Specific substrate-driven changes in human faecal microbiota composition contrast with functional redundancy in short-chain fatty acid production

Nicole Reichardt, Maren Vollmer, Grietje Holtrop, Freda Mabel Farquharson, Daniel Wefers, Mirko Bunzel, Sylvia H Duncan, Janice E Drew, Lynda M Williams, Graeme Milligan, Thomas Preston, Douglas Morrison, Harry J Flint, Petra Louis (Corresponding Author)

Research output: Contribution to journalArticle

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Abstract

The diet provides carbohydrates that are non-digestible in the upper gut and are major carbon and energy sources for the microbial community in the lower intestine, supporting a complex metabolic network. Fermentation produces the short-chain fatty acids (SCFAs) acetate, propionate and butyrate, which have health-promoting effects for the human host. Here we investigated microbial community changes and SCFA production during in vitro batch incubations of 15 different non-digestible carbohydrates, at two initial pH values with faecal microbiota from three different human donors. To investigate temporal stability and reproducibility, a further experiment was performed 1 year later with four of the carbohydrates. The lower pH (5.5) led to higher butyrate and the higher pH (6.5) to more propionate production. The strongest propionigenic effect was found with rhamnose, followed by galactomannans, whereas fructans and several α- and β-glucans led to higher butyrate production. 16S ribosomal RNA gene-based quantitative PCR analysis of 22 different microbial groups together with 454 sequencing revealed significant stimulation of specific bacteria in response to particular carbohydrates. Some changes were ascribed to metabolite cross-feeding, for example, utilisation by Eubacterium hallii of 1,2-propanediol produced from fermentation of rhamnose by Blautia spp. Despite marked inter-individual differences in microbiota composition, SCFA production was surprisingly reproducible for different carbohydrates, indicating a level of functional redundancy. Interestingly, butyrate formation was influenced not only by the overall % butyrate-producing bacteria in the community but also by the initial pH, consistent with a pH-dependent shift in the stoichiometry of butyrate production.
Original languageEnglish
Pages (from-to)610-622
Number of pages13
JournalThe ISME Journal
Volume12
Early online date1 Dec 2017
DOIs
Publication statusPublished - 2018

Fingerprint

Volatile Fatty Acids
Butyrates
Microbiota
short chain fatty acids
butyrates
carbohydrate
fatty acid
substrate
Carbohydrates
carbohydrates
Rhamnose
rhamnose
Propionates
fermentation
microbial community
Eubacterium hallii
propionates
Fermentation
microbial communities
Fructans

Keywords

  • microbial ecology
  • microbiome

Cite this

Specific substrate-driven changes in human faecal microbiota composition contrast with functional redundancy in short-chain fatty acid production. / Reichardt, Nicole; Vollmer, Maren ; Holtrop, Grietje; Farquharson, Freda Mabel; Wefers, Daniel; Bunzel, Mirko ; Duncan, Sylvia H; Drew, Janice E; Williams, Lynda M; Milligan, Graeme ; Preston, Thomas ; Morrison, Douglas ; Flint, Harry J; Louis, Petra (Corresponding Author).

In: The ISME Journal, Vol. 12, 2018, p. 610-622.

Research output: Contribution to journalArticle

Reichardt, Nicole ; Vollmer, Maren ; Holtrop, Grietje ; Farquharson, Freda Mabel ; Wefers, Daniel ; Bunzel, Mirko ; Duncan, Sylvia H ; Drew, Janice E ; Williams, Lynda M ; Milligan, Graeme ; Preston, Thomas ; Morrison, Douglas ; Flint, Harry J ; Louis, Petra. / Specific substrate-driven changes in human faecal microbiota composition contrast with functional redundancy in short-chain fatty acid production. In: The ISME Journal. 2018 ; Vol. 12. pp. 610-622.
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AU - Reichardt, Nicole

AU - Vollmer, Maren

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AU - Farquharson, Freda Mabel

AU - Wefers, Daniel

AU - Bunzel, Mirko

AU - Duncan, Sylvia H

AU - Drew, Janice E

AU - Williams, Lynda M

AU - Milligan, Graeme

AU - Preston, Thomas

AU - Morrison, Douglas

AU - Flint, Harry J

AU - Louis, Petra

N1 - The Rowett Institute and Biomathematics & Statistics Scotland receive financial support from the Scottish Government Rural and Environmental Sciences and Analytical Services. Nicole Reichardt was funded by a Scottish Government Strategic Partnership on Food and Drink Science. We would like to thank Donna Henderson for carrying out GC analysis and Alan Walker for help and advice with bioinformatic sequence analysis. Supplementary information is available at ISME Journal’s website.

PY - 2018

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N2 - The diet provides carbohydrates that are non-digestible in the upper gut and are major carbon and energy sources for the microbial community in the lower intestine, supporting a complex metabolic network. Fermentation produces the short-chain fatty acids (SCFAs) acetate, propionate and butyrate, which have health-promoting effects for the human host. Here we investigated microbial community changes and SCFA production during in vitro batch incubations of 15 different non-digestible carbohydrates, at two initial pH values with faecal microbiota from three different human donors. To investigate temporal stability and reproducibility, a further experiment was performed 1 year later with four of the carbohydrates. The lower pH (5.5) led to higher butyrate and the higher pH (6.5) to more propionate production. The strongest propionigenic effect was found with rhamnose, followed by galactomannans, whereas fructans and several α- and β-glucans led to higher butyrate production. 16S ribosomal RNA gene-based quantitative PCR analysis of 22 different microbial groups together with 454 sequencing revealed significant stimulation of specific bacteria in response to particular carbohydrates. Some changes were ascribed to metabolite cross-feeding, for example, utilisation by Eubacterium hallii of 1,2-propanediol produced from fermentation of rhamnose by Blautia spp. Despite marked inter-individual differences in microbiota composition, SCFA production was surprisingly reproducible for different carbohydrates, indicating a level of functional redundancy. Interestingly, butyrate formation was influenced not only by the overall % butyrate-producing bacteria in the community but also by the initial pH, consistent with a pH-dependent shift in the stoichiometry of butyrate production.

AB - The diet provides carbohydrates that are non-digestible in the upper gut and are major carbon and energy sources for the microbial community in the lower intestine, supporting a complex metabolic network. Fermentation produces the short-chain fatty acids (SCFAs) acetate, propionate and butyrate, which have health-promoting effects for the human host. Here we investigated microbial community changes and SCFA production during in vitro batch incubations of 15 different non-digestible carbohydrates, at two initial pH values with faecal microbiota from three different human donors. To investigate temporal stability and reproducibility, a further experiment was performed 1 year later with four of the carbohydrates. The lower pH (5.5) led to higher butyrate and the higher pH (6.5) to more propionate production. The strongest propionigenic effect was found with rhamnose, followed by galactomannans, whereas fructans and several α- and β-glucans led to higher butyrate production. 16S ribosomal RNA gene-based quantitative PCR analysis of 22 different microbial groups together with 454 sequencing revealed significant stimulation of specific bacteria in response to particular carbohydrates. Some changes were ascribed to metabolite cross-feeding, for example, utilisation by Eubacterium hallii of 1,2-propanediol produced from fermentation of rhamnose by Blautia spp. Despite marked inter-individual differences in microbiota composition, SCFA production was surprisingly reproducible for different carbohydrates, indicating a level of functional redundancy. Interestingly, butyrate formation was influenced not only by the overall % butyrate-producing bacteria in the community but also by the initial pH, consistent with a pH-dependent shift in the stoichiometry of butyrate production.

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