Starch and starch hydrolysates are favorable carbon sources for Bifidobacteria in the human gut

BMC Microbiology

Volumn 15, Issue 1, 2015, Pages

  Liu, Songling ^a   Ren, Fazheng ^a   Zhao, Liang ^a   Jiang, Lu ^a,b   Hao, Yanling ^a   Jin, Junhua ^c   Zhang, Ming ^b   Guo, Huiyuan ^a,c   Lei, Xingen ^d   Sun, Erna ^b   Liu, Hongna ^b  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b Higher Institution Engineering Research Center of Animal Product   (China)

^c Beijing Laboratory for Food Quality and Safety   (China)

^d Cornell University ^*  (United States)

Author keywords

Adaptation; Bifidobacteria; Gemomics; Nutrient niche; Starch

Indexed keywords

POLYSACCHARIDE; SIGNAL PEPTIDE; STARCH; STARCH HYDROLYSATE; CARBON;

ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL STRAIN; BIFIDOBACTERIUM; BIFIDOBACTERIUM LONGUM; CARBON SOURCE; CONTROLLED STUDY; GROWTH CURVE; INTESTINE FLORA; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MICROBIOME; NONHUMAN; POPULATION ABUNDANCE; PREDICTION; PROTEOMICS; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; CARBOHYDRATE METABOLISM; GASTROINTESTINAL TRACT; GENETICS; HUMAN; HYDROLYSIS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY;

BIFIDOBACTERIUM LONGUM;

BIFIDOBACTERIUM; CARBOHYDRATE METABOLISM; CARBON; GASTROINTESTINAL TRACT; HUMANS; HYDROLYSIS; METABOLIC NETWORKS AND PATHWAYS; STARCH;

EID: 84928752605     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/s12866-015-0362-3     Document Type: Article

References (41)

