The Mini Colon Model: a benchtop multi-bioreactor system to investigate the gut microbiome

References

• Fan Y, Pedersen O. Gut microbiota in human metabolic health and disease. Nat Rev Microbiol. 2021;19(1):55–14. doi:10.1038/s41579-020-0433-9.
   PubMed Web of Science ®Google Scholar
• Maruvada P, Leone V, Kaplan LM, Chang EB. The human microbiome and obesity: moving beyond associations. Cell Host Microbe. 2017;22(5):589–599. doi:10.1016/j.chom.2017.10.005.
   PubMed Web of Science ®Google Scholar
• Caporaso JG, Lauber CL, Costello EK, Berg-Lyons D, Gonzalez A, Stombaugh J, Knights D, Gajer P, Ravel J, Fierer N, et al. Moving pictures of the human microbiome. Genome Biol. 2011;12(5):R50. doi:10.1186/gb-2011-12-5-r50.
   PubMed Web of Science ®Google Scholar
• Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA. Diversity of the human intestinal microbial flora. Science. 2005;308(5728):1635–1638. doi:10.1126/science.1110591.
   PubMed Web of Science ®Google Scholar
• Schloig S, Arumugam M, Sunagawa S, Mitreva M, Tap J, Zhu A, Waller A, Mende DR, Kultima JR, Martin J. Genomic variation landscape of the human gut microbiome. Nature. 2013;493(7430):45–50. doi:10.1038/nature11711.
   PubMed Web of Science ®Google Scholar
• Arrieta M-C, Walter J, Finlay BB. Human microbiota-associated mice: a model with challenges. Cell Host Microbe. 2016;19(5):575–578. doi:10.1016/j.chom.2016.04.014.
   PubMed Web of Science ®Google Scholar
• Reardon S. A mouse’s house may ruin experiments. Nature. 2016;530(7590):264. doi:10.1038/nature.2016.19335.
   PubMed Web of Science ®Google Scholar
• Walter J, Armet AM, Finlay BB, Shanahan F. Establishing or exaggerating causality for the gut microbiome: lessons from human microbiota-associated rodents. Cell. 2020;180(2):221–232. doi:10.1016/j.cell.2019.12.025.
   PubMed Web of Science ®Google Scholar
• Guzman-Rodriguez M, McDonald JAK, Hyde R, Allen-Vercoe E, Claud EC, Sheth PM, Petrof EO. Using bioreactors to study the effects of drugs on the human microbiota. Methods. 2018;149:31–41. doi:10.1016/j.ymeth.2018.08.003.
   PubMed Web of Science ®Google Scholar
• García-Villalba R, Vissenaekens H, Pitart J, Romo-Vaquero M, Espín JC, Grootaert C, Selma MV, Raes K, Smagghe G, Possemiers S. Gastrointestinal simulation model TWIN-SHIME shows differences between human urolithin-metabotypes in gut microbiota composition, pomegranate polyphenol metabolism, and transport along the intestinal tract. J Agric Food Chem. 2017;65(27):5480–5493. doi:10.1021/acs.jafc.7b02049.
   PubMed Web of Science ®Google Scholar
• Minekus M, Smeets-Peeters M, Bernalier A, Marol-Bonnin S, Havenaar R, Marteau P, Alric M, Fonty G, Huis In’t Veld JHJ. 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(1):108–114. doi:10.1007/s002530051622.
   PubMed Web of Science ®Google Scholar
• Minekus M, Marteau P, Havenaar R, Veld JH. A multicompartmental dynamic computer-controlled model simulating the stomach and small intestine. Altern Lab Anim. 1995;23(2):197–209. doi:10.1177/026119299502300205.
   Web of Science ®Google Scholar
• McDonald JAK, Schroeter K, Fuentes S, Heikamp-deJong I, Khursigara CM, de Vos WM, Allen-Vercoe E. Evaluation of microbial community reproducibility, stability and composition in a human distal gut chemostat model. J Microbiol Methods. 2013;95(2):167–174. doi:10.1016/j.mimet.2013.08.008.
   PubMed Web of Science ®Google Scholar
• Venema K, van den Abbeele P. Experimental models of the gut microbiome. Best Pract Res Clin Gastroenterol. 2013;27(1):115–126. doi:10.1016/j.bpg.2013.03.002.
   PubMed Web of Science ®Google Scholar
• Auchtung JM, Robinson CD, Britton RA. Cultivation of stable, reproducible microbial communities from different fecal donors using minibioreactor arrays (MBRAs). Microbiome. 2015;3:42.
   PubMed Web of Science ®Google Scholar
• Robinson CD, Auchtung JM, Collins J, Britton RA. Epidemic Clostridium difficile strains demonstrate increased competitive fitness compared to nonepidemic isolates. Infect Immun. 2014;82(7):2815–2825. doi:10.1128/IAI.01524-14.
