Lactobacillus plantarum IFPL935 impacts colonic metabolism in a simulator of the human gut microbiota during feeding with red wine polyphenols

详细信息    查看全文

• 作者：E. Barroso (1)
  T. Van de Wiele (2)
  A. Jiménez-Girón (1)
  I. Mu?oz-González (1)
  P. J. Martín-Alvarez (1)
  M. V. Moreno-Arribas (1)
  B. Bartolomé (1)
  C. Peláez (1)
  M. C. Martínez-Cuesta (1)
  T. Requena (1)
  
• 关键词：Lactobacillus ; Polyphenol ; Colonic metabolism ; Probiotic ; Intestinal microbiota
• 刊名：Applied Microbiology and Biotechnology
• 出版年：2014
• 出版时间：August 2014
• 年：2014
• 卷：98
• 期：15
• 页码：6805-6815
• 全文大小：381 KB
• 参考文献：1. Arranz S, Chiva-Blanch G, Valderas-Martínez P, Medina-Remón A, Lamuela-Raventós RM, Estruch R (2012) Wine, beer, alcohol and polyphenols on cardiovascular disease and cancer. Nutrients 4:759-81 CrossRef
  2. Barroso E, Sánchez-Patán F, Martín-Alvarez PJ, Bartolomé B, Moreno-Arribas MV, Peláez C, Requena T, Van de Wiele T, Martínez-Cuesta MC (2013) / Lactobacillus plantarum IFPL935 favors the initial metabolism of red wine polyphenols when added to a colonic microbiota. J Agric Food Chem 61:10163-0172 CrossRef
  3. Bodas R, Prieto N, García-González R, Andrés S, Giráldez FJ, Lopez S (2012) Manipulation of rumen fermentation and methane production with plant secondary metabolites. Anim Feed Sci Technol 176:78-3 CrossRef
  4. Bolca S, Van de Wiele T, Possemiers S (2013) Gut metabotypes govern health effects of dietary polyphenols. Curr Opin Biotechnol 24:220-25 CrossRef
  5. Bremner JM, Keeney RD (1965) Steam distillation methods for determination of ammonium, nitrate and nitrite. Anal Chim Acta 32:485-95 CrossRef
  6. Busquet M, Calsamiglia S, Ferret A, Kamel C (2005) Screening for effects of plant extracts and active compounds of plants on dairy cattle rumen microbial fermentation in a continuous culture system. Anim Feed Sci Technol 124:597-13 CrossRef
  7. Cueva C, Sánchez-Patán F, Monagas M, Walton GE, Gibson GR, Martín-álvarez PJ, Bartolomé B, Moreno-Arribas MV (2013) In vitro fermentation of grape seed flavan-3-ol fractions by human faecal microbiota: changes in microbial groups and phenolic metabolites. FEMS Microbiol Ecol 83:792-05 CrossRef
  8. Daglia M (2012) Polyphenols as antimicrobial agents. Curr Opin Biotechnol 23:174-81 CrossRef
  9. De Boever P, Deplancke B, Verstraete W (2000) Fermentation by gut microbiota cultured in a Simulator of the Human Intestinal Microbial Ecosystem is improved by supplementing a soygerm powder. J Nutr 130:2599-606
  10. Dolara P, Luceri C, De FC, Femia AP, Giovannelli L, Caderni G, Cecchini C, Silvi S, Orpianesi C, Cresci A (2005) Red wine polyphenols influence carcinogenesis, intestinal microflora, oxidative damage and gene expression profiles of colonic mucosa in F344 rats. Mutat Res 591:237-46 CrossRef
  11. Duncan SH, Louis P, Flint HJ (2004) Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl Environ Microbiol 70:5810-817 CrossRef
  12. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR (2007) Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 104:13780-3785 CrossRef
  13. Griffiths RI, Whiteley AS, O’Donnell AG, Bailey MJ (2000) Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA based microbial community composition. Appl Environ Microbiol 66:5488-491 CrossRef
  14. Grootaert C, Van den Abbeele P, Marzorati M, Broekaert WF, Courtin CM, Delcour JA, Verstraete W, Van de Wiele T (2009) Comparison of prebiotic effects of arabinoxylan oligosaccharides and inulin in a simulator of the human intestinal microbial ecosystem. FEMS Microbiol Ecol 69:231-42 CrossRef
  15. Hartemink R, Domenech VR, Rombouts FM (1997) LAMVAB -a new selective medium for the isolation of lactobacilli from faeces. J Microbiol Methods 29:77-4 CrossRef
  16. Heilig HG, Zoetendal EG, Vaughan EE, Marteau P, Akkermans AD, de Vos WM (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 68:114-23 CrossRef
  17. Jacobs DM, Fuhrmann JC, van Dorsten FA, Rein D, Peters S, van Velzen EJ, Hollebrands B, Draijer R, van Duynhoven J, Garczarek U (2012) Impact of short-term intake of red wine and grape polyphenol extract on the human metabolome. J Agric Food Chem 60:3078-085 CrossRef
