Lactobacillus plantarum IFPL935 favors the initial metabolism of red wine polyphenols when added to a colonic microbiota

Journal of Agricultural and Food Chemistry

Volumn 61, Issue 42, 2013, Pages 10163-10172

  Barroso, Elvira ^a   Sánchez Patán, Fernando ^a   Martín Alvarez, Pedro J ^a   Bartolomé, Begoña ^a   Moreno Arribas, María Victoria ^a   Peláez, Carmen ^a   Requena, Teresa ^a   Van De Wiele, Tom ^b   Martínez Cuesta, M Carmen ^a  

^a INSTITUTE OF FOOD SCIENCE RESEARCH CIAL   (Spain)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

batch fermentations; colonic microbiota; Lactobacillus; metabolism; polyphenols

Indexed keywords

BACILLI; BIOCHEMISTRY; BIOMOLECULES; FATTY ACIDS; FLAVONOIDS; METABOLISM; WINE;

BATCH FERMENTATION; COLONIC MICROBIOTA; LACTOBACILLUS; LACTOBACILLUS PLANTARUM; MICROBIAL COMMUNITIES; PHENOLIC METABOLITES; POLYPHENOLS; PROTEOLYTIC ACTIVITIES;

METABOLITES;

LACTOBACILLUS; LACTOBACILLUS PLANTARUM;

BIFLAVONOID; CATECHIN; FLAVONOID; FLAVORING AGENT; POLYPHENOL; PROANTHOCYANIDIN; PROCYANIDIN;

ARTICLE; BACTERIUM; CLASSIFICATION; COLON; GENETICS; HUMAN; ISOLATION AND PURIFICATION; LACTOBACILLUS PLANTARUM; METABOLISM; MICROBIOLOGY; MICROFLORA; WINE;

BACTERIA; BIFLAVONOIDS; CATECHIN; COLON; FLAVONOIDS; FLAVORING AGENTS; HUMANS; LACTOBACILLUS PLANTARUM; MICROBIOTA; POLYPHENOLS; PROANTHOCYANIDINS; WINE;

EID: 84886537483     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf402816r     Document Type: Article

References (48)

