1932

Abstract

Mammals rely entirely on symbiotic microorganisms within their digestive tract to gain energy from plant biomass that is resistant to mammalian digestive enzymes. Especially in herbivorous animals, specialized organs (the rumen, cecum, and colon) have evolved that allow highly efficient fermentation of ingested plant biomass by complex anaerobic microbial communities. We consider here the two most intensively studied, representative gut microbial communities involved in degradation of plant fiber: those of the rumen and the human large intestine. These communities are dominated by bacteria belonging to the and phyla. In , degradative capacity is largely restricted to the cell surface and involves elaborate cellulosome complexes in specialized cellulolytic species. By contrast, in the , utilization of soluble polysaccharides, encoded by gene clusters (PULs), entails outer membrane binding proteins, and degradation is largely periplasmic or intracellular. Biomass degradation involves complex interplay between these distinct groups of bacteria as well as (in the rumen) eukaryotic microorganisms.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-092412-155618
2014-09-08
2024-04-17
Loading full text...

Full text loading...

/deliver/fulltext/micro/68/1/annurev-micro-092412-155618.html?itemId=/content/journals/10.1146/annurev-micro-092412-155618&mimeType=html&fmt=ahah

Literature Cited

  1. Albersheim P, An J, Freshour G, Fuller MS, Guillen R. 1.  et al. 1994. Structure and function studies of plant cell wall polysaccharides. Biochem. Soc. Trans. 22:374–78 [Google Scholar]
  2. Aminov RI, Walker AW, Duncan SH, Harmsen HJM, Welling GW, Flint HJ. 2.  2006. Molecular diversity, cultivation, and improved detection by fluorescent in situ hybridization of a dominant group of human gut bacteria related to Roseburia spp. or Eubacterium rectale. Appl. Environ. Microb. 72:6371–6 [Google Scholar]
  3. Anderson KL, Salyers AA. 3.  1989. Biochemical evidence that starch breakdown by Bacteroides thetaiotaomicron involves outer membrane starch-binding sites and periplasmic starch-degrading enzymes. J. Bacteriol. 171:3192–98 [Google Scholar]
  4. Anderson KL, Salyers AA. 4.  1989. Genetic evidence that outer membrane binding of starch is required for starch utilization by Bacteroides thetaiotaomicron. J. Bacteriol. 171:3199–204 [Google Scholar]
  5. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T. 5.  et al. 2011. Enterotypes of the human gut microbiome. Nature 473:174–80 [Google Scholar]
  6. Bayer EA, Chanzy H, Lamed R, Shoham Y. 6.  1998. Cellulose, cellulases and cellulosomes. Curr. Opin. Struct. Biol. 8:548–57 [Google Scholar]
  7. Bayer EA, Lamed R, White BA, Flint HJ. 7.  2008. From cellulosomes to cellulosomics. Chem. Rec. 8:364–77 [Google Scholar]
  8. Bayer EA, Morag E, Lamed R. 8.  1994. The cellulosome—a treasure-trove for biotechnology. Trends Biotechnol. 12:379–86 [Google Scholar]
  9. Bayer EA, Shoham Y, Lamed R. 9.  2000. Cellulose-decomposing bacteria and their enzyme systems. The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community M Dworkin, S Falkow, E Rosenberg, K-H Schleifer, E Stackebrandt New York: Springer-Verlag [Google Scholar]
  10. Bayer EA, Shoham Y, Lamed R. 10.  2013. Lignocellulose-decomposing bacteria and their enzyme systems. The Prokaryotes E Rosenberg 216–66 Berlin: Springer-Verlag [Google Scholar]
  11. Beguin P, Aubert JP. 11.  1994. The biological degradation of cellulose. FEMS Microbiol. Rev. 13:25–58 [Google Scholar]
  12. Ben-David Y. 12.  2013. Characterization of the cellulosome systems of two related human-gut bacteria Ruminococcus champanellensis and Ruminococcus bromii. Master's thesis, Weizmann Inst. Sci., Rehovot, Israel
