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High temporal and inter‐individual variation detected in the human ileal microbiota
Open accessAbstract
Summary: The diversity and temporal stability of the predominant bacteria in the human ileum was studied with the use of ileal effluent samples of seven individuals with Brooke ileostomies. The total number of bacteria within the ileal effluent was in the range of 10 7 –10 8 bacteria per gram (wet weight). The diversity of the bacteria in the ileal effluent showed marked differences compared with that in faecal samples from age‐matched healthy adults. The ileal effluent had a higher relative abundance of species within the orders Lactobacillales and Clostridiales , mainly Streptococcus bovis ‐related species, and the Veillonella group, and a lower proportion of species related to Ruminococcus gnavus , R. obeum and Bacteroides plebeius . In addition, inter‐individual differences were found, indicative of a highly personal ileal microbiota profile. Furthermore, temporal profiles showed large fluctuations per individual over a period of 9–28 days (average similarity over a period of 9 days was as low as 44%), and differences between morning and afternoon profiles were observed. Parallel cloning and sequencing efforts revealed several phylotypes that were not identified in previous studies (12 out of 65 phylotypes showed less than 97% sequence similarity with previously reported sequences). Achaea were found to be below detection limit by quantitative PCR. Overall, the results indicate that the microbiota of the human ileum is relatively unstable, less complex and consisting of different dominating phylotypes when compared with the colonic microbiota.
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“Oligosaccharides that are not hydrolyzed and absorbed in the small intestine are rapidly fermented by intestinal microbiota in the terminal ileum and the proximal colon [2,3].”
BackgroundIn vitro human gut microbiota fermentation models: opportunities, challenges, and pitfalls
Isenring, J., Bircher, L., Geirnaert, A., & Lacroix, C. (2023) · Microbiome Research Reports · doi:10.20517/mrr.2022.15 · Cited by 109
Seekatz, A. M., Schnizlein, M. K., Koenigsknecht, M. J., Baker, J. R., Hasler, W. L., Bleske, B. E., Young, V. B., & Sun, D. (2019) · mSphere · doi:10.1128/msphere.00126-19 · Cited by 98
“Single lumen naso-ileal tubes are unable to sample multiple sites simultaneously (18, 20, 21, 32).”
Genomics of Streptococcus salivarius , a major human commensal
Delorme, C., Abraham, A., Renault, P., & Guédon, É. (2014) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2014.10.001 · Cited by 103
Consumption of Lysozyme-Rich Milk Can Alter Microbial Fecal Populations
Maga, E. A., Desai, P., Weimer, B. C., Dao, N., Kültz, D., & Murray, J. D. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.00956-12 · Cited by 96
“tive tract (35), with the largest diversity and most bacteria found in the colon, and therefore the microbiota of feces is distinct from that of the rest of the GI tract in both pigs (7) and humans (4, 41).”
BackgroundThe microbiome: Composition and locations
Kennedy, M. S., & Chang, E. B. (2020) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2020.08.013 · Cited by 108
Characterization of the Gastrointestinal Microbiota in Health and Inflammatory Bowel Disease
Cruz, P. P. D., Prideaux, L., Wagner, J., Ng, S. C., McSweeney, C. S., Kirkwood, C. D., Morrison, M., & Kamm, M. A. (2011) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21751 · Cited by 97
Small intestinal bacterial overgrowth
Quigley, E. M. M. (2014) · Current Opinion in Gastroenterology · doi:10.1097/mog.0000000000000040 · Cited by 96
The emerging role of the small intestinal microbiota in human health and disease
Ruigrok, R. A. A. A., Weersma, R. K., & Vila, A. V. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2201155 · Cited by 101
Zaccaria, E., van Baarlen, P., de Greeff, A., Morrison, D. A., Smith, H. E., & Wells, J. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0099394 · Cited by 92
“In the gut HGT and natural competence are likely to have played a major role in the evolution and ecology of the microbiota as well as strain diversity [8].”
Patterns and Processes in Parasite Co-Infection
Viney, M., & Graham, A. L. (2013) · Advances in Parasitology/Advances in parasitology · doi:10.1016/b978-0-12-407706-5.00005-8 · Cited by 95
Species Level Description of the Human Ileal Bacterial Microbiota
Villmones, H. C., Haug, E. S., Ulvestad, E., Grude, N., Stenstad, T., Halland, A., & Kommedal, Ø. (2018) · Scientific Reports · doi:10.1038/s41598-018-23198-5 · Cited by 91
Heterogeneity across the murine small and large intestine
Bowcutt, R. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i41.15216 · Cited by 96
Cui, Z., Huntley, R. B., Zeng, Q., & Steven, B. T. (2020) · The ISME Journal · doi:10.1038/s41396-020-00784-y · Cited by 84
Jejunum: The understudied meeting place of dietary lipids and the microbiota
Lema, I., Araújo, J. R., Rolhion, N., & Demignot, S. (2020) · Biochimie · doi:10.1016/j.biochi.2020.09.007 · Cited by 92
The human gut microbiome: are we our enterotypes?
