The species composition of the human intestinal microbiota differs between particle-associated and liquid phase communities

Alan W Walker, Sylvia H Duncan, Hermie J M Harmsen, Grietje Holtrop, Gjalt W Welling, Harry James Flint

Research output: Contribution to journalArticle

81 Citations (Scopus)

Abstract

Many of the substrates available as energy sources for microorganisms in the human colon, including dietary plant fibre and secreted mucin, are insoluble. It seems likely that such insoluble substrates support a specialized microbiota, and in order to test this hypothesis, faecal samples from four healthy subjects were fractionated into insoluble (washed particulate) and liquid fractions. Analysis of 1252 PCR-amplified 16S rRNA sequences revealed a significantly lower percentage of Bacteroidetes (P = 0.021) and a significantly higher percentage of Firmicutes (P = 0.029) among bacterial sequences amplified from particle-associated (mean 76.8% Firmicutes, 18.5% Bacteroidetes) compared with liquid phase (mean 65.8% Firmicutes, 28.5% Bacteroidetes). Within the Firmicutes, the most significant association with solid particles was found for relatives of Ruminococcus-related clostridial cluster IV species that include Ruminococcus flavefaciens and R. bromii, which together accounted for 12.2% of particle-associated, but only 3.3% of liquid phase, sequences. These findings were strongly supported by microscopy, using group-specific FISH probes able to detect these species. This work suggests that the primary colonizers of insoluble substrates found in the gut are restricted to certain specialized groups of bacteria. The abundance of such primary degraders may often be underestimated because of the difficulty in recovering these bacteria and their nucleic acids from the insoluble substrate.

Original languageEnglish
Pages (from-to)3275-3283
Number of pages9
JournalEnvironmental Microbiology
Volume10
Issue number12
Early online date17 Aug 2008
DOIs
Publication statusPublished - Dec 2008

Keywords

  • in-situ hybridization
  • human colon
  • human gut
  • ruminococcus-flavefaciens
  • cell-surface
  • bacteroides-thetaiotaomicron
  • plant polysaccharides
  • bacterial-populations
  • sequence-analysis
  • dominant group
  • adult
  • bacteria
  • biodiversity
  • colon
  • DNA
  • bacterial
  • DNA, ribosomal
  • feces
  • genes
  • rRNA
  • humans
  • in situ hybridization
  • fluorescence
  • microscopy
  • fluorescence, molecular
  • sequence data
  • phylogeny
  • RNA, bacterial
  • RNA, ribosomal
  • 16S
  • sequence analysis, DNA
  • homology
  • nucleic acid

Cite this

The species composition of the human intestinal microbiota differs between particle-associated and liquid phase communities. / Walker, Alan W; Duncan, Sylvia H; Harmsen, Hermie J M; Holtrop, Grietje; Welling, Gjalt W; Flint, Harry James.

In: Environmental Microbiology, Vol. 10, No. 12, 12.2008, p. 3275-3283.

Research output: Contribution to journalArticle

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T1 - The species composition of the human intestinal microbiota differs between particle-associated and liquid phase communities

AU - Walker, Alan W

AU - Duncan, Sylvia H

AU - Harmsen, Hermie J M

AU - Holtrop, Grietje

AU - Welling, Gjalt W

AU - Flint, Harry James

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AB - Many of the substrates available as energy sources for microorganisms in the human colon, including dietary plant fibre and secreted mucin, are insoluble. It seems likely that such insoluble substrates support a specialized microbiota, and in order to test this hypothesis, faecal samples from four healthy subjects were fractionated into insoluble (washed particulate) and liquid fractions. Analysis of 1252 PCR-amplified 16S rRNA sequences revealed a significantly lower percentage of Bacteroidetes (P = 0.021) and a significantly higher percentage of Firmicutes (P = 0.029) among bacterial sequences amplified from particle-associated (mean 76.8% Firmicutes, 18.5% Bacteroidetes) compared with liquid phase (mean 65.8% Firmicutes, 28.5% Bacteroidetes). Within the Firmicutes, the most significant association with solid particles was found for relatives of Ruminococcus-related clostridial cluster IV species that include Ruminococcus flavefaciens and R. bromii, which together accounted for 12.2% of particle-associated, but only 3.3% of liquid phase, sequences. These findings were strongly supported by microscopy, using group-specific FISH probes able to detect these species. This work suggests that the primary colonizers of insoluble substrates found in the gut are restricted to certain specialized groups of bacteria. The abundance of such primary degraders may often be underestimated because of the difficulty in recovering these bacteria and their nucleic acids from the insoluble substrate.

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KW - cell-surface

KW - bacteroides-thetaiotaomicron

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KW - sequence-analysis

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KW - adult

KW - bacteria

KW - biodiversity

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KW - DNA, ribosomal

KW - feces

KW - genes

KW - rRNA

KW - humans

KW - in situ hybridization

KW - fluorescence

KW - microscopy

KW - fluorescence, molecular

KW - sequence data

KW - phylogeny

KW - RNA, bacterial

KW - RNA, ribosomal

KW - 16S

KW - sequence analysis, DNA

KW - homology

KW - nucleic acid

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DO - 10.1111/j.1462-2920.2008.01717.x

M3 - Article

VL - 10

SP - 3275

EP - 3283

JO - Environmental Microbiology

JF - Environmental Microbiology

SN - 1462-2912

IS - 12

ER -