  18. Jiménez-Gir?n A, Queipo-Ortu?o MI, Boto-Ord??ez M, Mu?oz-González I, Sánchez-Patán F, Monagas M, Martín-álvarez PJ, Murri M, Tinahones FJ, Andrés-Lacueva C, Bartolomé B, Moreno-Arribas MV (2013) Comparative study of microbial-derived phenolic metabolites in human feces after intake of gin, red wine, and dealcoholized red wine. J Agric Food Chem 61:3909-915 CrossRef
  19. Jin JS, Hattori M (2012) Isolation and characterization of a human intestinal bacterium / Eggerthella sp. CAT-1 capable of cleaving the C-ring of (+)-catechin and (?-epicatechin, followed by / p-dehydroxylation of the B-ring. Biol Pharm Bull 35:2252-256 CrossRef
  20. Kemperman RA, Gross G, Mondot S, Possemiers S, Marzorati M, Van de Wiele T, Dore J, Vaughan EE (2013) Impact of polyphenols from black tea and red wine/grape juice on a gut model microbiome. Food Res Int 53:659-69 CrossRef
  21. Kishimoto Y, Tani M, Kondo K (2013) Pleiotropic preventive effects of dietary polyphenols in cardiovascular diseases. Eur J Clin Nutr 67:532-35 CrossRef
  22. Kowalchuk GA, Bodelier PLE, Heilig GHJ, Stephen JR, Laanbroek HJ (1998) Community analysis of ammonia oxidizing bacteria, in relation to oxygen availability in soils and root-oxygenated sediments, using PCR, DGGE and oligonucleotide probe hybridisation. FEMS Microbiol Ecol 27:339-50 CrossRef
  23. Kutschera M, Engst W, Blaut M, Braune A (2011) Isolation of catechin-converting human intestinal bacteria. J Appl Microbiol 111:165-75 CrossRef
  24. Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, Almeida M, Arumugam M, Batto JM, Kennedy S, Leonard P, Li J, Burgdorf K, Grarup N, J?rgensen T, Brandslund I, Nielsen HB, Juncker AS, Bertalan M, Levenez F, Pons N, Rasmussen S, Sunagawa S, Tap J, Tims S, Zoetendal EG, Brunak S, Clément K, Doré J, Kleerebezem M, Kristiansen K, Renault P, Sicheritz-Ponten T, de Vos WM, Zucker JD, Raes J, Hansen T, Bork P, Wang J, Ehrlich SD, MetaHIT consortium (2013) Richness of human gut microbiome correlates with metabolic markers. Nature 500:541-46 CrossRef
  25. Marzorati M, Verhelst A, Luta G, Sinnott R, Verstraete W, Van de Wiele T, Possemiers S (2010) In vitro modulation of the human gastrointestinal microbial community by plant-derived polysaccharide-rich dietary supplements. Int J Food Microbiol 139:168-76 CrossRef
  26. Monagas M, Khan N, Andrés-Lacueva C, Urpí-Sardá M, Vázquez-Agell M, Lamuela-Raventós RM, Estruch R (2009) Dihydroxylated phenolic acids derived from microbial metabolism reduce lipopolysaccharide-stimulated cytokine secretion by human peripheral blood mononuclear cells. Br J Nutr 102:201-06 CrossRef
  27. Monagas M, Urpi-Sarda M, Sánchez-Patán F, Llorach R, Garrido I, Gómez-Cordovés C, Andrés-Lacueva C, Bartolome B (2010) Insights into the metabolism and microbial biotransformation of dietary flavan-3-ols and the bioactivity of their metabolites. Food Funct 1:233-53 CrossRef
  28. Possemiers S, Verthé K, Uyttendaele S, Verstraete W (2004) PCR-DGGE-based quantification of stability of the microbial community in a simulator of the human intestinal microbial ecosystem. FEMS Microbiol Ecol 49:495-07 CrossRef
  29. Queipo-Ortu?o MI, Boto-Ordó?ez M, Murri M, Gómez-Zumaquero JM, Clemente-Postigo M, Estruch R, Cardona Díaz F, Andrés-Lacueva C, Tinahones FJ (2012) Influence of red wine polyphenols and ethanol on the gut microbiota ecology and biochemical biomarkers. Am J Clin Nutr 95:1323-334 CrossRef
  30. Rechner AR, Kroner C (2005) Anthocyanins and colonic metabolites of dietary polyphenols inhibit platelet function. Thromb Res 116:327-34 CrossRef
  31. Requena T, Monagas M, Pozo-Bayón MA, Martín-Alvárez PJ, Bartolomé B, Del Campo R, Avila M, Martínez-Cuesta MC, Pelaez C, Moreno-Arribas MV (2010) Perspectives of the potential implications of wine polyphenols on human oral and gut microbiota. Trends Food Sci Technol 21:332-44 CrossRef
  32. Russell WR, Duncan SH, Scobbie L, Duncan G, Cantlay L, Calder AG, Anderson SE, Flint HJ (2013) Major phenylpropanoid-derived metabolites in the human gut can arise from microbial fermentation of protein. Mol Nutr Food Res 57:523-35 CrossRef
  33. Sánchez-Patán F, Monagas M, Moreno-Arribas MV, Bartolomé B (2011) Determination of microbial phenolic acids in human faeces by UPLC–ESI-TQ MS. J Agric Food Chem 59:2241-247 CrossRef
