Interactions of a lignin-rich fraction from Brewer's spent grain with gut microbiota in vitro

Journal of Agricultural and Food Chemistry

Volumn 61, Issue 27, 2013, Pages 6754-6762

  Niemi, Piritta ^a   Aura, Anna Marja ^a   Maukonen, Johanna ^a   Smeds, Annika I ^b   Mattila, Ismo ^a   Niemelä, Klaus ^a   Tamminen, Tarja ^a   Faulds, Craig B ^a,c   Buchert, Johanna ^a   Poutanen, Kaisa ^a  

^a VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^b ÅBO AKADEMI UNIVERSITY   (Finland)

^c AIX MARSEILLE UNIVERSITY   (France)

Author keywords

bifidobacteria; brewer's spent grain; colon microbiota; dietary fiber; in vitro fermentation; lactobacilli; lignan; lignin

Indexed keywords

BIFIDOBACTERIA; BREWER'S SPENT GRAIN; DIETARY FIBERS; IN-VITRO; LACTOBACILLI; LIGNAN; MICROBIOTAS;

BACILLI; FERMENTATION;

LIGNIN;

LIGNIN;

ARTICLE; BACTERIUM; BIOLOGICAL MODEL; CEREAL; CHEMISTRY; COLON; FECES; FERMENTATION; HUMAN; METABOLISM; MICROBIOLOGY; MICROFLORA; WASTE;

BACTERIA; CEREALS; COLON; FECES; FERMENTATION; HUMANS; LIGNIN; MICROBIOTA; MODELS, BIOLOGICAL; WASTE PRODUCTS;

EID: 84880015010     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf401738x     Document Type: Article

References (43)

