Three-stage continuous culture system with a self-generated anaerobia to study the regionalized metabolism of the human gut microbiota

Journal of Microbiological Methods

Volumn 96, Issue 1, 2014, Pages 111-118

  Feria Gervasio, David ^a   Tottey, William ^a   Gaci, Nadia ^a   Alric, Monique ^a   Cardot, Jean Michel ^a   Peyret, Pierre ^a   Martin, Jean François ^b   Pujos, Estelle ^b   Sébédio, Jean Louis ^b   Brugère, Jean François ^a  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b INRA and University of Auvergne   (France)

Author keywords

3S ECSIM; Fermentation gas; Gut microbiota; HuGChip; In vitro simulation of the colon

Indexed keywords

CARBON DIOXIDE; HYDROGEN;

ADULT; ANAEROBIC FERMENTATION; ARTICLE; BACTERIAL METABOLISM; BACTERIUM; BACTERIUM CULTURE; BACTEROIDACEAE; BIFIDOBACTERIUM; CLOSTRIDIUM; COLON FLORA; CONTINUOUS FLOW REACTOR; CONTROLLED STUDY; CORIOBACTERIACEAE; CYANOBACTERIUM; DESULFOVIBRIONACEAE; DNA FINGERPRINTING; DNA MICROARRAY; ENTEROBACTERIACEAE; FECES ANALYSIS; FEMALE; GAS; HUMAN; IN VITRO STUDY; INOCULATION; INTERMETHOD COMPARISON; INTESTINE FLORA; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MICROBIAL DIVERSITY; MICROBIAL MORPHOLOGY; NONHUMAN; PHYLOGENY; PORPHYROMONODACEAE; PREVOTELLACEAE; PRIORITY JOURNAL; PROPIONIBACTERIACEAE; VALIDATION STUDY;

3S-ECSIM; FERMENTATION GAS; GUT MICROBIOTA; HUGCHIP; IN-VITRO SIMULATION OF THE COLON;

ADULT; ANAEROBIOSIS; BIOREACTORS; BIOTA; CHROMATOGRAPHY, LIQUID; FEMALE; HUMANS; INTESTINE, LARGE; MASS SPECTROMETRY; MICROARRAY ANALYSIS; MICROBIOTA; MODELS, THEORETICAL; VOLUNTEERS;

EID: 84890818028     PISSN: 01677012     EISSN: 18728359     Source Type: Journal    
DOI: 10.1016/j.mimet.2013.11.015     Document Type: Article

References (44)

