In vitro fermentation of commercial α-gluco-oligosaccharide by faecal microbiota from lean and obese human subjects

British Journal of Nutrition

Volumn 109, Issue 11, 2013, Pages 1980-1989

  Sarbini, Shahrul R ^a   Kolida, Sofia ^b   Gibson, Glenn R ^b   Rastall, Robert A ^b  

^a DEPARTMENT OF CROP SCIENCE   (Malaysia)

^b UNIVERSITY OF READING   (United Kingdom)

Author keywords

Gluco oligosaccharides; Obese subjects; Prebiotics

Indexed keywords

ALPHA GLUCOOLIGOSACCHARIDE; CARBOXYLIC ACID; INULIN; OLIGOSACCHARIDE; PREBIOTIC AGENT; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BACTERIUM CULTURE; BACTEROIDES; BIFIDOBACTERIUM; CONTROLLED STUDY; ENZYME SPECIFICITY; FAECALIBACTERIUM PRAUSNITZII; FECES MICROFLORA; FERMENTATION; FLUORESCENCE IN SITU HYBRIDIZATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN EXPERIMENT; NONHUMAN; NORMAL HUMAN; POLYMERIZATION; PREVOTELLA; PRINCIPAL COMPONENT ANALYSIS;

ADULT; BACTERIA; FECES; FERMENTATION; HUMANS; OBESITY; OLIGOSACCHARIDES;

BACTERIA (MICROORGANISMS); BACTEROIDES; BIFIDOBACTERIUM SP.; FAECALIBACTERIUM PRAUSNITZII; PREVOTELLA;

EID: 84878014126     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114512004205     Document Type: Article

References (64)

