High temporal and inter-individual variation detected in the human ileal microbiota

Environmental Microbiology

Volumn 12, Issue 12, 2010, Pages 3213-3227

  Booijink, Carien C G M ^a,b   El Aidy, Sahar ^a,b   Rajilić Stojanović, Mirjana ^a   Heilig, Hans G H J ^a   Troost, Freddy J ^b,c   Smidt, Hauke ^a,b   Kleerebezem, Michiel ^a,b   De Vos, Willem M ^a,b   Zoetendal, Erwin G ^a,b  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^c MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; ARTICLE; BACTERIUM; CASE CONTROL STUDY; CLASSIFICATION; FECES; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; ILEOSTOMY; ILEUM; ISOLATION AND PURIFICATION; MALE; METAGENOME; MICROBIOLOGY; MIDDLE AGED; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYMERASE CHAIN REACTION; RNA GENE; TIME;

ADULT; AGED; BACTERIA; CASE-CONTROL STUDIES; FECES; FEMALE; GENES, RRNA; HUMANS; ILEOSTOMY; ILEUM; MALE; METAGENOME; MIDDLE AGED; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMERASE CHAIN REACTION; TIME FACTORS;

ACHAEA; BACTEROIDES PLEBEIUS; CLOSTRIDIALES; LACTOBACILLALES; RUMINOCOCCUS GNAVUS; STREPTOCOCCUS BOVIS; VEILLONELLA;

EID: 77956648022     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2010.02294.x     Document Type: Article

References (52)

