Microbiology (medical); Microbiology; intestinal microbiota; human colon; batch fermentation; gut microbes; mucosa
Abstract :
[en] Gastrointestinal simulations in vitro have only limited approaches to analyze the microbial communities inhabiting the mucosal compartment. Understanding and differentiating gut microbial ecosystems is crucial for a more comprehensive and accurate representation of the gut microbiome and its interactions with the host. Herein is suggested, in a short-term and static set-up (named “M-batches”), the analysis of mucosal and luminal populations of inhabitants of the human colon. After varying several parameters, such as the fermentation volume and the fecal inoculum (single or pool), only minor differences in microbial composition and metabolic production were identified. However, the pool created with feces from five donors and cultivated in a smaller volume (300 mL) seemed to provide a more stable luminal ecosystem. The study of commercially available coffee and green tea in the M-batches suggested some positive effects of these worldwide known beverages, including the increase in butyrate-producing bacteria and lactobacilli populations. We hope that this novel strategy can contribute to future advances in the study of intestinal ecosystems and host-microbe relationships and help elucidate roles of the microbiome in health and disease.
Goya-Jorge, Elizabeth ✱; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Santé publique vétérinaire ; Intestinal Regenerative Medicine Laboratory, Department of Clinical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, NC 27606, USA
Gonza Quito, Irma Elizabeth ✱; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH)
Douny, Caroline ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Analyse des denrées alimentaires
Scippo, Marie-Louise ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Analyse des denrées alimentaires
Delcenserie, Véronique ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Gestion de la qualité dans la chaîne alimentaire
✱ These authors have contributed equally to this work.
Language :
English
Title :
M-Batches to Simulate Luminal and Mucosal Human Gut Microbial Ecosystems: A Case Study of the Effects of Coffee and Green Tea
Original title :
[en] M-Batches to Simulate Luminal and Mucosal Human Gut Microbial Ecosystems: A Case Study of the Effects of Coffee and Green Tea
Roupar D. Berni P. Martins J.T. Caetano A.C. Teixeira J.A. Nobre C. Bioengineering Approaches to Simulate Human Colon Microbiome Ecosystem Trends Food Sci. Technol. 2021 112 808 822 10.1016/j.tifs.2021.04.035
Veintimilla-Gozalbo E. Asensio-Grau A. Calvo-Lerma J. Heredia A. Andrés A. In Vitro Simulation of Human Colonic Fermentation: A Practical Approach towards Models’ Design and Analytical Tools Appl. Sci. 2021 11 8135 10.3390/app11178135
Biagini F. Daddi C. Calvigioni M. De Maria C. Zhang Y.S. Ghelardi E. Vozzi G. Designs and Methodologies to Recreate in Vitro Human Gut Microbiota Models Biodes Manuf. 2023 6 298 318 10.1007/s42242-022-00210-6
Isenring J. Bircher L. Geirnaert A. Lacroix C. In Vitro Human Gut Microbiota Fermentation Models: Opportunities, Challenges, and Pitfalls Microbiome Res. Rep. 2023 2 2 10.20517/mrr.2022.15 38045607
Pérez-Burillo S. Molino S. Navajas-Porras B. Valverde-Moya Á.J. Hinojosa-Nogueira D. López-Maldonado A. Pastoriza S. Rufián-Henares J.Á. An in Vitro Batch Fermentation Protocol for Studying the Contribution of Food to Gut Microbiota Composition and Functionality Nat. Protoc. 2021 16 3186 3209 10.1038/s41596-021-00537-x 34089022