1. Gibson GR, Scott KP, Rastall RA, et al. (2010) Dietary prebio-tics: current status and new definition. Food Sci Technol Bull: Funct Foods 7, 1-19.
2. Gibson GR & Fuller R (2000) Aspects of in vitro and in vivo research approaches directed toward identifying probiotics and prebiotics for human use. J Nutr 130, 391.
3. Chung CH & Day DF (2002) Glucooligosaccharides from Leuconostoc mesenteroides B-742 (ATCC 13146): a potential prebiotic. J Indus Microbiol Biotechnol 29, 196-199.
4. Gibson GR (2004) Fibre and effects on probiotics (the prebiotic concept). Clin Nutr Suppl 1, 25-31.
5. Eckburg PB, Bik EM, Bernstein CN, et al. (2005) Diversity of the human intestinal microbial flora. Science 308, 1635-1638.
6. Ley RE, Bäckhed F, Turnbaugh P, et al. (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 102, 11070-11075.
7. Turnbaugh PJ, Ley RE, Mahowald MA, et al. (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027-1131.
8. Bäckhed F, Manchester JK, Semenkovich CF, et al. (2007) Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci U S A 104, 979-984.
9. Ley RE, Turnbaugh PJ, Klein S, et al. (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022-1023.
10. Collado MC, Isolauri E, Laitinen K, et al. (2008) Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. Am J Clin Nutr 88, 894-899.
11. Duncan SH, Lobley GE, Holtrop G, et al. (2008) Human colonic microbiota associated with diet, obesity and weight loss. Int J Obes 32, 1720-1724.
12. Hildebrandt MA, Hoffmann C, Sherrill-Mix SA, et al. (2009) High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 137, 1716-24e2.
13. Murphy EF, Cotter PD, Healy S, et al. (2010) Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models. Gut 59, 1635-1642.
14. Solabia, Bioecolians (2008) http://www.solabia.com/solabia/ solabianutrition.nsf/VS-OPM/37F9DE18A3D1085E-C12574EF003066A4?OpenDocument (cited 31 January 2011).
15. Jeanes A, Haynes WC, Wilham CA, et al. (1954) Characterization and classification of dextrans from ninety-six strains of bacteria. J Am Chem Soc 76, 5041-5052.
16. Franks AH, Harmsen HJM, Raangs GC, et al. (1998) Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16s rRNA-targeted oligonucleotide probes. Appl Environ Microbiol 64, 3336-3345.
17. Harmsen HJM, Elfferich P, Schut F, et al. (1999) A 16s rRNA-targeted probe for detection of lactobacilli and enterococci in faecal samples by fluorescent in situ hybridization. Microb Ecol Health Dis 11, 3-12.
18. Walker AW, Duncan SH, McWilliam Leitch EC, et al. (2005) pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl Environ Microbiol 71, 3692-3700.
19. Hold GL, Schwiertz A, Aminov RI, et al. (2003) Oligonucleo-tide probes that detect quantitatively significant groups of butyrate-producing bacteria in human feces. Appl Environ Microbiol 69, 4320-4324.
20. Harmsen HJM, Raangs GC, He T, et al. (2002) Extensive set of 16s rRNA-based probes for detection of bacteria in human feces. Appl Environ Microbiol 68, 2982-2990.
21. Manz W, Amann R, Ludwig W, et al. (1996) Application of a suite of 16s rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobac-ter-bacteroides in the natural environment. Microbiology 142, 1097-1106.
22. Langendijk P, Schut F, Jansen G, et al. (1995) Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16s rRNA-targeted probes and its application in fecal samples. Appl Environ Microbiol 61, 3069-3075.
23. Harmsen HJM, Wildeboer-Veloo ACM, Grijpstra J, et al. (2000) Development of 16s rRNA-based probes for the Coriobacterium group and the Atopobium cluster and their application for enumeration of Coriobacteriaceae in human feces from volunteers of different age groups. Appl Environ Microbiol 66, 4523-4527.
24. Cote GL (2007) Flavorings and other value-added products from sucrose. In Novel Enzyme Technology for Food Applications, pp. 243-269 [RA Rastall, editor]. Boca Raton, FL: CRC Press.
25. Olano-Martin E, Mountzouris KC, Gibson GR, et al. (2000) In vitro fermentability of dextran, oligodextran and maltodextrin by human gut bacteria. Br J Nutr 83, 247-255.
26. Kaneko T, Kohmoto T, Kikuchi H, et al. (1994) Effects of iso-maltooligosaccharides with different degrees of polymerization on human fecal bifidobacteria. Biosci Biotechnol Biochem 58, 2288-2290.
27. van den Broek LAM, Hinz SWA, Beldman G, et al. (2008) Bifidobacterium carbohydrases-their role in breakdown and synthesis of (potential) prebiotics. Mol Nutr Food Res 52, 146-163.
28. Rada V, Vlková E, Nevoral J, et al. (2006) Comparison of bacterial flora and enzymatic activity in faeces of infants and calves. FEMS Microbiol Lett 258, 25-28.
29. Sarbini SR, Kolida S, Naeye T, et al. (2011) In vitro fermentation of linear and alpha-1, 2-branched dextrans by the human fecal microbiota. Appl Environ Microbiol 77, 5307-5315.
30. Sanz ML, Gibson GR & Rastall RA (2005) Influence of disac-charide structure on prebiotic selectivity in vitro. J Agric Food Chem 53, 5192-5199.
31. Djouzi Z & Andrieux C (1997) Compared effects of three oligosaccharides on metabolism of intestinal microflora in rats inoculated with human faecal flora. Br J Nutr 78, 313-324.
32. Rowland IR (1988) Factors affecting metabolic activity of the intestinal microflora. Drug Metab Rev 19, 243-261.
33. Macfarlane GT & Cummings JH (1991) The colonic flora, fermentation and large bowel digestive function. In The Large Intestine: Physiology, Pathophysiology and Disease, pp. 51-92 [SF Phillips, JH Pemberton and RG Shorter, editors]. New York: Raven Press.