1. Allison C., McFarlan C., MacFarlane G.T. Studies on mixed populations of human intestinal bacteria grown in single-stage and multistage continuous culture systems. Appl. Environ. Microbiol. 1989, 55:672-678.
2. Arumugam M., Raes J., Pelletier E., Le Paslier D., Yamada T., Mende D.R., Fernandes G.R., Tap J., Bruls T., Batto J.M., Bertalan M., Borruel N., Casellas F., Fernandez L., Gautier L., Hansen T., Hattori M., Hayashi T., Kleerebezem M., Kurokawa K., Leclerc M., Levenez F., Manichanh C., Nielsen H.B., Nielsen T., Pons N., Poulain J., Qin J., Sicheritz-Ponten T., Tims S., Torrents D., Ugarte E., Zoetendal E.G., Wang J., Guarner F., Pedersen O., de Vos W.M., Brunak S., Dore J., Antolin M., Artiguenave F., Blottiere H.M., Almeida M., Brechot C., Cara C., Chervaux C., Cultrone A., Delorme C., Denariaz G., Dervyn R., Foerstner K.U., Friss C., van de Guchte M., Guedon E., Haimet F., Huber W., van Hylckama-Vlieg J., Jamet A., Juste C., Kaci G., Knol J., Lakhdari O., Layec S., Le Roux K., Maguin E., Merieux A., Melo Minardi R., M'Rini C., Muller J., Oozeer R., Parkhill J., Renault P., Rescigno M., Sanchez N., Sunagawa S., Torrejon A., Turner K., Vandemeulebrouck G., Varela E., Winogradsky Y., Zeller G., Weissenbach J., Ehrlich S.D., Bork P. Enterotypes of the human gut microbiome. Nature 2011, 473:174-180.
3. Bearne C.A., Mallett A.K., Rowland I.R., Brennan-Craddock W.E. Continuous culture of human faecal bacteria as an in vitro model for the colonic microflora. Toxicol. in Vitro 1990, 4:522-525.
4. Beerens H. Detection of bifidobacteria by using propionic acid as a selective agent. Appl. Environ. Microbiol. 1991, 57:2418-2419.
5. Benton H.P., Wong D.M., Trauger S.A., Siuzdak G. XCMS2: processing tandem mass spectrometry data for metabolite identification and structural characterization. Anal. Chem. 2008, 80:6382-6389.
6. Brugère J.-F., Mihajlovski A., Missaoui M., Peyret P. Tools for stools: the challenge of assessing human intestinal microbiota using molecular diagnostics. Expert. Rev. Mol. Diagn. 2009, 9:353-365.
7. Brugère, J.-F., Féria-Gervasio, D., Popse, Z., Tottey, W., Alric, M., 2011. The ECSIM Concept (Environmental Control System for Intestinal Microbiota) and Its Derivative Versions to Help Better Understand Human Gut Biology. In: GD Gargiulo, A McEwan (ed) Applied Biomedical Engineering. Chap 4: p 63-82. In: A. M. GD Gargiulo (Ed.), Applied Biomedical Engineering, InTech, Rijeka, pp. Chap 4: p63-82.
8. Cardinale M., Brusetti L., Quatrini P., Borin S., Puglia A.M., Rizzi A., Zanardini E., Sorlini C., Corselli C., Daffonchio D. Comparison of different primer sets for use in automated ribosomal intergenic spacer analysis of complex bacterial communities. Appl. Environ. Microbiol. 2004, 70:6147-6156.
9. Eckburg P.B., Bik E.M., Bernstein C.N., Purdom E., Dethlefsen L., Sargent M., Gill S.R., Nelson K.E., Relman D.A. Diversity of the human intestinal microbial flora. Science 2005, 308:1635-1638.
10. Eeckhaut E., Struijs K., Possemiers S., Vincken J.-P., Keukeleire D.D., Verstraete W. Metabolism of the lignan macromolecule into enterolignans in the gastrointestinal lumen as determined in the simulator of the human intestinal microbial ecosystem. J. Agric. Food Chem. 2008, 56:4806-4812.
11. Feria-Gervasio D., Denis S., Alric M., Brugère J.-F. In vitro maintenance of a human proximal colon microbiota using the continuous fermentation system P-ECSIM. Appl. Microbiol. Biotechnol. 2011, 91:1425-1433.
12. Fraher M.H., O'Toole P.W., Quigley E.M. Techniques used to characterize the gut microbiota: a guide for the clinician. Nat. Rev. Gastroenterol. Hepatol. 2012, 9:312-322.