  13. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ. 13.  2004. Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem. J. 382:769–81 [Google Scholar]
  14. Borneman WS, Ljungdahl LG, Hartley RD, Akin DE. 14.  1992. Purification and partial characterization of two feruloyl esterases from the anaerobic fungus Neocallimastix strain MC-2. Appl. Environ. Microbiol. 58:3762–66 [Google Scholar]
  15. Bowman BH, Taylor JW, Brownlee AG, Lee J, Lu SD, White TJ. 15.  1992. Molecular evolution of the fungi: relationship of the Basidiomycetes, Ascomycetes, and Chytridiomycetes. Mol. Biol. Evol. 9:285–96 [Google Scholar]
  16. Brookman JL, Ozkose E, Rogers S, Trinci APJ, Theodorou MK. 16.  2000. Identification of spores in the polycentric anaerobic gut fungi which enhance their ability to survive. FEMS Microbiol. Ecol. 31:261–67 [Google Scholar]
  17. Cameron EA, Maynard MA, Smith CJ, Smith TJ, Koropatkin NM, Martens EC. 17.  2012. Multidomain carbohydrate-binding proteins involved in Bacteroides thetaiotaomicron starch metabolism. J. Biol. Chem. 287:34614–25 [Google Scholar]
  18. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. 18.  2009. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37:D233–38 [Google Scholar]
  19. Chassard C, Delmas E, Robert C, Bernalier-Donadille A. 19.  2010. The cellulose-degrading microbial community of the human gut varies according to the presence or absence of methanogens. FEMS Microbiol. Ecol. 74:205–13 [Google Scholar]
  20. Chassard C, Goumy V, Leclerc M, Del’homme C, Bernalier-Donadille A. 20.  2007. Characterization of the xylan-degrading microbial community from human faeces. FEMS Microbiol. Ecol. 61:121–31 [Google Scholar]
  21. Cummings JH, Macfarlane GT. 21.  1991. The control and consequences of bacterial fermentation in the human colon. J. Appl. Bacteriol. 70:443–59 [Google Scholar]
  22. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB. 22.  et al. 2010. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. USA 107:14691–96 [Google Scholar]
  23. Demeyer DI. 23.  1981. Rumen microbes and digestion of plant cell walls. Agric. Environ. 6:295–337 [Google Scholar]
  24. Devillard E, Bera-Maillet C, Flint HJ, Scott KP, Newbold CJ. 24.  et al. 2003. Characterisation of XYN10B, a modular xylanase from the ruminal protozoan Polyplastron multivesiculatum, with a family 22 carbohydrate-binding module that binds to cellulose. Biochem. J. 373:495–503 [Google Scholar]
  25. Ding SY, Rincon MT, Lamed R, Martin JC, McCrae SI. 25.  et al. 2001. Cellulosomal scaffoldin-like proteins from Ruminococcus flavefaciens. J. Bacteriol. 183:1945–53 [Google Scholar]
  26. Dodd D, Mackie RI, Cann IK. 26.  2011. Xylan degradation, a metabolic property shared by rumen and human colonic Bacteroidetes. Mol. Microbiol. 79:292–304 [Google Scholar]
  27. Dodd D, Moon YH, Swaminathan K, Mackie RI, Cann IK. 27.  2010. Transcriptomic analyses of xylan degradation by Prevotella bryantii and insights into energy acquisition by xylanolytic Bacteroidetes. J. Biol. Chem. 285:30261–73 [Google Scholar]
  28. Duncan SH, Belenguer A, Holtrop G, Johnstone AM, Flint HJ, Lobley GE. 28.  2007. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl. Environ. Microbiol. 73:1073–78 [Google Scholar]
  29. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L. 29.  et al. 2005. Diversity of the human intestinal microbial flora. Science 308:1635–38 [Google Scholar]
  30. El Kaoutari A, Armougom F, Gordon JI, Raoult D, Henrissat B. 30.  2013. The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nat. Rev. Microbiol. 11:497–504 [Google Scholar]
  31. Ezer A, Matalon E, Jindou S, Borovok I, Atamna N. 31.  et al. 2008. Cell surface enzyme attachment is mediated by family 37 carbohydrate-binding modules, unique to Ruminococcus albus. J. Bacteriol. 190:8220–22 [Google Scholar]