Siezen, R. J., & Kleerebezem, M. (2011) · Microbial Biotechnology · doi:10.1111/j.1751-7915.2011.00290.x · Cited by 88
“It remains to be seen whether such stable and universal microbial consortia are also found in the small intestine where the genera Streptococcus, Clostridium and Veillonella are dominant (Booijink et al., 2007; 2010a,b; van den Bogert et al., 2011).”
BackgroundSelf-citationDlugosz, A., Winckler, B., Lundin, E., Zakikhany, K., Sandström, G., Ye, W., Engstrand, L. G., & Lindberg, G. (2015) · Scientific Reports · doi:10.1038/srep08508 · Cited by 85
Fanning, S., Hall, L. J., & van Sinderen, D. (2012) · Gut Microbes · doi:10.4161/gmic.20630 · Cited by 87
“Promoter fusions and primer extension analyses revealed the main promoters health is explored through metagenome projects, which analyze microbial composition and functionality,4,5,19,20 as well as stability.(21,22) These and other studies have greatly enhanced our knowledge on what constitutes a “normal” or healthy m…”
BackgroundZhang, Q., Zhong, D., Sun, R., Zhang, Y., Pegg, R. B., & Zhong, G. (2020) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2020.117418 · Cited by 83
Cell surface-associated compounds of probiotic lactobacilli sustain the strain-specificity dogma
Bron, P. A., Tomita, S., Mercenier, A., & Kleerebezem, M. (2013) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.06.001 · Cited by 86
Self-citationBiological factors controlling starch digestibility in human digestive system
Li, C., Hu, Y., Li, S., Yi, X., Shao, S., Yu, W., & Li, E. (2022) · Food Science and Human Wellness · doi:10.1016/j.fshw.2022.07.037 · Cited by 81
Comparison of the Distal Gut Microbiota from People and Animals in Africa
Ellis, R. J., Bruce, K. D., Jenkins, C., Stothard, J. R., Ajarova, L., Mugisha, L., & Viney, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054783 · Cited by 76
“microbial exposure, diet, infection effects [12,13,17–20]) and a genetic component [1,14,21,22] controlling the composition of the microbiota.”
BackgroundSystems biology of the gut: the interplay of food, microbiota and host at the mucosal interface
dos Santos, V. A. P. M., Müller, M. M., & de Vos, W. M. (2010) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2010.08.003 · Cited by 79
Unraveling the Role of the Human Gut Microbiome in Health and Diseases
Khalil, M., Ciaula, A. D., Mahdi, L., Jaber, N., Palo, D. M. D., Graziani, A., Baffy, G., & Portincasa, P. (2024) · Microorganisms · doi:10.3390/microorganisms12112333 · Cited by 100
“At this level, the community is mainly composed of facultative anaerobes, including phyla Proteobacteria and Bacteroides populated by Streptococci , Lactobacilli , and Enterococci species [58,59].”
Talley, N. J., Holtmann, G., & Walker, M. M. (2015) · Journal of Gastroenterology · doi:10.1007/s00535-015-1076-x · Cited by 75
“Jejunal and ileal microbiota consist mainly of facultative anaerobes, including streptococci, lactobacilli, the genus Veillonella, Proteobacteria and Bacteroides [78].”
van den Bogert, B., Boekhorst, J., Herrmann, R., Smid, E. J., Zoetendal, E. G., & Kleerebezem, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0083418 · Cited by 74
“parasanguinis are commonly detected as relatively dominant inhabitants in the upper respiratory tract [1], oral cavity [4,5], throat [6], esophagus [7], stomach [8], and small-intestine [9,10,11] of healthy individuals.”