   PubMed Web of Science ®Google Scholar
• Li L, Abou-Samra E, Ning Z, Zhang X, Mayne J, Wang J, Cheng K, Walker K, Stintzi A, Figeys D. An in vitro model maintaining taxon-specific functional activities of the gut microbiome. Nat Commun. 2019;10(1):4146. doi:10.1038/s41467-019-12087-8.
   PubMed Web of Science ®Google Scholar
• Naimi S, Viennois E, Gewirtz AT, Chassaing B. Direct impact of commonly used dietary emulsifiers on human gut microbiota. Microbiome. 2021;9(1):66. doi:10.1186/s40168-020-00996-6.
   PubMed Web of Science ®Google Scholar
• Chen Y-J, Wu H, Wu S-D, Lu N, Wang Y-T, Liu H-N, Dong L, Liu -T-T, Shen X-Z. Parasutterella, in association with irritable bowel syndrome and intestinal chronic inflammation. J Gastroenterol Hepatol. 2018;33(11):1844–1852. doi:10.1111/jgh.14281.
   PubMed Web of Science ®Google Scholar
• Petursdottir DH, Nordlander S, Qazi KR, Carvalho-Queiroz C, Ahmed Osman O, Hell E, Björkander S, Haileselassie Y, Navis M, Kokkinou E. Early-life human microbiota associated with childhood allergy promotes the T Helper 17 axis in mice. Front Immunol. 2017;8:1699. doi:10.3389/fimmu.2017.01699.
   PubMed Web of Science ®Google Scholar
• Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 2001;26:32–46.
   Web of Science ®Google Scholar
• Wexler HM. Bacteroides: the good, the bad, and the nitty-gritty. Clin Microbiol Rev. 2007;20(4):593–621. doi:10.1128/CMR.00008-07.
   PubMed Web of Science ®Google Scholar
• Jennings A, Koch M, Bang C, Franke A, Lieb W, Cassidy A. Microbial diversity and abundance of parabacteroides mediate the associations between higher intake of flavonoid-rich foods and lower blood pressure. Hypertension. 2021;78(4):1016–1026. doi:10.1161/HYPERTENSIONAHA.121.17441.
   PubMed Web of Science ®Google Scholar
• Lopez-Siles M, Duncan SH, Garcia-Gil LJ, Martinez-Medina M. Faecalibacterium prausnitzii: from microbiology to diagnostics and prognostics. ISME J. 2017;11(4):841–852. doi:10.1038/ismej.2016.176.
   PubMed Web of Science ®Google Scholar
• Binda C, Lopetuso LR, Rizzatti G, Gibiino G, Cennamo V, Gasbarrini A. Actinobacteria: a relevant minority for the maintenance of gut homeostasis. Dig Liver Dis. 2018;50(5):421–428. doi:10.1016/j.dld.2018.02.012.
   PubMedGoogle Scholar
• Wahlgren M, Axenstrand M, Håkansson Å, Marefati A, Lomstein Pedersen B. In vitro methods to study colon release: state of the art and an outlook on new strategies for better in-vitro biorelevant release media. Pharmaceutics. 2019;11(2):95. doi:10.3390/pharmaceutics11020095.
   PubMed Web of Science ®Google Scholar
• Jalili-Firoozinezhad S, Gazzaniga FS, Calamari EL, Camacho DM, Fadel CW, Bein A, Swenor B, Nestor B, Cronce MJ, Tovaglieri A. A complex human gut microbiome cultured in an anaerobic intestine-on-a-chip. Nat Biomed Eng. 2019;3(7):520–531. doi:10.1038/s41551-019-0397-0.
   PubMed Web of Science ®Google Scholar
• O’Donnell MM, Rea MC, Shanahan F, Ross RP. The use of a mini-bioreactor fermentation system as a reproducible, high-throughput ex vivo batch model of the distal colon. Front Microbiol. 2018;9:1844.
   PubMed Web of Science ®Google Scholar
• Schloss PD, Schubert AM, Zackular JP, Iverson KD, Young VB, Petrosino JF. Stabilization of the murine gut microbiome following weaning. Gut Microbes. 2012;3(4):383–393. doi:10.4161/gmic.21008.
   PubMed Web of Science ®Google Scholar
• Johnson JS, Spakowicz DJ, Hong B-Y, Petersen LM, Demkowicz P, Chen L, Leopold SR, Hanson BM, Agresta HO, Gerstein M. Evaluation of 16S rRNA gene sequencing for species and strain-level microbiome analysis. Nat Commun. 2019;10(1):5029. doi:10.1038/s41467-019-13036-1.
   PubMed Web of Science ®Google Scholar
• Kuczynski J, Lauber CL, Walters WA, Parfrey LW, Clemente JC, Gevers D, Knight R. Experimental and analytical tools for studying the human microbiome. Nat Rev Genet. 2011;13(1):47–58. doi:10.1038/nrg3129.