13. Gibson G.R., Cummings J.H., Macfarlane G.T. Use of a three-stage continuous culture system to study the effect of mucin on dissimilatory sulfate reduction and methanogenesis by mixed populations of human gut bacteria. Appl. Environ. Microbiol. 1988, 54:2750-2755.
14. Goodman A.L., Kallstrom G., Faith J.J., Reyes A., Moore A., Dantas G., Gordon J.I. Extensive personal human gut microbiota culture collections characterized and manipulated in gnotobiotic mice. Proc. Natl. Acad. Sci. 2011, 108:6252-6257.
15. Harper D., Ryan P. PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 2001, 4:1-9.
16. Hubalek Z. Protectants used in the cryopreservation of microorganisms. Cryobiology 2003, 46:205-229.
17. Kanehisa M., Goto S. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 2000, 28:27-30.
18. Kim B.-S., Kim J.N., Cerniglia C.E. In vitro culture conditions for maintaining a complex population of human gastrointestinal tract microbiota. BioMed Res. Int. 2011, (in press). 10.1155/2011/838040.
19. Maccaferri S., Klinder A., Cacciatore S., Chitarrari R., Honda H., Luchinat C., Bertini I., Carnevali P., Gibson G.R., Brigidi P., Costabile A. In vitro fermentation of potential prebiotic flours from natural sources: impact on the human colonic microbiota and metabolome. Mol. Nutr. Food Res. 2012, 56:1342-1352.
20. Macfarlane G.T., Macfarlane S. Models for intestinal fermentation: association between food components, delivery systems, bioavailability and functional interactions in the gut. Curr. Opin. Biotechnol. 2007, 18:156-162.
21. Macfarlane G.T., Gibson G.R., Cummings J.H. Comparison of fermentation reactions in different regions of the human colon. J. Appl. Bacteriol. 1992, 72:57-64.
22. Macfarlane G.T., Macfarlane S., Gibson G.R. Validation of a Three-Stage Compound Continuous Culture System for Investigating the Effect of Retention Time on the Ecology and Metabolism of Bacteria in the Human Colon. Microb. Ecol. 1998, 35:180-187.
23. Macfarlane S., Quigley M., Hopkins M., Newton D.F., Macfarlane G. Polysaccharide degradation by human intestinal bacteria during growth under multi-substrate limiting conditions in a three-stage continuous culture system. FEMS Microbiol. Ecol. 1998, 26:231-243.
24. Macfarlane S., Woodmansey E.J., Macfarlane G.T. Colonization of mucin by human intestinal bacteria and establishment of biofilm communities in a two-stage continuous culture system. Appl. Environ. Microbiol. 2005, 71:7483-7492.
25. McDonald J.A., Schroeter K., Fuentes S., Heikamp-deJong I., Khursigara C.M., de Vos W.M., Allen-Vercoe E. Evaluation of microbial community reproducibility, stability and composition in a human distal gut chemostat model. J. Microbiol. Methods 2013, 95:167-174.
26. Minekus M., Smeets-Peeters M., Bernalier A., Marol-Bonnin S., Havenaar R., Marteau P., Alric M., Fonty G. A computer-controlled system to simulate conditions of the large intestine with peristaltic mixing, water absorption and absorption of fermentation products. Appl. Microbiol. Biotechnol. 1999, 53:108-114.
27. Mitsuoka T., Hayakawa K. The fecal flora in man. I. Composition of the fecal flora of various age groups. Zentralbl. Bakteriol. Orig. A 1973, 223:333-342.
28. Molly K., Woestyne M.V., Verstraete W. Development of a 5-step multi-chamber reactor as a simulation of the human intestinal microbial ecosystem. Appl. Microbiol. Biotechnol. 1993, 39:254-258.
29. Nakamura N., Lin H.C., McSweeney C.S., Mackie R.I., Gaskins H.R. Mechanisms of microbial hydrogen disposal in the human colon and implications for health and disease. Ann. Rev. Food Sci. Technol. 2010, 1:363-395.
30. O'Hara A.M., Shanahan F. The gut flora as a forgotten organ. EMBO Rep. 2006, 7:688-693.
31. Payne A.N., Zihler A., Chassard C., Lacroix C. Advances and perspectives in in vitro human gut fermentation modeling. Trends Biotechnol. 2012, 30:17-25.
