish Government Rural and Environmental Sciences and Analytical Services (RESAS) and this work was partly funded by the Biotechnology and Biological Sciences Research Council (BBSRC-CASE) and Cargill, Inc. AWW, JP and 16S rRNA gene sequencing costs were funded by the Wellcome Trust (grant number 098051).",
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T1 - Modulation of the human gut microbiota by dietary fibres occurs at the species level

AU - Chung, Wing Sun Faith

AU - Walker, Alan W.

AU - Louis, Petra

AU - Parkhill, Julian

AU - Vermeiren, Joan

AU - Bosscher, Douwina

AU - Duncan, Sylvia H.

AU - Flint, Harry J.

N1 - Acknowledgements We would like to thank Donna Henderson for carrying out GC analysis, and Paul Scott, Iraad Bronner and the Wellcome Trust Sanger Institute’s core sequencing team for carrying out the Illumina MiSeq sequencing of 16S rRNA genes. We are grateful to Grietje Holtrop (BioSS) for advice on statistical analysis. Freda Farquharson kindly contributed her expertise with training on qPCR. The Rowett Institute of Nutrition and Health receives financial support from the Scottish Government Rural and Environmental Sciences and Analytical Services (RESAS) and this work was partly funded by the Biotechnology and Biological Sciences Research Council (BBSRC-CASE) and Cargill, Inc. AWW, JP and 16S rRNA gene sequencing costs were funded by the Wellcome Trust (grant number 098051).

PY - 2016/1/11

Y1 - 2016/1/11

N2 - Background: Dietary intake of specific non-digestible carbohydrates (including prebiotics) is increasingly seen as a highly effective approach for manipulating the composition and activities of the human gut microbiota to benefit health. Nevertheless, surprisingly little is known about the global response of the microbial community to particular carbohydrates. Recent in vivo dietary studies have demonstrated that the species composition of the human faecal microbiota is influenced by dietary intake. There is now potential to gain insights into the mechanisms involved by using in vitro systems that produce highly controlled conditions of pH and substrate supply.Results: We supplied two alternative non-digestible polysaccharides as energy sources to three different human gut microbial communities in anaerobic, pH-controlled continuous-flow fermentors. Community analysis showed that supply of apple pectin or inulin resulted in the highly specific enrichment of particular bacterial operational taxonomic units (OTUs; based on 16S rRNA gene sequences). Of the eight most abundant Bacteroides OTUs detected, two were promoted specifically by inulin and six by pectin. Among the Firmicutes, Eubacterium eligens in particular was strongly promoted by pectin, while several species were stimulated by inulin. Responses were influenced by pH, which was stepped up, and down, between 5.5, 6.0, 6.4 and 6.9 in parallel vessels within each experiment. In particular, several experiments involving downshifts to pH 5.5 resulted in Faecalibacterium prausnitzii replacing Bacteroides spp. as the dominant sequences observed. Community diversity was greater in the pectin-fed than in the inulin-fed fermentors, presumably reflecting the differing complexity of the two substrates.Conclusions: We have shown that particular non-digestible dietary carbohydrates have enormous potential for modifying the gut microbiota, but these modifications occur at the level of individual strains and species and are not easily predicted a priori. Furthermore, the gut environment, especially pH, plays a key role in determining the outcome of interspecies competition. This makes it crucial to put greater effort into identifying the range of bacteria that may be stimulated by a given prebiotic approach. Both for reasons of efficacy and of safety, the development of prebiotics intended to benefit human health has to take account of the highly individual species profiles that may result.

AB - Background: Dietary intake of specific non-digestible carbohydrates (including prebiotics) is increasingly seen as a highly effective approach for manipulating the composition and activities of the human gut microbiota to benefit health. Nevertheless, surprisingly little is known about the global response of the microbial community to particular carbohydrates. Recent in vivo dietary studies have demonstrated that the species composition of the human faecal microbiota is influenced by dietary intake. There is now potential to gain insights into the mechanisms involved by using in vitro systems that produce highly controlled conditions of pH and substrate supply.Results: We supplied two alternative non-digestible polysaccharides as energy sources to three different human gut microbial communities in anaerobic, pH-controlled continuous-flow fermentors. Community analysis showed that supply of apple pectin or inulin resulted in the highly specific enrichment of particular bacterial operational taxonomic units (OTUs; based on 16S rRNA gene sequences). Of the eight most abundant Bacteroides OTUs detected, two were promoted specifically by inulin and six by pectin. Among the Firmicutes, Eubacterium eligens in particular was strongly promoted by pectin, while several species were stimulated by inulin. Responses were influenced by pH, which was stepped up, and down, between 5.5, 6.0, 6.4 and 6.9 in parallel vessels within each experiment. In particular, several experiments involving downshifts to pH 5.5 resulted in Faecalibacterium prausnitzii replacing Bacteroides spp. as the dominant sequences observed. Community diversity was greater in the pectin-fed than in the inulin-fed fermentors, presumably reflecting the differing complexity of the two substrates.Conclusions: We have shown that particular non-digestible dietary carbohydrates have enormous potential for modifying the gut microbiota, but these modifications occur at the level of individual strains and species and are not easily predicted a priori. Furthermore, the gut environment, especially pH, plays a key role in determining the outcome of interspecies competition. This makes it crucial to put greater effort into identifying the range of bacteria that may be stimulated by a given prebiotic approach. Both for reasons of efficacy and of safety, the development of prebiotics intended to benefit human health has to take account of the highly individual species profiles that may result.

KW - Bacteroidetes

KW - Prebiotic

KW - Colonic anaerobes

KW - Faecalibacterium prausnitzii

KW - Firmicutes

KW - Inulin

KW - Pectin

KW - Propionate

KW - Butyrate-producing bacteria

KW - Human colonic microbiota

KW - Double-blind

KW - In-vitro

KW - Fermentation

KW - PH

KW - Bifidobacteria

KW - Health

KW - Consequences

U2 - 10.1186/s12915-015-0224-3

DO - 10.1186/s12915-015-0224-3

M3 - Article

VL - 14

JO - BMC Biology

JF - BMC Biology

SN - 1741-7007

M1 - 3

ER -