BackgroundMethodInfluentialSelf-citationImpact of protein on the composition and metabolism of the human gut microbiota and health
Duncan, S. H., Iyer, A. B., & Russell, W. R. (2020) · Proceedings of The Nutrition Society · doi:10.1017/s0029665120008022 · Cited by 72
“Many of the Gram-positive Firmicutes species are more tolerant of the mildly acidic conditions in the proximal colon which is likely to provide a competitive advantage for these bacterial species, whereas the growth of Bacteroidetes species are likely to be restricted here but are likely to be more active in the dista…”
InfluentialProbiotics and gut health: linking gut homeostasis and poultry productivity
Shini, S., & Bryden, W. L. (2021) · Animal Production Science · doi:10.1071/an20701 · Cited by 78
“The pH (close to neutral), and a longer transit time through the ileum create a suitable environment for microbial growth and metabolism (Booijink et al. 2010; Gerritsen et al. 2011).”
BackgroundThe small intestine: dining table of host–microbiota meetings
Delbaere, K., Roegiers, I. H., Bron, A., Durif, C., de Wiele, T. V., Blanquet‐Diot, S., & Marinelli, L. (2023) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuad022 · Cited by 73
“Through a batch set-up inoculated with ileostomy effluent in airtight ano xic tubes, shak en and incubated at 37 ◦C for 24 h, the authors studied the impact of ileal microbial digestion on the green tea catechins and described interindividual differences between donors in both aerobic ( E. coli , Proteus sp ., and Ent…”
InfluentialFuller, M. F. (2012) · British Journal Of Nutrition · doi:10.1017/s0007114512002279 · Cited by 71
“Although there have been several studies of the microbiology of human ileostomy fluid((52,61,62)) there is understandably rather little information about the normal human ileal microbiota.”
Early life establishment of site-specific microbial communities in the gut
Romano-Keeler, J., Moore, D. J., Wang, C., Brucker, R. M., Fonnesbeck, C., Slaughter, J. C., Li, H., Curran, D. P., Meng, S., Correa, H., et al. (2014) · Gut Microbes · doi:10.4161/gmic.28442 · Cited by 66
“com Gut Microbes 197 in adults where feces have a greater microbial diversity than intestinal mucosa(10,12) or ileostomy effluent.(23) Samples of the neonatal microbiota collected anywhere from seconds to within 24 h after delivery across different body habitats (skin, oral, and rectal mucosa) were relatively homogene…”
BackgroundMolecular Mechanisms of Lacticaseibacillus rhamnosus, LGG® Probiotic Function
Leser, T. D., & Baker, A. (2024) · Microorganisms · doi:10.3390/microorganisms12040794 · Cited by 65
“Microbiota analyses predominantly rely on stool samples which, at best, represent the microbiota of the distal colon but not the small intestine [16].”
Background
Metadata
- Authors
- Booijink, C. C. G. M., El‐Aidy, S., Rajilić‐Stojanović, M., Heilig, H. G. H. J., Troost, F. J., Smidt, H., Kleerebezem, M., De Vos, W. M., & Zoetendal, E. G.
- Affiliations
- TiFN (NL)
- Wageningen University & Research (NL)
- Maastricht University Medical Centre (NL)
- Corresponding author
- Zoetendal, Erwin G.
- Venue
- Environmental Microbiology
- Publisher
- Wiley
- Published
- 2010-12
- Volume
- 12
- Issue
- 12
- Pages
- 3213-3227
- ISSN
- 1462-2912 (ISSN-L)
- 1462-2920
- OpenAlex
- W2130329894
- Cited by
- 324
- References
- 52
- Citations by year
- 2026: 9 · 2025: 13 · 2024: 17 · 2023: 27 · 2022: 22 · 2021: 23 · 2020: 30 · 2019: 29 · 2018: 24 · 2017: 17 · 2016: 10 · 2015: 15 · 2014: 24 · 2013: 28 · 2012: 18
- FWCI
- 8.31
- Type
- journal article
- Language
- en
- Open access
- green
- research.wur.nl
- Locations
- Environmental Microbiology (publishedVersion)
- PubMed (publishedVersion)
- TechnoRep (University of Belgrade – Faculty of Technology and Metallurgy) (publishedVersion)
- Research Publications (Maastricht University) (publishedVersion)
- Socio-Environmental Systems Modeling (acceptedVersion)
- Research Publications (Maastricht University) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Keywords
- ileal microbiota, ileostomy, temporal stability, interindividual variability, bacterial diversity, Lactobacillales, Clostridiales, Streptococcus bovis, Veillonella, Ruminococcus, Bacteroides plebeius, Achaea, novel phylotypes, human gut bacteria
- MeSH terms
- Adult, Aged, Bacteria, Feces, Female, Humans, Ileostomy, Ileum, Male, Middle Aged, Molecular Sequence Data, Phylogeny, Time Factors, Case-Control Studies, Polymerase Chain Reaction, Genes, rRNA, Metagenome
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