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Arabinoxylans and inulin differentially modulate the mucosal and luminal gut microbiota and mucin-degradation in humanized rats

Pieter Van den Abbeele, Philippe Gerard, Sylvie Rabot, Aurelia Bruneau, Sahar El Aidy, Muriel Derrien, Michiel Kleerebezem, Erwin G Zoetendal, Hauke Smidt, Willy Verstraete UGent, et al. (2011) ENVIRONMENTAL MICROBIOLOGY. 13(10). p.2667-2680
abstract
The endogenous gut microbiota affects the host in many ways. Prebiotics should favour beneficial intestinal microbes and thus improve host health. In this study, we investigated how a novel class of potential prebiotic long-chain arabinoxylans (LC-AX) and the well-established prebiotic inulin (IN) modulate the gut microbiota of humanized rats. Six weeks after axenic rats were inoculated with a human faecal microbiota, their colonic microbiota was similar to this inoculum (similar to 70%), whereas their caecal microbiota was enriched with Verrucomicrobia and Firmicutes concomitant with lower abundance of Bacteroidetes. Moreover, different Bifidobacterium species colonized the lumen (B. adolescentis) and mucus (B. longum and B. bifidum). Both LC-AX and IN increased SCFA levels and induced a shift from acetate towards health-promoting propionate and butyrate respectively. By applying a high-resolution phylogenetic micro-array (HITChip) at the site of fermentation (caecum), IN and LC-AX were shown to stimulate bacterial groups with known butyrate-producers (Roseburia intestinalis, Eubacterium rectale, Anaerostipes caccae) and bifidobacteria (B. longum) respectively. Prebiotic administration also resulted in lower caecal abundances of the mucin-degrading Akkermansia muciniphila and potentially more mucin production by the host. Both factors might explain the increased caecal mucin levels for LC-AX (threefold) and IN (sixfold). These mucins were degraded along the colon, resulting in high faecal abundances of Akkermansia muciniphila for LC-AX and especially IN-treated rats. Finally, the microbial changes caused an adaptation period for the host with less weight gain, after which the host fine-tuned the interaction with this altered microbiota. Our results demonstrate that next to IN, LC-AX are promising prebiotic compounds by stimulating production of health-promoting metabolites by specific microbes in the proximal regions. Further, prebiotic supplementation shifted mucin degradation to distal regions, where mucin-degraders may produce beneficial metabolites (e. g. propionate by Akkermansia muciniphila), so that prebiotics may potentially improve gut health along the entire length of the intestine.
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author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
CHAIN FATTY-ACIDS, 16S RIBOSOMAL-RNA, GRADIENT GEL-ELECTROPHORESIS, BUTYRATE-PRODUCING BACTERIUM, HUMAN GASTROINTESTINAL-TRACT, HUMAN INTESTINAL MICROBIOTA, INFLAMMATORY-BOWEL-DISEASE, IN-VITRO FERMENTATION, FECAL MICROBIOTA, HUMAN FECES
journal title
ENVIRONMENTAL MICROBIOLOGY
Environ. Microbiol.