1. Smith, C. E.; Tucker, K. L. Health benefits of cereal fibre: a review of clinical trials Nutr. Res. Rev. 2011, 24, 118-131
2. Commission Directive 2008/100/EC. http://eur-lex.europa.eu/LexUriServ/ LexUriServ.do?uri=OJ:L:2008:285:0009:0012:EN:PDF (accessed Feb 20, 2013).
3. Vanholme, R.; Demedts, B.; Morreel, K.; Ralph, J.; Boerjan, W. Lignin biosynthesis and structure Plant Physiol. 2010, 153, 895-905
4. Bunzel, M.; Ralph, J.; Lu, F.; Hatfield, R. D.; Steinhart, H. Lignins and ferulate-coniferyl alcohol cross-coupling products in cereal grains J. Agric. Food Chem. 2004, 52, 6496-6502
5. Holloway, W. D.; Tasman-Jones, C.; Lee, S. P. Digestion of certain fractions of dietary fiber in humans Am. J. Clin. Nutr. 1978, 31, 927-930
6. Garleb, K. A.; Fahey, G. C.; Lewis, S. M.; Kerley, M. S.; Montgomery, L. Chemical composition and digestibility of fiber fractions of certain by-product feedstuffs fed to ruminants J. Anim. Sci. 1988, 66, 2650-2662
7. Palonen, H.; Tjerneld, F.; Zacchi, G.; Tenkanen, M. Adsorption of Trichoderma reesei CBH I and EG II and their catalytic domains on steam pretreated softwood and isolated lignin J. Biotechnol. 2004, 107, 65-72
8. Geib, S. M.; Filley, T. R.; Hatcher, P. G.; Hoover, K.; Carlson, J. E.; Jimenez-Gasco, M. d. M.; Nakagawa-Izumi, A.; Sleighter, R. L.; Tien, M. Lignin degradation in wood-feeding insects Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 12932-12937
9. Csonka, F. A.; Phillips, M.; Jones, D. B. Studies on lignin metabolism J. Biol. Chem. 1929, 85, 65-75
10. Silanikove, N.; Brosh, A. Lignocellulose degradation and subsequent metabolism of lignin fermentation products by the desert black Bedouin goat fed on wheat straw as a single-component diet Br. J. Nutr. 1989, 62, 509-520
11. Williams, R. D.; Olmsted, W. H.; Hamann, C. H.; Fiorito, J. A.; Duckles, D. The effect of cellulose, hemicellulose and lignin on the weight of the stool: a contribution to the study of laxation in man J. Nutr. 1936, 11, 433-449
12. Kelsay, J. L.; Goering, H. K.; Behall, K. M.; Prather, E. S. Effect of fiber from fruits and vegetables on metabolic responses of human subjects: fiber intakes, fecal excretions, and apparent digestibilities Am. J. Clin. Nutr. 1981, 34, 1849-1852
13. Leonowicz, A.; Matuszewska, A.; Luterek, J.; Ziegenhagen, D.; Wojtaś-Wasilewska, M.; Cho, N.; Hofrichter, M.; Rogalski, J. Biodegradation of lignin by white rot fungi Fungal Genet. Biol. 1999, 27, 175-185
14. Bugg, T. D.; Ahmad, M.; Hardiman, E. M.; Singh, R. The emerging role for bacteria in lignin degradation and bio-product formation Curr. Opin. Biotechnol. 2011, 22, 394-400
15. Aura, A.-M.; Mattila, I.; Hyötyläinen, T.; Gopalacharyulu, P.; Cheynier, V.; Souquet, J.; Bes, M.; Bourvellec, C.; Guyot, S.; Orešič, M. Characterization of microbial metabolism of Syrah grape products in an in vitro colon model using targeted and non-targeted analytical approaches Eur. J. Nutr. 2012, 1-14
16. Bazzocco, S.; Mattila, I.; Guyot, S.; Renard, C.; Aura, A.-M. Factors affecting the conversion of apple polyphenols to phenolic acids and fruit matrix to short-chain fatty acids by human faecal microbiota in vitro Eur. J. Nutr. 2008, 47, 442-452
17. Scalbert, A. Antimicrobial properties of tannins Phytochemistry 1991, 30, 3875-3883
18. Niemi, P.; Tamminen, T.; Smeds, A.; Viljanen, K.; Ohra-aho, T.; Holopainen-Mantila, U.; Faulds, C. B.; Poutanen, K.; Buchert, J. Characterization of lipids and lignans in brewer's spent grain and its enzymatically extracted fraction J. Agric. Food Chem. 2012, 60, 9910-9917
19. Smeds, A. I.; Eklund, P. C.; Sjöholm, R. E.; Willför, S. M.; Nishibe, S.; Deyama, T.; Holmbom, B. R. Quantification of a broad spectrum of lignans in cereals, oilseeds, and nuts J. Agric. Food Chem. 2007, 55, 1337-1346
20. Smeds, A. I.; Hakala, K.; Hurmerinta, T. T.; Kortela, L.; Saarinen, N. M.; Mäkelä, S. I. Determination of plant and enterolignans in human serum by high-performance liquid chromatography with tandem mass spectrometric detection J. Pharm. Biomed. Anal. 2006, 41, 898-905
21. Barry, J.-L.; Hoebler, C.; MacFarlane, G. T.; MacFarlane, S.; Mathers, J. C.; Reed, K. A.; Mortensen, P. B.; Nordgaard, I.; Rowland, I. R.; Rumney, C. J. Estimation of the fermentability of dietary fibre in vitro: a European interlaboratory study Br. J. Nutr. 1995, 74, 303-322
22. Schooley, D. L.; Kubiak, F. M.; Evans, J. V. Capillary gas chromatographic analysis of volatile and non-volatile organic acids from biological samples as the t-butyldimethylsilyl derivatives J. Chromatogr. Sci. 1985, 23, 385-390