  32. Fillingham IJ, Kroon PA, Williamson G, Gilbert HJ, Hazlewood GP. 32.  1999. A modular cinnamoyl ester hydrolase from the anaerobic fungus Piromyces equi acts synergistically with xylanase and is part of a multiprotein cellulose-binding cellulase-hemicellulase complex. Biochem. J. 343:215–24 [Google Scholar]
  33. Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA. 33.  2008. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nature Rev. Microbiol 6:121–31 [Google Scholar]
  34. Flint HJ, Forsberg CW. 34.  1995. Polysaccharide degradation in the rumen: biochemistry and genetics. Ruminant Physiology: Digestion, Metabolism, Growth and Reproduction: Proceedings of the Eighth International Symposium on Ruminant Physiology WV Engelhardt, S Leonard-Marek, G Breves, D Giesecke 43–70 Stuttgart, Ger.: Ferdinand Enke Verlag
  35. Flint HJ, Martin J, McPherson CA, Daniel AS, Zhang J-X. 35.  1993. A bifunctional enzyme, with separate xylanase and β(1,3-1,4)-glucanase domains, encoded by the xynD gene of Ruminococcus flavefaciens. J. Bacteriol. 175:2943–51 [Google Scholar]
  36. Flint HJ, Scott KP, Duncan SH, Louis P, Forano E. 36.  2012. Microbial degradation of complex carbohydrates in the gut. Gut Microbes 3:289–306 [Google Scholar]
  37. Flint HJ, Scott KP, Louis P, Duncan SH. 37.  2012. The role of the gut microbiota in nutrition and health. Nat. Rev. Gastroenterol. Hepatol. 9:577–89 [Google Scholar]
  38. Flint HJ, Whitehead TR, Martin JC, Gasparic A. 38.  1997. Interrupted catalytic domain structures in xylanases from two distantly related strains of Prevotella ruminicola. Bba-Protein Struct. M 1337:161–5 [Google Scholar]
  39. Garcia-Vallve S, Romeu A, Palau J. 39.  2000. Horizontal gene transfer of glycosyl hydrolases of the rumen fungi. Mol. Biol. Evol. 17:352–61 [Google Scholar]
  40. Gasparic A, Martin J, Daniel AS, Flint HJ. 40.  1995. A xylan hydrolase gene cluster in Prevotella ruminicola B14: sequence relationships, synergistic interactions, and oxygen sensitivity of a novel enzyme with exoxylanase and β-(1,4)-xylosidase activities. Appl. Environ. Microbiol. 61:2958–64 [Google Scholar]
  41. Gilbert HJ, Knox JP, Boraston AB. 41.  2013. Advances in understanding the molecular basis of plant cell wall polysaccharide recognition by carbohydrate-binding modules. Curr. Opin. Struct. Biol. 23:669–77 [Google Scholar]
  42. Goldenfeld N, Woese C. 42.  2007. Biology's next revolution. Nature 445:369 [Google Scholar]
  43. Henrissat B, Davies G. 43.  1997. Structural and sequence-based classification of glycoside hydrolases. Curr. Opin. Struct. Biol. 7:637–44 [Google Scholar]
  44. Hespell RB. 44.  1981. Ruminal microorganisms—their significance and nutritional value. Dev. Indust. Microbiol. 22:261–75 [Google Scholar]
  45. Himmel ME, Xu Q, Luo Y, Lamed R, Bayer EA. 45.  2010. Microbial enzyme systems for biomass conversion: emerging paradigms. Biofuels 1:323–41 [Google Scholar]
  46. Holdeman LV, Good IJ, Moore WEC. 46.  1976. Human fecal flora: variation in bacterial composition within individuals and a possible effect of emotional stress. Appl. Environ. Microbiol. 31:359–75 [Google Scholar]
  47. Jalak J, Kurasin M, Teugjas H, Valjamae P. 47.  2012. Endo-exo synergism in cellulose hydrolysis revisited. J. Biol. Chem. 287:28802–15 [Google Scholar]
  48. Jindou S, Borovok I, Rincon MT, Flint HJ, Antonopoulos DA. 48.  et al. 2006. Conservation and divergence in cellulosome architecture between two strains of Ruminococcus flavefaciens. J. Bacteriol. 188:7971–76 [Google Scholar]
  49. Kahel-Raifer H, Jindou S, Bahari L, Nataf Y, Shoham Y. 49.  et al. 2010. The unique set of putative membrane-associated anti-σ factors in Clostridium thermocellum suggests a novel extracellular carbohydrate-sensing mechanism involved in gene regulation. FEMS Microbiol. Lett. 308:84–93 [Google Scholar]