1. Del Rio, D.; Rodriguez-Mateos, A.; Spencer, J. P. E.; Tognolini, M.; Borges, G.; Crozier, A. Dietary (poly)phenolics in human health: Structures, bioavailability, and evidence of protective effects against chronic diseases Antioxid. Redox Signal. 2013, 18, 1818-1892
2. Waterhouse, A. L. Wine phenolics Ann. N.Y. Acad. Sci. 2002, 957, 21-36
3. Crozier, A. Dietary phenolics, absorption, mammalian and microbial metabolism and colonic health Mol. Nutr. Food Res. 2009, 53, S5-6
4. Hackman, R. M.; Polagruto, J. A.; Yan Zhu, Q.; Sun, B.; Fujii, H.; Keen, C. L. Flavanols: Digestion, absorption and bioactivity Phytochem. Rev. 2008, 7, 195-208
5. van Duynhoven, J.; Vaughan, E. E.; Jacobs, D. M.; Kemperman, R. A.; van Velzen, E. J.; Gross, G.; Roger, L. C.; Possemiers, S.; Smilde, A. K.; Doré, J.; Westerhuis, J. A.; Van de Wiele, T. Metabolic fate of polyphenols in the human superorganism Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 4531-4538
6. Possemiers, S.; Bolca, S.; Verstraete, W.; Heyerick, A. The intestinal microbiome: A separate organ inside the body with the metabolic potential to influence the bioactivity of botanicals Fitoterapia. 2011, 82, 53-66
7. Aura, A. M. Microbial metabolism of dietary phenolic compounds in the colon Phytochem. Rev. 2008, 7, 407-429
8. Selma, M. V.; Espín, J. C.; Tomás-Barberán, F. A. Interaction between phenolics and gut microbiota: Role in human health J. Agric. Food Chem. 2009, 57, 6485-6501
9. Requena, T.; Monagas, M.; Pozo-Bayon, M. A.; Martin-Alvarez, P. J.; Bartolome, B.; del Campo, R.; Avila, M.; Martinez-Cuesta, M. C.; Pelaez, C.; Moreno-Arribas, M. V. Perspectives of the potential implications of wine polyphenols on human oral and gut microbiota Trends Food Sci. Technol. 2010, 21, 332-344
10. Tzounis, X.; Vulevic, J.; Kuhnle, G. C.; George, T.; Leonczak, J.; Gibson, G. R.; Kwik-Uribe, C.; Spencer, J. P. Flavonol monomer-induced changes to the human faecal microflora Br. J. Nutr. 2008, 99, 782-792
11. Dolara, P.; Luceri, C.; De, F. C.; Femia, A. P.; Giovannelli, L.; Caderni, G.; Cecchini, C.; Silvi, S.; Orpianesi, C.; Cresci, A. Red wine polyphenols influence carcinogenesis, intestinal microflora, oxidative damage and gene expression profiles of colonic mucosa in F344 rats Mutat. Res. 2005, 591, 237-246
12. Queipo-Ortuño, M. I.; Boto-Ordoñez, M.; Murri, M.; Gomez-Zumaquero, J. M.; Clemente-Postigo, M.; Estruch, R.; Cardona Diaz, F.; Andrés-Lacueva, C.; Tinahones, F. J. Influence of red wine polyphenols and ethanol on the gut microbiota ecology and biochemical biomarkers Am. J. Clin. Nutr. 2012, 95, 1323-1334
13. Tabasco, R.; Sánchez-Patán, F.; Monagas, M.; Bartolomé, B.; Moreno-Arribas, M. V.; Peláez, C.; Requena, T. Effect of grape polyphenols on lactic acid bacteria and bifidobacteria growth: Resistance and metabolism Food Microbiol. 2011, 28, 1345-1352
14. Sánchez-Patán, F.; Tabasco, R.; Monagas, M.; Requena, T.; Peláez, C.; Moreno-Arribas, M. V.; Bartolomé, B. Capability of Lactobacillus plantarum IFPL935 to catabolize flavan-3-ol compounds and complex phenolic extracts J. Agric. Food Chem. 2012, 60, 7142-7151
15. Wang, L. Q.; Meselhy, M. R.; Li, Y.; Nakamura, N.; Min, B. S.; Qin, G. W.; Hattori, M.. The heterocyclic ring fission and dehydroxylation of catechins and related compounds by Eubacterium sp. strain SDG-2, a human intestinal bacterium Chem. Pharm. Bull. 2011, 49, 1640-1643
16. Kutschera, M.; Engst, W.; Blaut, M.; Braune, A. Isolation of catechin-converting human intestinal bacteria J. Appl. Microbiol. 2011, 111, 165-175
17. Fontecha, J.; Peláez, C.; Juárez, M.; Requena, T.; Gómez, C.; Ramos, M. Biochemical and microbiological characteristics of artisanal hard goat's cheese J. Dairy Sci. 1990, 73, 1150-1157
18. Sánchez-Patán, F.; Cueva, C.; Monagas, M.; Walton, G. E.; Gibson, G. R.; Quintanilla-López, J. E.; Lebrón-Aguilar, R.; Martín-álvarez, P. J.; Moreno-Arribas, M. V.; Bartolomé, B. 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. 2012, 60, 2136-2147
19. Molly, K.; van de Woestijne, M.; Verstraete, W. Development of a 5-step multichamber reactor as a simulation of the human intestinal microbial ecosystem Appl. Microbiol. Biotechnol. 1993, 39, 254-258
20. 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. 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
21. Molly, K.; van de Woestyne, M.; DeSmet, I.; Verstraete, W. Validation of the simulator of the human intestinal microbial ecosystem (SHIME) reactor using microorganism associated activities Microb. Ecol. Health Dis. 1994, 7, 191-200
22. Possemiers, S.; Bolca, S.; Grootaert, C.; Heyerick, A.; Decroos, K.; Dhooge, W.; De Keukeleire, D.; Rabot, S.; Verstraete, W.; Van de Wiele, T. The prenylflavonoid isoxanthohumol from hops (Humulus lupulus L.) is activated into the potent phytoestrogen 8-prenylnaringenin in vitro and in the human intestine J. Nutr. 2006, 136, 1862-1867
23. Nübel, U.; Engelen, B.; Felske, A.; Snaidr, J.; Wieshuber, A.; Amann, R. I.; Ludwig, W.; Backhaus, H. Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis J. Bacteriol. 1996, 178, 5636-5643
24. Byun, R.; Nadkarni, M. A.; Chhour, K. L.; Martin, F. E.; Jacques, N. A.; Hunter, N. Quantitative analysis of diverse Lactobacillus species present in advanced dental caries J. Clin. Microbiol. 2004, 42, 3128-3136