Goya-Jorge E. Bondue P. Gonza I. Laforêt F. Antoine C. Boutaleb S. Douny C. Scippo M.-L. de Ribaucourt J.C. Crahay F. et al. Butyrogenic, Bifidogenic and Slight Anti-Inflammatory Effects of a Green Kiwifruit Powder (Kiwi FFG®) in a Human Gastrointestinal Model Simulating Mild Constipation Food Res. Int. 2023 173 113348 10.1016/j.foodres.2023.113348 37803696
Singh V. Son H. Lee G. Lee S. Unno T. Shin J.-H. Role, Relevance, and Possibilities of in Vitro Fermentation Models in Human Dietary, and Gut-Microbial Studies Biotechnol. Bioeng. 2022 119 3044 3061 10.1002/bit.28206
Song C. Chai Z. Chen S. Zhang H. Zhang X. Zhou Y. Intestinal Mucus Components and Secretion Mechanisms: What We Do and Do Not Know Exp. Mol. Med. 2023 55 681 691 10.1038/s12276-023-00960-y
Luis A.S. Hansson G.C. Intestinal Mucus and Their Glycans: A Habitat for Thriving Microbiota Cell Host Microbe 2023 31 1087 1100 10.1016/j.chom.2023.05.026
Tailford L.E. Crost E.H. Kavanaugh D. Juge N. Mucin Glycan Foraging in the Human Gut Microbiome Front. Genet. 2015 6 81 10.3389/fgene.2015.00081
Glover J.S. Ticer T.D. Engevik M.A. Characterizing the Mucin-Degrading Capacity of the Human Gut Microbiota Sci. Rep. 2022 12 8456 10.1038/s41598-022-11819-z 35589783
Pan M. Barua N. Ip M. Mucin-Degrading Gut Commensals Isolated from Healthy Faecal Donor Suppress Intestinal Epithelial Inflammation and Regulate Tight Junction Barrier Function Front. Immunol. 2022 13 1021094 10.3389/fimmu.2022.1021094 36311778
Van Herreweghen F. De Paepe K. Roume H. Kerckhof F.-M. Van de Wiele T. Mucin Degradation Niche as a Driver of Microbiome Composition and Akkermansia Muciniphila Abundance in a Dynamic Gut Model Is Donor Independent FEMS Microbiol. Ecol. 2018 94 fiy186 10.1093/femsec/fiy186 30239657
Vaga S. Lee S. Ji B. Andreasson A. Talley N.J. Agréus L. Bidkhori G. Kovatcheva-Datchary P. Park J. Lee D. et al. Compositional and Functional Differences of the Mucosal Microbiota along the Intestine of Healthy Individuals Sci. Rep. 2020 10 14977 10.1038/s41598-020-71939-2 32917913
Van den Abbeele P. Roos S. Eeckhaut V. MacKenzie D.A. Derde M. Verstraete W. Marzorati M. Possemiers S. Vanhoecke B. Van Immerseel F. et al. Incorporating a Mucosal Environment in a Dynamic Gut Model Results in a More Representative Colonization by Lactobacilli Microb. Biotechnol. 2012 5 106 115 10.1111/j.1751-7915.2011.00308.x 21989255
Tran T.H.T. Boudry C. Everaert N. Théwis A. Portetelle D. Daube G. Nezer C. Taminiau B. Bindelle J. Adding Mucins to an in Vitro Batch Fermentation Model of the Large Intestine Induces Changes in Microbial Population Isolated from Porcine Feces Depending on the Substrate FEMS Microbiol. Ecol. 2016 92 fiv165 10.1093/femsec/fiv165 26691596
Douny C. Dufourny S. Brose F. Verachtert P. Rondia P. Lebrun S. Marzorati M. Everaert N. Delcenserie V. Scippo M.-L. Development of an Analytical Method to Detect Short-Chain Fatty Acids by SPME-GC-MS in Samples Coming from an in Vitro Gastrointestinal Model J. Chromatogr. B 2019 1124 188 196 10.1016/j.jchromb.2019.06.013
Goya-Jorge E. Gonza I. Bondue P. Douny C. Taminiau B. Daube G. Scippo M.-L. Delcenserie V. Human Adult Microbiota in a Static Colon Model: AhR Transcriptional Activity at the Crossroads of Host-Microbe Interaction Foods 2022 11 1946 10.3390/foods11131946