  34. Sánchez-Patán F, Cueva C, Monagas M, Walton GE, Gibson GR, Quintanilla-López JE, Lebrón-Aguilar R, Martín-álvarez PJ, Moreno-Arribas MV, Bartolomé B (2012a) In vitro fermentation of a red wine extract by human gut microbiota: Changes in microbial groups and formation of phenolic metabolites. J Agric Food Chem 60:2136-147 CrossRef
  35. Sánchez-Patán F, Tabasco R, Monagas M, Requena T, Peláez C, Moreno-Arribas MV, Bartolomé B (2012b) Capability of / Lactobacillus plantarum IFPL935 to catabolize flavan-3-ol compounds and complex phenolic extracts. J Agric Food Chem 60:7142-151 CrossRef
  36. Selma MV, Espín JC, Tomás-Barberán FA (2009) Interaction between phenolics and gut microbiota: role in human health. J Agric Food Chem 57:6485-501 CrossRef
  37. Stevenson DE, Hurst RD (2007) Polyphenolic phytochemicals—just antioxidants or much more? Cell Mol Life Sci 64:2900-916 CrossRef
  38. Tabasco R, Sánchez-Patán F, Monagas M, Bartolomé B, Moreno-Arribas MV, Peláez C, Requena T (2011) Effect of grape polyphenols on lactic acid bacteria and bifidobacteria growth: resistance and metabolism. Food Microbiol 28:1345-352 CrossRef
  39. Tomás-Barberán FA, Andrés-Lacueva C (2012) Polyphenols and health: current state and progress. J Agric Food Chem 60:8773-775 CrossRef
  40. Tzounis X, Vulevic J, Kuhnle GC, George T, Leonczak J, Gibson GR, Kwik-Uribe C, Spencer JP (2008) Flavonol monomer induced changes to the human faecal microflora. Br J Nutr 99:782-92 CrossRef
  41. Tzounis X, Rodriguez-Mateos A, Vulevic J, Gibson GR, Kwik-Uribe C, Spencer JPE (2011) Prebiotic evaluation of cocoa-derived flavanols in healthy humans by using a randomized, controlled, double-blind, crossover intervention study. Am J Clin Nutr 93:62-2 CrossRef
  42. Van de Wiele T, Boon N, Possemiers S, Jacobs H, Verstraete W (2007) Inulin-type fructans of longer degree of polymerization exert more pronounced in vitro prebiotic effects. J Appl Microbiol 102:452-60
  43. Van den Abbeele P, Grootaert C, Marzorati M, Possemiers S, Verstraete W, Gérard P, Rabot S, Bruneau A, El Aidy S, Derrien M, Zoetendal E, Kleerebezem M, Smidt H, Van de Wiele T (2010) Microbial community development in a dynamic gut model is reproducible, colon region specific, and selective for / Bacteroidetes and / Clostridium cluster IX. Appl Environ Microbiol 76:5237-246 CrossRef
  44. Van den Abbeele P, Venema K, Van de Wiele T, Verstraete W, Possemiers S (2013) Different human gut models reveal the distinct fermentation patterns of arabinoxylan versus inulin. J Agric Food Chem 61:9819-827 CrossRef
  45. Van Dorsten FA, Peters S, Gross G, Gómez-Roldán V, Klinkenberg M, De Vos RC, Vaughan EE, Van Duynhoven JP, Possemiers S, Van de Wiele T, Jacobs DM (2012) Gut microbial metabolism of polyphenols from black tea and red wine/grape juice is source-specific and colon-region dependent. J Agric Food Chem 60:11331-1342 CrossRef
  46. Van Duynhoven J, Vaughan EE, Jacobs DM, Kemperman RA, Van Velzen EJ, Gross G, Roger LC, Possemiers S, Smilde AK, Doré J, Westerhuis JA, Van de Wiele T (2011) Metabolic fate of polyphenols in the human superorganism. Proc Natl Acad Sci U S A 108:4531-538 CrossRef
  47. Wang LQ, Meselhy MR, Li Y, Nakamura N, Min BS, Qin GW, Hattori M (2001) The heterocyclic ring fission and dehydroxylation of catechins and related compounds by / Eubacterium sp. strain SDG-2, a human intestinal bacterium. Chem Pharm Bull 49:1640-643 CrossRef
  48. Ward NC, Croft KD, Puddey IB, Hodgson JM (2004) Supplementation with grape seed polyphenols results in increased urinary excretion of 3-hydroxyphenylpropionic acid, an important metabolite of proanthocyanidins in humans. J Agric Food Chem 52:5545-549 CrossRef
  49. Waterhouse AL (2002) Wine phenolics. Ann N Y Acad Sci 957:21-6 CrossRef
  50. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, Sinha R, Gilroy E, Gupta K, Baldassano R, Nessel L, Li H, Bushman FD, Lewis JD (2011) Linking long-term dietary patterns with gut microbial enterotypes. Science 334:105-08 CrossRef
  51. Xia EQ, Deng GF, Guo YJ, Li HB (2010) Biological activities of polyphenols from grapes. Int J Mol Sci 11:622-46 CrossRef
  