1. Schell MA, Karmirantzou M, Snel B, Vilanova D, Berger B, Pessi G, et al. The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc Natl Acad Sci U S A. 2002;99(22):14422-7.
2. Hentages DJ, editor. Human intestinal microflora in health and disease. New York: academic; 1983.
3. Chang DE, Smalley DJ, Tucker DL, Leatham MP, Norris WE, Stevenson SJ, et al. Carbon nutrition of Escherichia coli in the mouse intestine. Proc Natl Acad Sci U S A. 2004;101(19):7427-32.
4. Anderson KL, Salyers AA. Biochemical-evidence that the starch breakdown by Bacteriodes thetaiotaomicron involves outer-membrane starch-binding sites and repriplasmic starch-degrading enzymes. J Bacteriol. 1989;171(6):3192-8.
5. Grabitske HA, Slavin JL. Low-Digestible Carbohydrates in Practice. J Am Diet Assoc. 2008;108(10):1677-81.
6. Lattimer JM, Haub MD. Effects of Dietary Fiber and Its Components on Metabolic Health. Nutrients. 2010;2(12):1266-89.
7. Turroni F, Bottacini F, Foroni E, Mulder I, Kim J-H, Zomer A, et al. Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proc Natl Acad Sci U S A. 2010;107(45):19514-9.
8. Sela DA, Chapman J, Adeuya A, Kim JH, Chen F, Whitehead TR, et al. The genome sequence of Bifidobacterium longum subsp infantis reveals adaptations for milk utilization within the infant microbiome. Proc Natl Acad Sci U S A. 2008;105(48):18964-9.
9. El Kaoutari A, Armougom F, Gordon JI, Raoult D, Henrissat B. The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nat Rev Microbiol. 2013;11(7):497-504.
10. Zhao L, Xu W, Ibrahim SA, Jin J, Feng J, Jiang J, et al. Effects of Age and Region on Fecal Microflora in Elderly Subjects Living in Bama, Guangxi, China. Curr Microbiol. 2011;62(1):64-70.
11. Hao Y, Huang D, Guo H, Xiao M, An H, Zhao L, et al. Complete Genome Sequence of Bifidobacterium longum subsp longum BBMN68, a New Strain from a Healthy Chinese Centenarian. J Bacteriol. 2011;193(3):787-8.
12. Chi Zhang HZ, Xiaobing Du, Lei Zhang, Tongxia Zhu. Initial studies between food composition of Bamma's health macrobian and bifidobacteria in human intestinal tract. Food Sci China. 1994; 177.
13. Topping DL, Clifton PM. Short-chain fatty acids and human colonic function: Roles of resistant starch and nonstarch polysaccharides. Physiol Rev. 2001;81(3):1031-64.
14. Beck IT. Role of panceatic enzymes in digestion. Am J Clin Nutr. 1973;26(3):311-25.
15. Englyst HN, Cummings JH. Digestion of the polysaccharides of some ceral foods in the human small-intestine. Am J Clin Nutr. 1985;42(5):778-87.
16. Duranti S, Turroni F, Lugli GA, Milani C, Viappiani A, Mangifesta M, et al. Genomic Characterization and Transcriptional Studies of the Starch-Utilizing Strain Bifidobacterium adolescentis 22L. Appl Environ Microbiol. 2014;80(19):6080-90.
17. Caspi R, Foerster H, Fulcher CA, Hopkinson R, Ingraham J, Kaipa P, et al. MetaCyc: a multiorganism database of metabolic pathways and enzymes. Nucleic Acids Res. 2006;34:D511-6.
18. Motherway MOC, Fitzgerald GF, Neirynck S, Ryan S, Steidler L, van Sinderen D. Characterization of ApuB, an extracellular type II amylopullulanase from Bifidobacterium breve UCC2003. Appl Environ Microbiol. 2008;74(20):6271-9.
19. Cantarel BL, Lombard V, Henrissat B. Complex Carbohydrate Utilization by the Healthy Human Microbiome. Plos One. 2012; 7(6).
20. J-z X, Takahashi S, Nishimoto M, Odamaki T, Yaeshima T, Iwatsuki K, et al. Distribution of In Vitro Fermentation Ability of Lacto-N-Biose I, a Major Building Block of Human Milk Oligosaccharides, in Bifidobacterial Strains. Appl Environ Microbiol. 2010;76(1):54-9.
21. Leitch ECM, Walker AW, Duncan SH, Holtrop G, Flint HJ. Selective colonization of insoluble substrates by human faecal bacteria. Environ Microbiol. 2007;9(3):667-79.
22. Ryan SM, Fitzgerald GF, van Sinderen D. Screening for and identification of starch-, amylopectin-, and pullulan-degrading activities in bifidobacterial strains. Appl Environ Microbiol. 2006;72(8):5289-96.
23. Hopkins MJ, Englyst HN, Macfarlane S, Furrie E, Macfarlane GT, McBain AJ. Degradation of cross-linked and non-cross-linked arabinoxylans by the intestinal microbiota in children. Appl Environ Microbiol. 2003;69(11):6354-60.
24. Hooper LV, Midtvedt T, Gordon JI. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr. 2002;22:283-307.
25. Chassard C, Goumy V, Leclerc M, Del'homme C, Bernalier-Donadille A. Characterization of the xylan-degrading microbial community from human faeces. FEMS Microbiol Ecol. 2007;61(1):121-31.
26. Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol. 2008;6(2):121-31.
27. Motherway MOC, Zomer A, Leahy SC, Reunanen J, Bottacini F, Claesson MJ, et al. Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. Proc Natl Acad Sci U S A. 2011;108(27):11217-22.
28. Sonnenburg JL, Xu J, Leip DD, Chen CH, Westover BP, Weatherford J, et al. Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Sci. 2005;307(5717):1955-9.
29. Garrido D, Kim JH, German JB, Raybould HE, Mills DA. Oligosaccharide Binding Proteins from Bifidobacterium longum subsp infantis Reveal a Preference for Host Glycans. Plos One. 2011; 6(3).
30. Guglielmetti S, Tamagnini I, Mora D, Minuzzo M, Scarafoni A, Arioli S, et al. Implication of an outer surface lipoprotein in adhesion of Bifidobacterium bifidum to Caco-2 cells. Appl Environ Microbiol. 2008;74(15):4695-702.
31. Coppa GV, Bruni S, Morelli L, Soldi S, Gabrielli O. The first prebiotics in humans - Human milk oligosaccharides. J Clin Gastroenterol. 2004;38(6):S80-3.
32. Boehm G, Fanaro S, Moro G, Knol J, Arslanoglu S, Mosca F, et al. Prebiotic oligosaccharides in infant nutrition: effects on intestinal flora. Agro Food Industry Hi-Tech. 2004;15(5):14-6.
33. Xu J, Bjursell MK, Himrod J, Deng S, Carmichael LK, Chiang HC, et al. A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Sci. 2003;299(5615):2074-6.
34. Rakoff-Nahoum S, Coyne MJ, Comstock LE. An Ecological Network of Polysaccharide Utilization among Human Intestinal Symbionts. Curr Biol. 2014;24(1):40-9.
35. Barrangou R, Altermann E, Hutkins R, Cano R, Klaenhammer TR. Functional and comparative genomic analyses of an operon involved in fructooligosaccharide utilization by Lactobacillus acidophilus. Proc Natl Acad Sci U S A. 2003;100(15):8957-62.
36. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 2009;37(Database issue):D233-8.
37. Rey S, Acab M, Gardy JL, Laird MR, DeFays K, Lambert C, et al. PSORTdb: a protein subcellular localization database for bacteria. Nucleic Acids Res. 2005;33:D164-8.
38. Xiao M, Xu P, Zhao J, Wang Z, Zuo F, Zhang J, et al. Oxidative stress-related responses of Bifidobacterium longum subsp longum BBMN68 at the proteomic level after exposure to oxygen. Microbiology-Sgm. 2011;157:1573-88.
39. Jin J, Zhang B, Guo H, Cui J, Jiang L, Song S, et al. Mechanism Analysis of Acid Tolerance Response of Bifidobacterium longum subsp longum BBMN 68 by Gene Expression Profile Using RNA-Sequencing. PLoS One. 2012; 7(12).
40. Jin J, Liu S, Zhao L, Ge K, Mao X, Ren F. Changes in ffh, uvrA, groES and dnaK mRNA Abundance as a Function of Acid-Adaptation and Growth Phase in Bifidobacterium longum BBMN68 Isolated from Healthy Centenarians. Curr Microbiol. 2011;62(2):612-7.
41. Sonnenburg JL, Chen CTL, Gordon JI. Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host. PLoS Biol. 2006;4(12):2213-26.