  50. Kang SH, Barak Y, Lamed R, Bayer EA, Morrison M. 50.  2006. The functional repertoire of prokaryote cellulosomes includes the serpin superfamily of serine proteinase inhibitors. Mol. Microbiol. 60:1344–54 [Google Scholar]
  51. Keegstra K, Talmadge KW, Bauer WD, Albersheim P. 51.  1973. The structure of plant cell walls III: a model of the walls of suspension-cultured sycamore cells based on the interconnections of the macromolecular components. Plant Physiol. 51:188–97 [Google Scholar]
  52. Klemm D, Heublein B, Fink HP, Bohn A. 52.  2005. Cellulose: fascinating biopolymer and sustainable raw material. Angew. Chem. Int. Ed. 44:3358–93 [Google Scholar]
  53. Klieve AV, Swain RA. 53.  1993. Estimation of ruminal bacteriophage numbers by pulsed-field gel electrophoresis and laser densitometry. Appl. Environ. Microbiol. 59:2299–303 [Google Scholar]
  54. Koropatkin NM, Cameron EA, Martens EC. 54.  2012. How glycan metabolism shapes the human gut microbiota. Nat. Rev. Microbiol. 10:323–35 [Google Scholar]
  55. Koropatkin NM, Martens EC, Gordon JI, Smith TJ. 55.  2008. Starch catabolism by a prominent human gut symbiont is directed by the recognition of amylose helices. Structure 16:1105–15 [Google Scholar]
  56. Leitch ECM, Walker AW, Duncan SH, Holtrop G, Flint HJ. 56.  2007. Selective colonization of insoluble substrates by human faecal bacteria. Environ. Microbiol. 9:667–79 [Google Scholar]
  57. Lodish H, Berk A, Zipursky SL, Matsudaira P, Baltimore D, Darnell J. 57.  2000. Molecular Cell Biology New York: WH Freeman, 4th ed..
  58. Lopez-Siles M, Khan TM, Duncan SH, Harmsen HJM, Garcia-Gil LJ. 58.  et al. 2012. Cultured representatives of two major phylogroups of human colonic Faecalibacterium prausnitzii can utilize pectin, uronic acids, and host-derived substrate for growth. Appl. Environ. Microbiol. 78:420–28 [Google Scholar]
  59. Martens EC, Chiang HC, Gordon JI. 59.  2008. Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 4:447–57 [Google Scholar]
  60. Martens EC, Koropatkin NM, Smith TJ, Gordon JI. 60.  2009. Complex glycan catabolism by the human gut microbiota: the Bacteroidetes Sus-like paradigm. J. Biol. Chem. 284:24673–77 [Google Scholar]
  61. Martens EC, Lowe EC, Chiang H, Pudlo NA, Wu M. 61.  et al. 2011. Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLoS Biol. 9:e1001221 [Google Scholar]
  62. Martinez I, Kim J, Duffy PR, Schlegel VL, Walter J. 62.  2010. Resistant starches Types 2 and 4 have differential effects on the composition of the fecal microbiota in human subjects. PLoS ONE 5:e15046 [Google Scholar]
  63. Martinez I, Lattimer JM, Hubach KL, Case JA, Yang JY. 63.  et al. 2013. Gut microbiome composition is linked to whole grain-induced immunological improvements. ISME J. 7:269–80 [Google Scholar]
  64. McNulty NP, Wu M, Erickson AR, Pan CL, Erickson BK. 64.  et al. 2013. Effects of diet on resource utilization by a model human gut microbiota containing Bacteroides cellulosilyticus WH2, a symbiont with an extensive glycobiome. PLoS Biol. 11:e1001637 [Google Scholar]
  65. Miller MEB, Antonopoulos DA, Rincon MT, Band M, Bari A. 65.  et al. 2009. Diversity and strain specificity of plant cell wall degrading enzymes revealed by the draft genome of Ruminococcus flavefaciens FD-1. PLoS ONE 4:e6650 [Google Scholar]
  66. Mirande C, Kadlecikova E, Matulova M, Capek P, Bernalier-Donadille A. 66.  et al. 2010. Dietary fibre degradation and fermentation by two xylanolytic bacteria Bacteroides xylanisolvens XB1AT and Roseburia intestinalis XB6B4 from the human intestine. J. Appl. Microbiol. 109:451–60 [Google Scholar]
  67. Mirande C, Mosoni P, Bera-Maillet C, Bernalier-Donadille A, Forano E. 67.  2010. Characterization of Xyn10A, a highly active xylanase from the human gut bacterium Bacteroides xylanisolvens XB1A. Appl. Microbiol. Biol. 87:2097–105 [Google Scholar]