1. Ahmed, S., Macfarlane, G.T., Fite, A., McBain, A.J., Gilbert, P., and Macfarlane, S. (2007) Mucosa-associated bacterial diversity in relation to human terminal ileum and colonic biopsy samples. Appl Environ Microbiol 73: 7435-7442.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
3. Andersson, H. (1992) The ileostomy model for the study of carbohydrate digestion and carbohydrate effects on sterol excretion in man. Eur J Clin Nutr 46: S69-S76.
4. Baker, G.C., Smith, J.J., and Cowan, D.A. (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55: 541-555.
5. Baumgart, M., Dogan, B., Rishniw, M., Weitzman, G., Bosworth, B., Yantiss, R., et al. (2007) Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn's disease involving the ileum. ISME J 1: 403-418.
6. Bentley, D.W., Nichols, R.L., Condon, R.E., and Gorbach, S.L. (1972) The microflora of the human ileum and intrabdominal colon: results of direct needle aspiration at surgery and evaluation of the technique. J Lab Clin Med 79: 421-429.
7. Byun, R., Nadkarni, M.A., Chhour, K.L., Martin, F.E., Jacques, N.A., and Hunter, N. (2004) Quantitative analysis of diverse Lactobacillus species present in advanced dental caries. J Clin Microbiol 42: 3128-3136.
8. Claesson, M.J., O'Sullivan, O., Wang, Q., Nikkila, J., Marchesi, J.R., Smidt, H., et al. (2009) Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine. PLoS ONE 4: e6669.
9. Dethlefsen, L., Eckburg, P.B., Bik, E.M., and Relman, D.A. (2006) Assembly of the human intestinal microbiota. Trends Ecol Evol 21: 517-523.
10. Dicksved, J., Halfvarson, J., Rosenquist, M., Jarnerot, G., Tysk, C., Apajalahti, J., et al. (2008) Molecular analysis of the gut microbiota of identical twins with Crohn's disease. ISME J 2: 716-727.
11. Foubert, E.L., and Douglas, H.C. (1948) Studies on the anaerobic micrococci: II. The fermentation of lactate by Micrococcus lactilyticus. J Bacteriol 56: 35-36.
12. Fromin, N., Hamelin, J., Tarnawski, S., Roesti, D., Jourdain-Miserez, K., Forestier, N., et al. (2002) Statistical analysis of denaturing gel electrophoresis (DGE) fingerprinting patterns. Environ Microbiol 4: 634-643.
13. Gill, S.R., Pop, M., Deboy, R.T., Eckburg, P.B., Turnbaugh, P.J., Samuel, B.S., et al. (2006) Metagenomic analysis of the human distal gut microbiome. Science 312: 1355-1359.
14. Gorbach, S.L., Nahas, L., Weinstein, L., Levitan, R., and Patterson, J.F. (1967) Studies of intestinal microflora. IV. The microflora of ileostomy effluent: a unique microbial ecology. Gastroenterology 53: 874-880.
15. Hane, B.G., Jager, K., and Drexler, H.G. (1993) The Pearson product-moment correlation coefficient is better suited for identification of DNA fingerprint profiles than band matching algorithms. Electrophoresis 14: 967-972.
16. Hartman, A.L., Lough, D.M., Barupal, D.K., Fiehn, O., Fishbein, T., Zasloff, M., and Eisen, J.A. (2009) Human gut microbiome adopts an alternative state following small bowel transplantation. Proc Natl Acad Sci USA 106: 17187-17192.
17. Hayashi, H., Sakamoto, M., Kitahara, M., and Benno, Y. (2003) Molecular analysis of fecal microbiota in elderly individuals using 16S rDNA library and T-RFLP. Microbiol Immunol 47: 557-570.
18. Hayashi, H., Takahashi, R., Nishi, T., Sakamoto, M., and Benno, Y. (2005) Molecular analysis of jejunal, ileal, caecal and recto-sigmoidal human colonic microbiota using 16S rRNA gene libraries and terminal restriction fragment length polymorphism. J Med Microbiol 54: 1093-1101.
19. Heilig, H.G.H.J., Zoetendal, E.G., Vaughan, E.E., Marteau, P., Akkermans, A.D.L., and De Vos, W.M. (2002) Molecular diversity of Lactobacillus spp. and other lactic acid bacteria in the human intestine as determined by specific amplification of 16S ribosomal DNA. Appl Environ Microbiol 68: 114-123.
20. Hope, A. (1968) A simplified Monte Carlo significance test procedure. J R Stat Soc 30B: 582-598.
21. Kane, M.D., Poulsen, L.K., and Stahl, D.A. (1993) Monitoring the enrichment and isolation of sulfate-reducing bacteria by using oligonucleotide hybridization probes designed from environmentally derived 16S rRNA sequences. Appl Environ Microbiol 59: 682-686.
22. Kurokawa, K., Itoh, T., Kuwahara, T., Oshima, K., Toh, H., Toyoda, A., et al. (2007) Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res 14: 169-181.
23. Lane, D.J. (1991) 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematic. Stackebrandt, E., and Goodfellow, M. (eds). Chichester, UK: John Wiley & Sons, pp. 115-175.
24. Leps, J., and Smilauer, P. (2003) Multivariate Analysis of Ecological Data Using CANOCO. Cambridge, UK: Cambridge University Press.
25. Ley, R.E., Turnbaugh, P.J., Klein, S., and Gordon, J.I. (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444: 1022-1023.
26. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
27. Matsuki, T., Watanabe, K., Fujimoto, J., Takada, T., and Tanaka, R. (2004) Use of 16S rRNA gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in human feces. Appl Environ Microbiol 70: 7220-7228.