32. Qin J., Li R., Raes J., Arumugam M., Burgdorf K.S., Manichanh C., Nielsen T., Pons N., Levenez F., Yamada T., Mende D.R., Li J., Xu J., Li S., Li D., Cao J., Wang B., Liang H., Zheng H., Xie Y., Tap J., Lepage P., Bertalan M., Batto J.M., Hansen T., Le Paslier D., Linneberg A., Nielsen H.B., Pelletier E., Renault P., Sicheritz-Ponten T., Turner K., Zhu H., Yu C., Jian M., Zhou Y., Li Y., Zhang X., Qin N., Yang H., Wang J., Brunak S., Dore J., Guarner F., Kristiansen K., Pedersen O., Parkhill J., Weissenbach J., Bork P., Ehrlich S.D. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010, 464:59-65.
33. Rajilić-Stojanović M., Maathuis A., Heilig H.G., Venema K., de Vos W.M., Smidt H. Evaluating the microbial diversity of an in vitro model of the human large intestine by phylogenetic microarray analysis. Microbiology 2010, 156:3270-3281.
34. Samuel B.S., Gordon J.I. A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. Proc. Natl. Acad. Sci. 2006, 103:10011-10016.
35. Smith C.A., Want E.J., O'Maille G., Abagyan R., Siuzdak G. XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal. Chem. 2006, 78:779-787.
36. Stearns J.C., Lynch M.D., Senadheera D.B., Tenenbaum H.C., Goldberg M.B., Cvitkovitch D.G., Croitoru K., Moreno-Hagelsieb G., Neufeld J.D. Bacterial biogeography of the human digestive tract. Sci. Rep. 2011, 1.
37. Tap J., Mondot S., Levenez F., Pelletier E., Caron C., Furet J.P., Ugarte E., Munoz-Tamayo R., Paslier D.L., Nalin R., Dore J., Leclerc M. Towards the human intestinal microbiota phylogenetic core. Environ. Microbiol. 2009, 11:2574-2584.
38. Tottey W., Denonfoux J., Jaziri F., Parisot N., Missaoui M., Hill D., Borrel G., Peyretaillade E., Alric M., Harris H.M., Jeffery I.B., Claesson M.J., O'Toole P.W., Peyret P., Brugere J.F. The human gut chip "HuGChip", an explorative phylogenetic microarray for determining gut microbiome diversity at family level. PLoS One 2013, 8:e62544.
39. Turnbaugh P.J., Ridaura V.K., Faith J.J., Rey F.E., Knight R., Gordon J.I. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med. 2009, 1:6ra14.
40. Tzortzis G., Goulas A.K., Gee J.M., Gibson G.R. A novel galactooligosaccharide mixture increases the bifidobacterial population numbers in a continuous in vitro fermentation system and in the proximal colonic contents of pigs in vivo. J. Nutr. 2005, 135:1726-1731.
41. Van den Abbeele P., Grootaert C., Marzorati M., Possemiers S., Verstraete W., Gérard P., Rabot S., Bruneau A., El Aidy S., Derrien M. Microbial community development in a dynamic gut model is reproducible, colon region specific, and selective for Bacteroidetes and Clostridium cluster IX. Appl. Environ. Microbiol. 2010, 76:5237-5246.
42. Van den Abbeele P., Roos S., Eeckhaut V., MacKenzie D.A., Derde M., Verstraete W., Marzorati M., Possemiers S., Vanhoecke B., Van Immerseel F. Incorporating a mucosal environment in a dynamic gut model results in a more representative colonization by lactobacilli. Microb. Biotechnol. 2012, 5:106-115.
43. Wishart D.S., Tzur D., Knox C., Eisner R., Guo A.C., Young N., Cheng D., Jewell K., Arndt D., Sawhney S., Fung C., Nikolai L., Lewis M., Coutouly M.A., Forsythe I., Tang P., Shrivastava S., Jeroncic K., Stothard P., Amegbey G., Block D., Hau D.D., Wagner J., Miniaci J., Clements M., Gebremedhin M., Guo N., Zhang Y., Duggan G.E., Macinnis G.D., Weljie A.M., Dowlatabadi R., Bamforth F., Clive D., Greiner R., Li L., Marrie T., Sykes B.D., Vogel H.J., Querengesser L. HMDB: the Human Metabolome Database. Nucleic Acids Res. 2007, 35:D521-D526.
44. Yu Z., Morrison M. Improved extraction of PCR-quality community DNA from digesta and fecal samples. Biotechniques 2004, 36:808-812.