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Microbial community development in a dynamic gut model is reproducible, colon region specific, and selective for Bacteroidetes and Clostridium cluster IX

Pieter Van den Abbeele, Charlotte Grootaert UGent, Massimo Marzorati UGent, Sam Possemiers, Willy Verstraete UGent, Philippe Gerard, Sylvie Rabot, Aurelia Bruneau, Sahar El Aidy, Muriel Derrien, et al. (2010) APPLIED AND ENVIRONMENTAL MICROBIOLOGY. 76(15). p.5237-5246
abstract
Dynamic, multicompartment in vitro gastrointestinal simulators are often used to monitor gut microbial dynamics and activity. These reactors need to harbor a microbial community that is stable upon inoculation, colon region specific, and relevant to in vivo conditions. Together with the reproducibility of the colonization process, these criteria are often overlooked when the modulatory properties from different treatments are compared. We therefore investigated the microbial colonization process in two identical simulators of the human intestinal microbial ecosystem (SHIME), simultaneously inoculated with the same human fecal microbiota with a high-resolution phylogenetic microarray: the human intestinal tract chip (HITChip). Following inoculation of the in vitro colon compartments, microbial community composition reached steady state after 2 weeks, whereas 3 weeks were required to reach functional stability. This dynamic colonization process was reproducible in both SHIME units and resulted in highly diverse microbial communities which were colon region specific, with the proximal regions harboring saccharolytic microbes (e. g., Bacteroides spp. and Eubacterium spp.) and the distal regions harboring mucin-degrading microbes (e. g., Akkermansia spp.). Importantly, the shift from an in vivo to an in vitro environment resulted in an increased Bacteroidetes/Firmicutes ratio, whereas Clostridium cluster IX (propionate producers) was enriched compared to clusters IV and XIVa (butyrate producers). This was supported by proportionally higher in vitro propionate concentrations. In conclusion, high-resolution analysis of in vitro-cultured gut microbiota offers new insight on the microbial colonization process and indicates the importance of digestive parameters that may be crucial in the development of new in vitro models.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
HUMAN INTESTINAL BACTERIA, 8-PRENYLNARINGENIN IN-VITRO, CONTINUOUS-CULTURE SYSTEM, ECOSYSTEM, SIMULATOR, FERMENTATION, INNATE IMMUNITY, RETENTION TIME, HUMULUS-LUPULUS L., GASTROINTESTINAL-TRACT
journal title
APPLIED AND ENVIRONMENTAL MICROBIOLOGY
Appl. Environ. Microbiol.
volume
76
issue
15
pages
5237 - 5246
Web of Science type
Article
Web of Science id
000280266200037
JCR category
BIOTECHNOLOGY & APPLIED MICROBIOLOGY
JCR impact factor
3.778 (2010)
JCR rank
32/158 (2010)
JCR quartile
1 (2010)
ISSN
0099-2240
DOI
10.1128/AEM.00759-10
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
1107099
handle
http://hdl.handle.net/1854/LU-1107099
date created
2011-01-21 11:59:49
date last changed
2016-12-19 15:46:15
@article{1107099,
  abstract     = {Dynamic, multicompartment in vitro gastrointestinal simulators are often used to monitor gut microbial dynamics and activity. These reactors need to harbor a microbial community that is stable upon inoculation, colon region specific, and relevant to in vivo conditions. Together with the reproducibility of the colonization process, these criteria are often overlooked when the modulatory properties from different treatments are compared. We therefore investigated the microbial colonization process in two identical simulators of the human intestinal microbial ecosystem (SHIME), simultaneously inoculated with the same human fecal microbiota with a high-resolution phylogenetic microarray: the human intestinal tract chip (HITChip). Following inoculation of the in vitro colon compartments, microbial community composition reached steady state after 2 weeks, whereas 3 weeks were required to reach functional stability. This dynamic colonization process was reproducible in both SHIME units and resulted in highly diverse microbial communities which were colon region specific, with the proximal regions harboring saccharolytic microbes (e. g., Bacteroides spp. and Eubacterium spp.) and the distal regions harboring mucin-degrading microbes (e. g., Akkermansia spp.). Importantly, the shift from an in vivo to an in vitro environment resulted in an increased Bacteroidetes/Firmicutes ratio, whereas Clostridium cluster IX (propionate producers) was enriched compared to clusters IV and XIVa (butyrate producers). This was supported by proportionally higher in vitro propionate concentrations. In conclusion, high-resolution analysis of in vitro-cultured gut microbiota offers new insight on the microbial colonization process and indicates the importance of digestive parameters that may be crucial in the development of new in vitro models.},
  author       = {Van den Abbeele, Pieter and Grootaert, Charlotte and Marzorati, Massimo and Possemiers, Sam and Verstraete, Willy and Gerard, Philippe and Rabot, Sylvie and Bruneau, Aurelia and El Aidy, Sahar and Derrien, Muriel and Zoetendal, Erwin and Kleerebezem, Michiel and Smidt, Hauke and Van de Wiele, Tom},
  issn         = {0099-2240},
  journal      = {APPLIED AND ENVIRONMENTAL MICROBIOLOGY},
  keyword      = {HUMAN INTESTINAL BACTERIA,8-PRENYLNARINGENIN IN-VITRO,CONTINUOUS-CULTURE SYSTEM,ECOSYSTEM,SIMULATOR,FERMENTATION,INNATE IMMUNITY,RETENTION TIME,HUMULUS-LUPULUS L.,GASTROINTESTINAL-TRACT},
  language     = {eng},
  number       = {15},
  pages        = {5237--5246},
  title        = {Microbial community development in a dynamic gut model is reproducible, colon region specific, and selective for Bacteroidetes and Clostridium cluster IX},
  url          = {http://dx.doi.org/10.1128/AEM.00759-10},
  volume       = {76},
  year         = {2010},
}

Chicago
Van den Abbeele, Pieter, Charlotte Grootaert, Massimo Marzorati, Sam Possemiers, Willy Verstraete, Philippe Gerard, Sylvie Rabot, et al. 2010. “Microbial Community Development in a Dynamic Gut Model Is Reproducible, Colon Region Specific, and Selective for Bacteroidetes and Clostridium Cluster IX.” Applied and Environmental Microbiology 76 (15): 5237–5246.
APA
Van den Abbeele, P., Grootaert, C., Marzorati, M., Possemiers, S., Verstraete, W., Gerard, P., Rabot, S., et al. (2010). Microbial community development in a dynamic gut model is reproducible, colon region specific, and selective for Bacteroidetes and Clostridium cluster IX. APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 76(15), 5237–5246.
Vancouver
1.
Van den Abbeele P, Grootaert C, Marzorati M, Possemiers S, Verstraete W, Gerard P, et al. Microbial community development in a dynamic gut model is reproducible, colon region specific, and selective for Bacteroidetes and Clostridium cluster IX. APPLIED AND ENVIRONMENTAL MICROBIOLOGY. 2010;76(15):5237–46.
MLA
Van den Abbeele, Pieter, Charlotte Grootaert, Massimo Marzorati, et al. “Microbial Community Development in a Dynamic Gut Model Is Reproducible, Colon Region Specific, and Selective for Bacteroidetes and Clostridium Cluster IX.” APPLIED AND ENVIRONMENTAL MICROBIOLOGY 76.15 (2010): 5237–5246. Print.