• 作者单位：E. Barroso (1)
  T. Van de Wiele (2)
  A. Jiménez-Girón (1)
  I. Mu?oz-González (1)
  P. J. Martín-Alvarez (1)
  M. V. Moreno-Arribas (1)
  B. Bartolomé (1)
  C. Peláez (1)
  M. C. Martínez-Cuesta (1)
  T. Requena (1)
  
  1. Departamento de Biotecnología y Microbiología de Alimentos, Instituto de Investigación en Ciencias de la Alimentación CIAL (CSIC-UAM), Nicolás Cabrera 9, 28049, Madrid, Spain
  2. LabMET, Faculty of Bioscience Engineering, Ghent University, 9000, Ghent, Belgium
  
• ISSN：1432-0614

文摘

The colonic microbiota plays an important role in the bioavailibility of dietary polyphenols. This work has evaluated the impact on the gut microbiota of long-term feeding with both a red wine polyphenolic extract and the flavan-3-ol metabolizer strain Lactobacillus plantarum IFPL935. The study was conducted in the dynamic Simulator of the Human Intestinal Microbial Ecosystem (SHIME). The feeding of the gut microbiota model with red wine polyphenols caused an initial decrease in the counts of total bacteria in the ascending colon (AC), with Bacteroides, Clostridium coccoides/Eubacterium rectale and Bifidobacterium being the most affected bacterial groups. The bacterial counts recovered to initial numbers faster than the overall microbial fermentation and proteolysis, which seemed to be longer affected by polyphenols. Addition of L. plantarum IFPL935 helped to promptly recover total counts, Lactobacillus and Enterobacteriaceae and led to an increase in lactic acid formation in the AC vessel at the start of the polyphenol treatment as well as butyric acid in the transverse (TC) and descending (DC) vessels after 5?days. Moreover, L. plantarum IFPL935 favoured the conversion in the DC vessel of monomeric flavan-3-ols and their intermediate metabolites into phenylpropionic acids and in particular 3-(3-hydroxyphenyl)propionic acid. The results open the possibilities of using L. plantarum IFPL935 as a food ingredient for helping individuals showing a low polyphenol-fermenting metabotype to increase their colonic microbial capacities of metabolizing dietary polyphenols.