23. Castillo, S.; Mattila, I.; Miettinen, J.; Orešič, M.; Hyötyläinen, T. Data analysis tool for comprehensive two-dimensional gas chromatography/time-of-flight mass spectrometry Anal. Chem. 2011, 83, 3058-3067
24. Golm metabolome database; http://gmd.mpimp-golm.mpg.de/search.aspx (accessed May 30, 2012).
25. Smeds, A. I.; Eklund, P. C.; Willför, S. M. Content, composition, and stereochemical characterisation of lignans in berries and seeds Food Chem. 2012, 134, 1991-1998
26. Niemelä, K.; Sjöström, E. Simultaneous identification of aromatic and aliphatic low molecular weight compounds from alkaline pulping liquor by capillary gas-liquid chromatography-mass spectrometry Holzforschung 1986, 40, 361-368
27. Niemelä, K. Low-molecular-weight organic compounds in birch kraft black liquor Ann. Acad. Sci. Fenn., Ser. A II, Chem. 1990, 229, 1-142
28. Comalada, M.; Bailón, E.; de Haro, O.; Lara-Villoslada, F.; Xaus, J.; Zarzuelo, A.; Gálvez, J. The effects of short-chain fatty acids on colon epithelial proliferation and survival depend on the cellular phenotype J. Cancer Res. Clin. Oncol. 2006, 132, 487-497
29. Hosseini, E.; Grootaert, C.; Verstraete, W.; Van de Wiele, T. Propionate as a health-promoting microbial metabolite in the human gut Nutr. Rev. 2011, 69, 245-258
30. Kontula, P.; Jaskari, J.; Nollet, L.; De Smet, I.; von Wright, A.; Poutanen, K.; Mattila-Sandholm, T. The colonization of a simulator of the human intestinal microbial ecosystem by a probiotic strain fed on a fermented oat bran product: effects on the gastrointestinal microbiota Appl. Microbiol. Biotechnol. 1998, 50, 246-252
31. Janer, C.; Arigoni, F.; Lee, B. H.; Peláez, C.; Requena, T. Enzymatic ability of Bifidobacterium animalis subsp. lactis to hydrolyze milk proteins: Identification and characterization of endopeptidase O Appl. Environ. Microbiol. 2005, 71, 8460-8465
32. Aura, A.-M.; Oikarinen, S.; Mutanen, M.; Heinonen, S.-M.; Adlercreutz, H. C. T.; Virtanen, H.; Poutanen, K. S. Suitability of a batch in vitro fermentation model using human faecal microbiota for prediction of conversion of flaxseed lignans to enterolactone with reference to an in vivo rat model Eur. J. Nutr. 2006, 45, 45-51
33. Hernanz, D.; Nuñez, V.; Sancho, A. I.; Faulds, C. B.; Williamson, G.; Bartolomé, B.; Gómez-Cordovés, C. Hydroxycinnamic acids and ferulic acid dehydrodimers in barley and processed barley J. Agric. Food Chem. 2001, 49, 4884-4888
34. Braune, A.; Bunzel, M.; Yonekura, R.; Blaut, M. Conversion of dehydrodiferulic acids by human intestinal microbiota J. Agric. Food Chem. 2009, 57, 3356-3362
35. Adlercreutz, H. Lignans and human health Crit. Rev. Clin. Lab. Sci. 2007, 44, 483-525
36. Begum, A. N.; Nicolle, C.; Mila, I.; Lapierre, C.; Nagano, K.; Fukushima, K.; Heinonen, S.; Adlercreutz, H.; Rémésy, C.; Scalbert, A. Dietary lignins are precursors of mammalian lignans in rats J. Nutr. 2004, 134, 120-127
37. Heinonen, S.; Nurmi, T.; Liukkonen, K.; Poutanen, K.; Wähälä, K.; Deyama, T.; Nishibe, S.; Adlercreutz, H. In vitro metabolism of plant lignans: new precursors of mammalian lignans enterolactone and enterodiol J. Agric. Food Chem. 2001, 49, 3178-3186
38. Pietinen, P.; Stumpf, K.; Männistö, S.; Kataja, V.; Uusitupa, M.; Adlercreutz, H. Serum enterolactone and risk of breast cancer: a case-control study in eastern Finland Cancer Epidemiol. Biomarkers Prev. 2001, 10, 339-344
39. Vanharanta, M.; Voutilainen, S.; Lakka, T. A.; van der Lee, M.; Adlercreutz, H.; Salonen, J. T. Risk of acute coronary events according to serum concentrations of enterolactone: a prospective population-based case-control study Lancet 1999, 354, 2112-2115
40. Funk, C.; Weber, P.; Thilker, J.; Grabber, J. H.; Steinhart, H.; Bunzel, M. Influence of lignification and feruloylation of maize cell walls on the adsorption of heterocyclic aromatic amines J. Agric. Food Chem. 2006, 54, 1860-1867
41. Funk, C.; Braune, A.; Grabber, J. H.; Steinhart, H.; Bunzel, M. Model studies of lignified fiber fermentation by human fecal microbiota and its impact on heterocyclic aromatic amine adsorption Mutat. Res. 2007, 624, 41-48
42. Vitaglione, P.; Napolitano, A.; Fogliano, V. Cereal dietary fibre: a natural functional ingredient to deliver phenolic compounds into the gut Trends Food Sci. Technol. 2008, 19, 451-463
43. Dizhbite, T.; Telysheva, G.; Jurkjane, V.; Viesturs, U. Characterization of the radical scavenging activity of lignins-natural antioxidants Bioresour. Technol. 2004, 95, 309-317-317