volume
13
issue
10
pages
2667 - 2680
Web of Science type
Article
Web of Science id
000295971300005
JCR category
MICROBIOLOGY
JCR impact factor
5.843 (2011)
JCR rank
14/111 (2011)
JCR quartile
1 (2011)
ISSN
1462-2912
DOI
10.1111/j.1462-2920.2011.02533.x
project
Biotechnology for a sustainable economy (Bio-Economy)
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
1981038
handle
http://hdl.handle.net/1854/LU-1981038
date created
2012-01-09 16:14:11
date last changed
2016-12-19 15:45:28
@article{1981038,
  abstract     = {The endogenous gut microbiota affects the host in many ways. Prebiotics should favour beneficial intestinal microbes and thus improve host health. In this study, we investigated how a novel class of potential prebiotic long-chain arabinoxylans (LC-AX) and the well-established prebiotic inulin (IN) modulate the gut microbiota of humanized rats. Six weeks after axenic rats were inoculated with a human faecal microbiota, their colonic microbiota was similar to this inoculum (similar to 70\%), whereas their caecal microbiota was enriched with Verrucomicrobia and Firmicutes concomitant with lower abundance of Bacteroidetes. Moreover, different Bifidobacterium species colonized the lumen (B. adolescentis) and mucus (B. longum and B. bifidum). Both LC-AX and IN increased SCFA levels and induced a shift from acetate towards health-promoting propionate and butyrate respectively. By applying a high-resolution phylogenetic micro-array (HITChip) at the site of fermentation (caecum), IN and LC-AX were shown to stimulate bacterial groups with known butyrate-producers (Roseburia intestinalis, Eubacterium rectale, Anaerostipes caccae) and bifidobacteria (B. longum) respectively. Prebiotic administration also resulted in lower caecal abundances of the mucin-degrading Akkermansia muciniphila and potentially more mucin production by the host. Both factors might explain the increased caecal mucin levels for LC-AX (threefold) and IN (sixfold). These mucins were degraded along the colon, resulting in high faecal abundances of Akkermansia muciniphila for LC-AX and especially IN-treated rats. Finally, the microbial changes caused an adaptation period for the host with less weight gain, after which the host fine-tuned the interaction with this altered microbiota. Our results demonstrate that next to IN, LC-AX are promising prebiotic compounds by stimulating production of health-promoting metabolites by specific microbes in the proximal regions. Further, prebiotic supplementation shifted mucin degradation to distal regions, where mucin-degraders may produce beneficial metabolites (e. g. propionate by Akkermansia muciniphila), so that prebiotics may potentially improve gut health along the entire length of the intestine.},
  author       = {Van den Abbeele, Pieter and Gerard, Philippe and Rabot, Sylvie and Bruneau, Aurelia and El Aidy, Sahar and Derrien, Muriel and Kleerebezem, Michiel and Zoetendal, Erwin G and Smidt, Hauke and Verstraete, Willy and Van de Wiele, Tom and Possemiers, Sam},
  issn         = {1462-2912},
  journal      = {ENVIRONMENTAL MICROBIOLOGY},
  keyword      = {CHAIN FATTY-ACIDS,16S RIBOSOMAL-RNA,GRADIENT GEL-ELECTROPHORESIS,BUTYRATE-PRODUCING BACTERIUM,HUMAN GASTROINTESTINAL-TRACT,HUMAN INTESTINAL MICROBIOTA,INFLAMMATORY-BOWEL-DISEASE,IN-VITRO FERMENTATION,FECAL MICROBIOTA,HUMAN FECES},
  language     = {eng},
  number       = {10},
  pages        = {2667--2680},
  title        = {Arabinoxylans and inulin differentially modulate the mucosal and luminal gut microbiota and mucin-degradation in humanized rats},
  url          = {http://dx.doi.org/10.1111/j.1462-2920.2011.02533.x},
  volume       = {13},
  year         = {2011},
}

Chicago
Van den Abbeele, Pieter, Philippe Gerard, Sylvie Rabot, Aurelia Bruneau, Sahar El Aidy, Muriel Derrien, Michiel Kleerebezem, et al. 2011. “Arabinoxylans and Inulin Differentially Modulate the Mucosal and Luminal Gut Microbiota and Mucin-degradation in Humanized Rats.” Environmental Microbiology 13 (10): 2667–2680.
APA
Van den Abbeele, P., Gerard, P., Rabot, S., Bruneau, A., El Aidy, S., Derrien, M., Kleerebezem, M., et al. (2011). Arabinoxylans and inulin differentially modulate the mucosal and luminal gut microbiota and mucin-degradation in humanized rats. ENVIRONMENTAL MICROBIOLOGY, 13(10), 2667–2680.
Vancouver
1.
Van den Abbeele P, Gerard P, Rabot S, Bruneau A, El Aidy S, Derrien M, et al. Arabinoxylans and inulin differentially modulate the mucosal and luminal gut microbiota and mucin-degradation in humanized rats. ENVIRONMENTAL MICROBIOLOGY. 2011;13(10):2667–80.
MLA
Van den Abbeele, Pieter, Philippe Gerard, Sylvie Rabot, et al. “Arabinoxylans and Inulin Differentially Modulate the Mucosal and Luminal Gut Microbiota and Mucin-degradation in Humanized Rats.” ENVIRONMENTAL MICROBIOLOGY 13.10 (2011): 2667–2680. Print.