   PubMed Web of Science ®Google Scholar
• Duncan SH, Hold GL, Harmsen HJM, Stewart CS, Flint HJ. Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as Faecalibacterium prausnitzii gen. nov., comb. nov. Int J Syst Evol Microbiol. 2002;52(Pt 6):2141–2146. doi:10.1099/00207713-52-6-2141.
   PubMedGoogle Scholar
• Bradley PH, Pollard KS. Proteobacteria explain significant functional variability in the human gut microbiome. Microbiome. 2017;5(1):36. doi:10.1186/s40168-017-0244-z.
   PubMedGoogle Scholar
• Rizzatti G, Lopetuso LR, Gibiino G, Binda C, Gasbarrini A. Proteobacteria: a common factor in human diseases. Biomed Res Int. 2017;2017:e9351507. doi:10.1155/2017/9351507.
   PubMed Web of Science ®Google Scholar
• Kumar P, Libchaber A. Pressure and temperature dependence of growth and morphology of Escherichia coli: experiments and stochastic model. Biophys J. 2013;105(3):783–793. doi:10.1016/j.bpj.2013.06.029.
   PubMed Web of Science ®Google Scholar
• Renouf M, Hendrich S. Bacteroides uniformis is a putative bacterial species associated with the degradation of the Isoflavone Genistein in human feces. J Nutr. 2011;141(6):1120–1126. doi:10.3945/jn.111.140988.
   PubMed Web of Science ®Google Scholar
• Taketani M, Zhang J, Zhang S, Triassi AJ, Huang Y-J, Griffith LG, Voigt CA. Genetic circuit design automation for the gut resident species Bacteroides thetaiotaomicron. Nat Biotechnol. 2020;38(8):962–969. doi:10.1038/s41587-020-0468-5.
   PubMed Web of Science ®Google Scholar
• Nugent SG, Kumar D, Rampton DS, Evans DF. Intestinal luminal pH in inflammatory bowel disease: possible determinants and implications for therapy with aminosalicylates and other drugs. Gut. 2001;48(4):571–577. doi:10.1136/gut.48.4.571.
   PubMed Web of Science ®Google Scholar
• Bertoni S, Liu Z, Correia A, Martins JP, Rahikkala A, Fontana F, Kemell M, Liu D, Albertini B, Passerini N. pH and reactive oxygen species-sequential responsive nano-in-micro composite for targeted therapy of inflammatory bowel disease. Adv Funct Mater. 2018;28(50):1806175. doi:10.1002/adfm.201806175.
   Web of Science ®Google Scholar
• Liu L, Firrman J, Tanes C, Bittinger K, Thomas-Gahring A, Wu GD, Van den Abbeele P, Tomasula PM. Establishing a mucosal gut microbial community in vitro using an artificial simulator. PLOS ONE. 2018;13(7):e0197692. doi:10.1371/journal.pone.0197692.
   PubMed Web of Science ®Google Scholar
• Javdan B, Lopez JG, Chankhamjon P, Lee YCJ, Hull R, Wu Q, Wang X, Chatterjee S, Donia MS. Personalized mapping of drug metabolism by the human gut microbiome. Cell. 2020;181(7):1661–1679.e22. doi:10.1016/j.cell.2020.05.001.
   PubMed Web of Science ®Google Scholar
• Junker B. Foam and its mitigation in fermentation systems. Biotechnol Prog. 2007;23(4):767–784. doi:10.1002/bp070032r.
   PubMed Web of Science ®Google Scholar
• Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol. 2016;18(5):1403–1414. doi:10.1111/1462-2920.13023.
   PubMed Web of Science ®Google Scholar
• Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37(8):852–857. doi:10.1038/s41587-019-0209-9.
   PubMed Web of Science ®Google Scholar
• Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. PNAS. 2011;108(supplement_1):4516–4522. doi:10.1073/pnas.1000080107.
   PubMed Web of Science ®Google Scholar
• Glöckner FO, Yilmaz P, Quast C, Gerken J, Beccati A, Ciuprina A, Bruns G, Yarza P, Peplies J, Westram R. 25 years of serving the community with ribosomal RNA gene reference databases and tools. J Biotechnol. 2017;261:169–176. doi:10.1016/j.jbiotec.2017.06.1198.
   PubMed Web of Science ®Google Scholar
• Werner JJ, Knights D, Garcia ML, Scalfone NB, Smith S, Yarasheski K, Cummings TA, Beers AR, Knight R, and Angenent LT, et al. Bacterial community structures are unique and resilient in full-scale bioenergy systems. PNAS. 2011;108(10):4158–4163. doi:10.1073/pnas.1015676108.
   PubMed Web of Science ®Google Scholar
• Kalsi S, Mingels R, Lu S, Cheong Y, Morgan H. Metal oxide sensors for long term pH monitoring. NanoBioTech Montreux Conference. 2018:2. https://eprints.soton.ac.uk/427026/
   Google Scholar