25. Matsuki, T.; Watanabe, K.; Fujimoto, J.; Miyamoto, Y.; Takada, T.; Matsumoto, K.; Oyaizu, H.; Tanaka, R. Development of 16S rRNA-gene-targeted group-specific primers for the detection and identification of predominant bacteria in human feces Appl. Environ. Microbiol. 2002, 68, 5445-5451
26. Bartosch, S.; Fite, A.; Macfarlane, G. T.; McMurdo, M.E.. Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota Appl. Environ. Microbiol. 2004, 70, 3575-3581
27. 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
28. Leser, T. D.; Amenuvor, J. Z.; Jensen, T. K.; Lindecrona, R. H.; Boye, M.; Moller, K. Culture independent analysis of gut bacteria: The pig gastrointestinal tract microbiota revisited Appl. Environ. Microbiol. 2002, 68, 673-690
29. Sghir, A.; Gramet, G.; Suau, A.; Rochet, V.; Pochart, P.; Dore, J. Quantification of bacterial groups within human fecal flora by oligonucleotide probe hybridization Appl. Environ. Microbiol. 2000, 66, 2263-2266
30. 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
31. 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
32. Louis, P.; Flint, H. J. Development of a semiquantitative degenerate real-time PCR-based assay for estimation of numbers of butyryl-coenzyme A (CoA) CoA transferase genes in complex bacterial samples Appl. Environ. Microbiol. 2007, 73, 2009-2012
33. Griffiths, R. I.; Whiteley, A. S.; O'Donnell, A. G.; Bailey, M.J.. Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNAbased microbial community composition Appl. Environ. Microbiol. 2000, 66, 5488-5491
34. Kowalchuk, G. A.; Bodelier, P. L. E.; Heilig, G. H. J.; Stephen, J. R.; Laanbroek, H. J. Community analysis of ammonia oxidising bacteria, in relation to oxygen availability in soils and root-oxygenated sediments, using PCR, DGGE and oligonucleotide probe hybridisation FEMS Microbiol. Ecol. 1998, 27, 339-350
35. Godornes, C.; Leader, B. T.; Molini, B. J.; Centurion-Lara, A.; Lukehart, S. A. Quantification of rabbit cytokine mRNA by real-time RT-PCR Cytokine 2007, 38, 1-7
36. Alander, M.; De Smet, I.; Nollet, L.; Verstraete, W.; Von Wright, A.; Mattila-Sandholm, T. The effect of probiotic strains on the microbiota of the simulator of the human intestinal microbial ecosystem (SHIME) Int. J. Food Microbiol. 1999, 46, 71-79
37. Bremner, J. M.; Keeney, R. D. Steam distillation methods for determination of ammonium, nitrate and nitrite Anal. Chem. Acta 1965, 32, 485-495
38. Sánchez-Patán, F.; Monagas, M.; Moreno-Arribas, M. V.; Bartolomé, B.. Determination of microbial phenolic acids in human faeces by UPLC-ESI-TQ MS J. Agric. Food. Chem. 2011, 59, 2241-2247
39. Jiménez-Giŕn, A.; Queipo-Ortuño, M. I.; Boto-Ord́ñez, M.; Muñoz-González, I.; Sánchez-Patán, F.; Monagas, M.; Martín-álvarez, P. J.; Murri, M.; Tinahones, F. J.; Andrés-Lacueva, C.; Bartolomé, B.; Moreno-Arribas, M. V. Comparative study of microbial-derived phenolic metabolites in human feces after intake of gin, red wine, and dealcoholized red wine J. Agric. Food Chem. 2013, 61, 3909-3915
40. Gibson, G. R.; Fuller, R. Aspects of in vitro and in vivo research approaches directed toward identifying probiotics and prebiotics for human use J. Nutr. 2000, 130, 391S-395S
41. Monagas, M.; Urpi-Sarda, M.; Sanchez-Patan, F.; Llorach, R.; Garrido, I.; Gomez-Cordoves, C.; Andres-Lacueva, C.; Bartolome, B. Insights into the metabolism and microbial biotransformation of dietary flavan-3-ols and the bioactivity of their metabolites Food Funct. 2010, 1, 233-253
42. Clifford, M. N. Diet-derived phenols in plasma and tissues and their implications for health Planta Med. 2004, 70, 1103-1114
43. Van Dorsten, F. A.; Peters, S.; Gross, G.; Gomez-Roldan, V.; Klinkenberg, M.; de Vos, R. C.; Vaughan, E. E.; van Duynhoven, J. P.; Possemiers, S.; van de Wiele, T.; Jacobs, D. M. Gut microbial metabolism of polyphenols from black tea and red wine/grape juice is source-specific and colon-region dependent J. Agric. Food Chem. 2012, 60, 11331-11342
44. Roberfroid, M.; Gibson, G. R.; Hoyles, L.; McCartney, A. L.; Rastall, R.; Rowland, I.; Wolvers, D.; Watzl, B.; Szajewska, H.; Stahl, B.; Guarner, F.; Respondek, F.; Whelan, K.; Coxam, V.; Davicco, M. J.; Léotoing, L.; Wittrant, Y.; Delzenne, N. M.; Cani, P. D.; Neyrinck, A. M.; Meheust, A. Prebiotic effects: Metabolic and health benefits Br. J. Nutr. 2010, 104 (Suppl 2) S1-63
45. Macfarlane, G. T.; Macfarlane, S. Bacteria, colonic fermentation, and gastrointestinal health J. AOAC Int. 2012, 95, 50-60
46. Louis, P.; Young, P.; Holtrop, G.; Flint, H. J. Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA:acetate CoA-transferase gene Environ. Microbiol. 2010, 12, 304-314
47. Belenguer, A.; Duncan, S. H.; Calder, G.; Holtrop, G.; Louis, P.; Lobley, G. E.; Flint, H. J. Two routes of metabolic cross-feeding between bifidobacteria and butyrate-producing anaerobes from the human gut Appl. Environ. Microbiol. 2006, 72, 3593-3599
48. Barcenilla, A.; Pryde, S. E.; Martin, J. C.; Duncan, S. H.; Stewart, C. S.; Henderson, C.; Flint, H. J. Phylogenetic relationships of butyrate-producing bacteria from the human gut Appl. Environ. Microbiol. 2000, 66, 1654-1661