Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men

Anne Salonen, Leo Lahti, Jarkko Salojärvi, Grietje Holtrop, Katri Korpela, Sylvia H Duncan, Priya Date, Freda Farquharson, Alexandra M Johnstone, Gerald E Lobley, Petra Louis, Harry J Flint, Willem M de Vos

Research output: Contribution to journalArticle

167 Citations (Scopus)

Abstract

There is growing interest in understanding how diet affects the intestinal microbiota, including its possible associations with systemic diseases such as metabolic syndrome. Here we report a comprehensive and deep microbiota analysis of 14 obese males consuming fully controlled diets supplemented with resistant starch (RS) or non-starch polysaccharides (NSPs) and a weight-loss (WL) diet. We analyzed the composition, diversity and dynamics of the fecal microbiota on each dietary regime by phylogenetic microarray and quantitative PCR (qPCR) analysis. In addition, we analyzed fecal short chain fatty acids (SCFAs) as a proxy of colonic fermentation, and indices of insulin sensitivity from blood samples. The diet explained around 10% of the total variance in microbiota composition, which was substantially less than the inter-individual variance. Yet, each of the study diets induced clear and distinct changes in the microbiota. Multiple Ruminococcaceae phylotypes increased on the RS diet, whereas mostly Lachnospiraceae phylotypes increased on the NSP diet. Bifidobacteria decreased significantly on the WL diet. The RS diet decreased the diversity of the microbiota significantly. The total 16S ribosomal RNA gene signal estimated by qPCR correlated positively with the three major SCFAs, while the amount of propionate specifically correlated with the Bacteroidetes. The dietary responsiveness of the individual’s microbiota varied substantially and associated inversely with its diversity, suggesting that individuals can be stratified into responders and non-responders based on the features of their intestinal microbiota.
Original languageEnglish
Pages (from-to)2218-2230
Number of pages13
JournalThe ISME Journal
Volume8
Issue number11
Early online date24 Apr 2014
DOIs
Publication statusPublished - Nov 2014

Fingerprint

individual variation
intestinal microorganisms
Microbiota
Fermentation
fermentation
diet
Diet
resistant starch
Starch
Reducing Diet
Volatile Fatty Acids
starch
short chain fatty acids
Polysaccharides
polysaccharide
quantitative polymerase chain reaction
16S Ribosomal RNA
Bacteroidetes
weight loss
polysaccharides

Keywords

  • dietary intervention
  • intestinal microbiota
  • phylogenetic microarray
  • responder
  • short chain fatty acid
  • 16S rRNA

Cite this

Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men. / Salonen, Anne; Lahti, Leo; Salojärvi, Jarkko; Holtrop, Grietje; Korpela, Katri; Duncan, Sylvia H; Date, Priya; Farquharson, Freda; Johnstone, Alexandra M; Lobley, Gerald E; Louis, Petra; Flint, Harry J; de Vos, Willem M.

In: The ISME Journal, Vol. 8, No. 11, 11.2014, p. 2218-2230.

Research output: Contribution to journalArticle

Salonen, Anne ; Lahti, Leo ; Salojärvi, Jarkko ; Holtrop, Grietje ; Korpela, Katri ; Duncan, Sylvia H ; Date, Priya ; Farquharson, Freda ; Johnstone, Alexandra M ; Lobley, Gerald E ; Louis, Petra ; Flint, Harry J ; de Vos, Willem M. / Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men. In: The ISME Journal. 2014 ; Vol. 8, No. 11. pp. 2218-2230.
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AU - Lahti, Leo

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AU - Duncan, Sylvia H

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AU - Johnstone, Alexandra M

AU - Lobley, Gerald E

AU - Louis, Petra

AU - Flint, Harry J

AU - de Vos, Willem M

N1 - We thank the HITChip team from University of Wageningen for excellent technical assistance. This work was partly funded by the Finnish Funding Agency for Technology and Innovation (TEKES) grant 40274/06 (WMdV) and Academy of Finland grants (118602, 1141130, 137389, 141140 (WMdV) and 256950 (LL) and carried out in the context of the Finnish Centre of Excellence in Microbial Food Safety Research (CoE-MiFoSa). The Rowett Institute and Biomathematics and Statistics Scotland receive support from the Scottish Government Food, Land and People program. The human dietary study reported here was largely funded by a grant from the World Cancer Research Fund to HJF, GEL and AMJ.

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N2 - There is growing interest in understanding how diet affects the intestinal microbiota, including its possible associations with systemic diseases such as metabolic syndrome. Here we report a comprehensive and deep microbiota analysis of 14 obese males consuming fully controlled diets supplemented with resistant starch (RS) or non-starch polysaccharides (NSPs) and a weight-loss (WL) diet. We analyzed the composition, diversity and dynamics of the fecal microbiota on each dietary regime by phylogenetic microarray and quantitative PCR (qPCR) analysis. In addition, we analyzed fecal short chain fatty acids (SCFAs) as a proxy of colonic fermentation, and indices of insulin sensitivity from blood samples. The diet explained around 10% of the total variance in microbiota composition, which was substantially less than the inter-individual variance. Yet, each of the study diets induced clear and distinct changes in the microbiota. Multiple Ruminococcaceae phylotypes increased on the RS diet, whereas mostly Lachnospiraceae phylotypes increased on the NSP diet. Bifidobacteria decreased significantly on the WL diet. The RS diet decreased the diversity of the microbiota significantly. The total 16S ribosomal RNA gene signal estimated by qPCR correlated positively with the three major SCFAs, while the amount of propionate specifically correlated with the Bacteroidetes. The dietary responsiveness of the individual’s microbiota varied substantially and associated inversely with its diversity, suggesting that individuals can be stratified into responders and non-responders based on the features of their intestinal microbiota.

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