34. Pokusaeva K, O'Connell-Motherway M, Zomer A, et al. (2009) Characterization of two novel a-glucosidases from Bifidobacterium breve UCC2003. Appl Environ Microbiol 75, 1135-1143.
35. Sanz ML, Côté GL, Gibson GR, et al. (2006) Influence of glycosidic linkages and molecular weight on the fermentation of maltose-based oligosaccharides by human gut bacteria. J Agric Food Chem 54, 9779-9784.
36. Jia W, Whitehead RN, Griffiths L, et al. (2010) Is the abundance of Faecalibacterium prausnitzii relevant to Crohn's disease? FEMS Microbiol Lett 310, 138-144.
37. Bastard J-P, Maachi M, Lagathu C, et al. (2006) Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw 17, 4-12.
38. Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444, 860-867.
39. Sbarbati A, Osculati F, Silvagni D, et al. (2006) Obesity and inflammation: evidence for an elementary lesion. Pediatrics 117, 220-223.
40. Scanlan PD, Shanahan F, O'Mahony C, et al. (2006) Culture-independent analyses of temporal variation of the dominant fecal microbiota and targeted bacterial subgroups in Crohn's disease. J Clin Microbiol 44, 3980-3988.
41. Fogarty AW, Glancy C, Jones S, et al. (2008) A prospective study of weight change and systemic inflammation over 9y. Am J Clin Nutr 87, 30-35.
42. Cani PD, Neyrinck AM, Fava F, et al. (2007) Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 50, 2374-2383.
43. Bäckhed F, Ding H, Wang T, et al. (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A 101, 15718-15723.
44. Turnbaugh PJ, Hamady M, Yatsunenko T, et al. (2009) A core gut microbiome in obese and lean twins. Nature 457, 480-484.
45. Falony G, Lazidou K, Verschaeren A, et al. (2009) In vitro kinetic analysis of fermentation of prebiotic inulin-type fructans by Bifidobacterium species reveals four different phenotypes. Appl Environ Microbiol 75, 454-461.
46. Al-Lahham Sa H, Peppelenbosch MP, Roelofsen H, et al. (2010) Biological effects of propionic acid in humans; metabolism, potential applications and underlying mechanisms. Biochim Biophys Acta-Mol Cell Biol Lip 1801, 1175-1183.
47. Kennedy A, Martinez K, Chuang C-C, et al. (2009) Saturated fatty acid-mediated inflammation and insulin resistance in adipose tissue: mechanisms of action and implications. J Nutr 139, 1-4.
48. Ruijschop RMAJ, Boelrijk AEM & te Giffel MC (2008) Satiety effects of a dairy beverage fermented with propionic acid bacteria. Int Dairy J 18, 945-950.
49. Chen W, Anderson J & Jennings D (1984) Propionate may mediate the hypo-cholesterolemic effects of certain soluble plant fibers in cholesterol-fed rats. Proc Soc Exp Biol Med 175, 215-218.
50. Macy JM, Ljungdahl LG & Gottschalk G (1978) Pathway of succinate and propionate formation in Bacteroides fragilis. J Bacteriol 134, 84-91.
51. Salminen S, Bouley C, Boutron-Ruault MC, et al. (1998) Functional food science and gastrointestinal physiology and function. Br J Nutr 80, 147-171.
52. Zigová J, SturdIk E, Vandák D, et al. (1999) Butyric acid production by Clostridium butyricum with integrated extraction and pertraction. Proc Biochem 34, 835-843.
53. Janssen PH & O'Farrell KA (1999) Succinispira mobilis gen. Nov., sp. Nov., a succinate-decarboxylating anaerobic bacterium. Int J Syst Evol Microbiol 49, 1009-1013.
54. Van Gylswyk NO (1995) Succiniclasticum ruminis gen. Nov., sp. Nov., a ruminal bacterium converting succinate to propionate as the sole energy-yielding mechanism. Int J Syst Bacteriol 45, 297-300.
55. Djouzi Z, Andrieux C, Pelenc V, et al. (1995) Degradation and fermentation of a-gluco-oligosaccharides by bacterial strains from human colon: in vitro and in vivo studies in gnotobiotic rats. J Appl Microbiol 79, 117-127.
56. Flickinger EA, Wolf BW, Garleb KA, et al. (2000) Glucose-based oligosaccharides exhibit different in vitro fermentation patterns and affect in vivo apparent nutrient digestibility and microbial populations in dogs. J Nutr 130, 1267-1273.
57. Smiricky-Tjardes MR, Flickinger EA, Grieshop CM, et al. (2003) In vitro fermentation characteristics of selected oligo-saccharides by swine fecal microflora. J Anim Sci 81, 2505-2514.
58. Hartemink R & Rombouts FM (1997) Gas formation from oligosaccharides by the intestinal microflora. In Non-digestible Oligosaccharides: Healthy Food for the Colon? Proceedings of the International Symposium, pp. 57-66 [R Hartemink, editor]. Wageningen: Wageningen Graduate School VLAG.
59. Kolida S & Gibson GR (2007) Prebiotic capacity of inulin-type fructans. J Nutr 137, 2503S-2506S.
60. Bernalier A, Dore J & Durand M (1999) Biochemistry of fermentation. In Colonic Microbiota, Nutrition and Health, pp. 37-53 [GR Gibson and MB Roberfroid, editors]. Dordrecht: Kluwer Academic Publishers.
61. Falony G, Calmeyn T, Leroy F, et al. (2009) Coculture fermentations of Bifidobacterium species and Bacteroides thetaiotaomicron reveal a mechanistic insight into the pre-biotic effect of inulin-type fructans. Appl Environ Microbiol 75, 2312-2319.
62. 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, 5810-5817.
63. Duncan SH, Hold GL, Harmsen H, et al. (2002) Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as Faecalibacter-ium prausnitzii gen. Nov., comb. Nov. Int J Syst Evol Micro-biol 52, 2141-2146.
64. Valette P, Pelenc V, Djouzi Z, et al. (1993) Bioavailability of new synthesised glucooligosaccharides in the intestinal tract of gnotobiotic rats. J Sci Food Agric 62, 121-127.