Douny C. Benmedjadi S. Brose F. Afé O.H.I. Igout A. Hounhouigan D.J. Anihouvi V.B. Scippo M.-L. Development of an Analytical Method for the Simultaneous Measurement of 10 Biogenic Amines in Meat: Application to Beninese Grilled Pork Samples Food Anal. Methods 2019 12 2392 2400 10.1007/s12161-019-01587-4
Livak K.J. Schmittgen T.D. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 2001 25 402 408 10.1006/meth.2001.1262
Van den Abbeele P. Belzer C. Goossens M. Kleerebezem M. De Vos W.M. Thas O. De Weirdt R. Kerckhof F.-M. Van de Wiele T. Butyrate-Producing Clostridium Cluster XIVa Species Specifically Colonize Mucins in an in Vitro Gut Model ISME J. 2013 7 949 961 10.1038/ismej.2012.158 23235287
Goya-Jorge E. Gonza I. Bondue P. Druart G. Al-Chihab M. Boutaleb S. Douny C. Scippo M.-L. Thonart P. Delcenserie V. Evaluation of Four Multispecies Probiotic Cocktails in a Human Colonic Fermentation Model Probiotics Antimicrob. Proteins 2023 15 10.1007/s12602-023-10162-7 37725305
Firrman J. Liu L. Mahalak K. Tanes C. Bittinger K. Tu V. Bobokalonov J. Mattei L. Zhang H. Van den Abbeele P. The Impact of Environmental PH on the Gut Microbiota Community Structure and Short Chain Fatty Acid Production FEMS Microbiol. Ecol. 2022 98 fiac038 10.1093/femsec/fiac038 35383853
Ghyselinck J. Verstrepen L. Moens F. Van den Abbeele P. Said J. Smith B. Bjarnason I. Basit A.W. Gaisford S. A 4-Strain Probiotic Supplement Influences Gut Microbiota Composition and Gut Wall Function in Patients with Ulcerative Colitis Int. J. Pharm. 2020 587 119648 10.1016/j.ijpharm.2020.119648 32679260
Aguirre M. Eck A. Koenen M.E. Savelkoul P.H.M. Budding A.E. Venema K. Evaluation of an Optimal Preparation of Human Standardized Fecal Inocula for in Vitro Fermentation Studies J. Microbiol. Methods 2015 117 78 84 10.1016/j.mimet.2015.07.019
Aguirre M. Ramiro-Garcia J. Koenen M.E. Venema K. To Pool or Not to Pool? Impact of the Use of Individual and Pooled Fecal Samples for in Vitro Fermentation Studies J. Microbiol. Methods 2014 107 1 7 10.1016/j.mimet.2014.08.022
Chen J. Tang H. Zhang M. Sang S. Jia L. Ou C. Exploration of the Roles of Microbiota on Biogenic Amines Formation during Traditional Fermentation of Scomber Japonicus Front. Microbiol. 2022 13 1030789 10.3389/fmicb.2022.1030789
Pérez-Burillo S. Mehta T. Esteban-Muñoz A. Pastoriza S. Paliy O. Ángel Rufián-Henares J. Effect of in Vitro Digestion-Fermentation on Green and Roasted Coffee Bioactivity: The Role of the Gut Microbiota Food Chem. 2019 279 252 259 10.1016/j.foodchem.2018.11.137
Preda M. Popa M.I. Mihai M.M. Oţelea T.C. Holban A.M. Effects of Coffee on Intestinal Microbiota, Immunity, and Disease Caffeinated and Cocoa Based Beverages Grumezescu A.M. Holban A.M. Woodhead Publishing Sawston, UK 2019 391 421 978-0-12-815864-7
González S. Salazar N. Ruiz-Saavedra S. Gómez-Martín M. de Los Reyes-Gavilán C.G. Gueimonde M. Long-Term Coffee Consumption Is Associated with Fecal Microbial Composition in Humans Nutrients 2020 12 1287 10.3390/nu12051287
Wu Z. Huang S. Li T. Li N. Han D. Zhang B. Xu Z.Z. Zhang S. Pang J. Wang S. et al. Gut Microbiota from Green Tea Polyphenol-Dosed Mice Improves Intestinal Epithelial Homeostasis and Ameliorates Experimental Colitis Microbiome 2021 9 184 10.1186/s40168-021-01115-9
Pérez-Burillo S. Navajas-Porras B. López-Maldonado A. Hinojosa-Nogueira D. Pastoriza S. Rufián-Henares J.Á. Green Tea and Its Relation to Human Gut Microbiome Molecules 2021 26 3907 10.3390/molecules26133907 34206736
Chapkin R.S. Davidson L.A. Park H. Jin U.-H. Fan Y.-Y. Cheng Y. Hensel M.E. Landrock K.K. Allred C. Menon R. et al. Role of the Aryl Hydrocarbon Receptor (AhR) in Mediating the Effects of Coffee in the Colon Mol. Nutr. Food Res. 2021 65 e2100539 10.1002/mnfr.202100539