28. Mattila-Sandholm, T., Blaut, M., Daly, C., De Vuyst, L., Doré, J., Gibson, G., et al. (2002) Food, GI-tract functionality and human health cluster: PROEUHEALTH. Microb Ecol Health Dis 14: 65-74.
29. Maukonen, J., Matto, J., Suihko, M.L., and Saarela, M. (2008) Intra-individual diversity and similarity of salivary and faecal microbiota. J Med Microbiol 57: 1560-1568.
30. Milinovich, G.J., Burrell, P.C., Pollitt, C.C., Bouvet, A., and Trott, D.J. (2008) Streptococcus henryi sp. nov. and Streptococcus caballi sp. nov., isolated from the hindgut of horses with oligofructose-induced laminitis. Int J Syst Evol Microbiol 58: 262-266.
31. Muyzer, G., De Waal, E.C., and Uitterlinden, A.G. (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59: 695-700.
32. Neut, C., Bulois, P., Desreumaux, P., Membre, J.M., Lederman, E., Gambiez, L., et al. (2002) Changes in the bacterial flora of the neoterminal ileum after ileocolonic resection for Crohn's disease. Am J Gastroenterol 97: 939-946.
33. Nubel, U., Engelen, B., Felske, A., Snaidr, J., Wieshuber, A., Amann, R.I., et al. (1996) Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J Bacteriol 178: 5636-5643.
34. Rajilić-Stojanović, M. (2007) Diversity of the human gastrointesinal microbiota - novel perspectives from high throughput analyses. PhD Thesis. Wageningen, the Netherlands: Laboratory of Microbiology, Wageningen University, pp. 1-214.
35. Rajilić-Stojanović, M., Smidt, H., and De Vos, W.M. (2007) Diversity of the human gastrointestinal tract microbiota revisited. Environ Microbiol 9: 2125-2136.
36. Rajilić-Stojanović, M., Heilig, H.G.H.J., Molenaar, D., Kajander, K., Surakka, A., Smidt, H., and De Vos, W.M. (2009) Development and application of the human intestinal tract chip, a phylogenetic microarray: analysis of universally conserved phylotypes in the abundant microbiota of young and elderly adults. Environ Microbiol 11: 1736-1751.
37. Reysenbach, A.-L., and Pace, N.R. (1995) Protocol 16. Reliable amplification of hyperthermophilic archaeal 16S rRNA genes by the polymerase chain reaction. In Archaea: A Laboratory Manual - Thermophiles, Vol. 3. Robb, F.T., and Place, A.R. (eds). Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press, pp. 101-107.
38. Ruseler-van Embden, J.G., Schouten, W.R., Van Lieshout, L.M., and Auwerda, H.J. (1992) Changes in bacterial composition and enzymatic activity in ileostomy and ileal reservoir during intermittent occlusion: a study using dogs. Appl Environ Microbiol 58: 111-118.
39. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. New York, USA: Cold Spring Harbor.
40. Sanguinetti, C.J., Dias Neto, E., and Simpson, A.J. (1994) Rapid silver staining and recovery of PCR products separated on polyacrylamide gels. Biotechniques 17: 914-921.
41. Simpson, E.H. (1949) Measurement of diversity. Nature 163: 688-688.
42. Suzuki, M.T., Taylor, L.T., and DeLong, E.F. (2000) Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5'-nuclease assays. Appl Environ Microbiol 66: 4605-4614.
43. Tap, J., Mondot, S., Levenez, F., Pelletier, E., Caron, C., Furet, J.P., et al. (2009) Towards the human intestinal microbiota phylogenetic core. Environ Microbiol 11: 2574-2584.
44. Turnbaugh, P.J., Hamady, M., Yatsunenko, T., Cantarel, B.L., Duncan, A., Ley, R.E., et al. (2009) A core gut microbiome in obese and lean twins. Nature 457: 480-484.
45. Vanhoutte, T., Huys, F., De Brandt, E., and Swings, J. (2004) Temporal stability analysis of the microbiota in human feces by denaturing gradient gel electrophoresis using universal and group-specific 16S rRNA gene primers. FEMS Microbiol Ecol 48: 437-446.
46. Wang, M., Ahrne, S., Jeppsson, B., and Molin, G. (2005) Comparison of bacterial diversity along the human intestinal tract by direct cloning and sequencing of 16S rRNA genes. FEMS Microbiol Ecol 54: 219-231.
47. Wang, X., Heazlewood, S.P., Krause, D.O., and Florin, T.H. (2003) Molecular characterization of the microbial species that colonize human ileal and colonic mucosa by using 16S rDNA sequence analysis. J Appl Microbiol 95: 508-520.
48. Willing, B., Halfvarson, J., Dicksved, J., Rosenquist, M., Jarnerot, G., Engstrand, L., et al. (2009) Twin studies reveal specific imbalances in the mucosa-associated microbiota of patients with ileal Crohn's disease. Inflamm Bowel Dis 15: 653-660.
49. Zoetendal, E.G., Akkermans, A.D.L., and De Vos, W.M. (1998) Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl Environ Microbiol 64: 3854-3859.
50. Zoetendal, E.G., Akkermans, A.D.L., Akkermans-van Vliet, W.M., De Visser, A.G.M., and De Vos, W.M. (2001) The host genotype affects the bacterial community in the human gastrointestinal tract. Microb Ecol Health Dis 13: 129-134.
51. Zoetendal, E.G., Heilig, H.G.H.J., Klaassens, E.M., Booijink, C.C.G.M., Kleerebezem, M., Smidt, H., and De Vos, W.M. (2006) Isolation of DNA from bacterial samples of the human gastrointestinal tract. Nat Protoc 1: 870-873.
52. Zoetendal, E.G., Rajilić-Stojanović, M., and De Vos, W.M. (2008) High-throughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut 57: 1605-1615.