Palermo C.M. Hernando J.I.M. Dertinger S.D. Kende A.S. Gasiewicz T.A. Identification of Potential Aryl Hydrocarbon Receptor Antagonists in Green Tea Chem. Res. Toxicol. 2003 16 865 872 10.1021/tx025672c 12870889
Williams S.N. Shih H. Guenette D.K. Brackney W. Denison M.S. Pickwell G.V. Quattrochi L.C. Comparative Studies on the Effects of Green Tea Extracts and Individual Tea Catechins on Human CYP1A Gene Expression Chem. Biol. Interact. 2000 128 211 229 10.1016/S0009-2797(00)00204-0 11064004
Stockinger B. Shah K. Wincent E. AHR in the Intestinal Microenvironment: Safeguarding Barrier Function Nat. Rev. Gastroenterol. Hepatol. 2021 18 559 570 10.1038/s41575-021-00430-8
Lamas B. Natividad J.M. Sokol H. Aryl Hydrocarbon Receptor and Intestinal Immunity Mucosal Immunol. 2018 11 1024 1038 10.1038/s41385-018-0019-2
Agus A. Planchais J. Sokol H. Gut Microbiota Regulation of Tryptophan Metabolism in Health and Disease Cell Host Microbe 2018 23 716 724 10.1016/j.chom.2018.05.003
Bacchetti De Gregoris T. Aldred N. Clare A.S. Burgess J.G. Improvement of Phylum- and Class-Specific Primers for Real-Time PCR Quantification of Bacterial Taxa J. Microbiol. Methods 2011 86 351 356 10.1016/j.mimet.2011.06.010
Matsuki T. Watanabe K. Fujimoto J. Takada T. Tanaka R. Use of 16S RRNA Gene-Targeted Group-Specific Primers for Real-Time PCR Analysis of Predominant Bacteria in Human Feces Appl. Environ. Microbiol. 2004 70 7220 7228 10.1128/AEM.70.12.7220-7228.2004
Ramirez-Farias C. Slezak K. Fuller Z. Duncan A. Holtrop G. Louis P. Effect of Inulin on the Human Gut Microbiota: Stimulation of Bifidobacterium Adolescentis and Faecalibacterium Prausnitzii Br. J. Nutr. 2009 101 541 550 10.1017/S0007114508019880
Morel F.B. Oozeer R. Piloquet H. Moyon T. Pagniez A. Knol J. Darmaun D. Michel C. Preweaning Modulation of Intestinal Microbiota by Oligosaccharides or Amoxicillin Can Contribute to Programming of Adult Microbiota in Rats Nutrition 2015 31 515 522 10.1016/j.nut.2014.09.011
Amit-Romach E. Sklan D. Uni Z. Microflora Ecology of the Chicken Intestine Using 16S Ribosomal DNA Primers Poult. Sci. 2004 83 1093 1098 10.1093/ps/83.7.1093
Rinttilä T. Kassinen A. Malinen E. Krogius L. Palva A. Development of an Extensive Set of 16S RDNA-Targeted Primers for Quantification of Pathogenic and Indigenous Bacteria in Faecal Samples by Real-Time PCR J. Appl. Microbiol. 2004 97 1166 1177 10.1111/j.1365-2672.2004.02409.x
Everard A. Belzer C. Geurts L. Ouwerkerk J.P. Druart C. Bindels L.B. Guiot Y. Derrien M. Muccioli G.G. Delzenne N.M. et al. Cross-Talk between Akkermansia Muciniphila and Intestinal Epithelium Controls Diet-Induced Obesity Proc. Nat. Acad. Sci. USA 2013 110 9066 9071 10.1073/pnas.1219451110
Wang R.F. Cao W.W. Cerniglia C.E. PCR Detection and Quantitation of Predominant Anaerobic Bacteria in Human and Animal Fecal Samples Appl. Environ. Microbiol. 1996 62 1242 1247 10.1128/aem.62.4.1242-1247.1996
Wu F. Guo X. Zhang J. Zhang M. Ou Z. Peng Y. Phascolarctobacterium Faecium Abundant Colonization in Human Gastrointestinal Tract Exp. Ther. Med. 2017 14 3122 3126 10.3892/etm.2017.4878
Lyra A. Krogius-Kurikka L. Nikkilä J. Malinen E. Kajander K. Kurikka K. Korpela R. Palva A. Effect of a Multispecies Probiotic Supplement on Quantity of Irritable Bowel Syndrome-Related Intestinal Microbial Phylotypes BMC Gastroenterol. 2010 10 110 10.1186/1471-230X-10-110