  68. Miyazaki K, Martin JC, Marinsek-Logar R, Flint HJ. 68.  1997. Degradation and utilization of xylans by the rumen anaerobe Prevotella bryantii (formerly P. ruminicola subsp brevis) β14. Anaerobe 3:373–81 [Google Scholar]
  69. Miyazaki K, Miyamoto H, Mercer DK, Hirase T, Martin JC. 69.  et al. 2003. Involvement of the multidomain regulatory protein XynR in positive control of xylanase gene expression in the ruminal anaerobe Prevotella bryantii B14. J. Bacteriol. 185:2219–26 [Google Scholar]
  70. Mohnen D. 70.  2008. Pectin structure and biosynthesis. Curr. Opin. Plant Biol. 11:266–77 [Google Scholar]
  71. Motherway MO, Fitzgerald GF, Neirynck S, Ryan S, Steidler L, Van Sinderen D. 71.  2008. Characterization of ApuB, an extracellular type II amylopullulanase from Bifidobacterium breve UCC2003. Appl. Environ. Microb. 74:6271–9 [Google Scholar]
  72. Ohara H, Karita S, Kimura T, Sakka K, Ohmiya K. 72.  2000. Characterization of the cellulolytic complex (cellulosome) from Ruminococcus albus. Biosci. Biotech. Biochem. 64:254–60 [Google Scholar]
  73. Orpin CG. 73.  1983. The role of ciliate protozoa and fungi in the rumen digestion of plant cell walls. Anim. Feed Sci. Technol. 10:121–43 [Google Scholar]
  74. Parra R. 74.  1978. Comparison of foregut and hindgut fermentation in herbivores. The Ecology of Arboreal Folivores GG Montgomery 205–29 Washington, DC: Smithson. Inst. [Google Scholar]
  75. Purushe J, Fouts DE, Morrison M, White BA, Mackie RI. 75.  et al. 2010. Comparative genome analysis of Prevotella ruminicola and Prevotella bryantii: insights into their environmental niche. Microb. Ecol. 60:721–29 [Google Scholar]
  76. Qi M, Jun HS, Forsberg CW. 76.  2008. Cel9D, an atypical 1,4-β-D-glucan glucohydrolase from Fibrobacter succinogenes: characteristics, catalytic residues, and synergistic interactions with other cellulases. J. Bacteriol. 190:1976–84 [Google Scholar]
  77. Qi M, Wang P, O’Toole N, Barboza PS, Ungerfeld E. 77.  et al. 2011. Snapshot of the eukaryotic gene expression in muskoxen rumen—a metatranscriptomic approach. PLoS One 6:e20521 [Google Scholar]
  78. Rakotoarivonina H, Larson MA, Morrison M, Girardeau JP, Gaillard-Martinie B. 78.  et al. 2005. The Ruminococcus albus pilA1-pilA2 locus: expression and putative role of two adjacent pil genes in pilus formation and bacterial adhesion to cellulose. Microbiology 151:1291–99 [Google Scholar]
  79. Ramsay AG, Scott KP, Martin JC, Rincon MT, Flint HJ. 79.  2006. Cell-associated α-amylases of butyrate-producing Firmicute bacteria from the human colon. Microbiology 152:3281–90 [Google Scholar]
  80. Reeves AR, Wang GR, Salyers AA. 80.  1997. Characterization of four outer membrane proteins that play a role in utilization of starch by Bacteroides thetaiotaomicron. J. Bacteriol. 179:643–9 [Google Scholar]
  81. Rincon MT, Cepeljnik T, Martin JC, Barak Y, Lamed R. 81.  et al. 2007. A novel cell surface-anchored cellulose-binding protein encoded by the sca gene cluster of Ruminococcus flavefaciens. J. Bacteriol. 189:4774–83 [Google Scholar]
  82. Rincon MT, Cepeljnik T, Martin JC, Lamed R, Barak Y. 82.  et al. 2005. Unconventional mode of attachment of the Ruminococcus flavefaciens cellulosome to the cell surface. J. Bacteriol. 187:7569–78 [Google Scholar]
  83. Rincon MT, Dassa B, Flint HJ, Travis AJ, Jindou S. 83.  et al. 2010. Abundance and diversity of dockerin-containing proteins in the fiber-degrading rumen bacterium, Ruminococcus flavefaciens FD-1. PLoS ONE 5:e12476 [Google Scholar]
  84. Rincon MT, Martin JC, Aurilia V, McCrae SI, Rucklidge GJ. 84.  et al. 2004. ScaC, an adaptor protein carrying a novel cohesin that expands the dockerin-binding repertoire of the Ruminococcus flavefaciens 17 cellulosome. J. Bacteriol. 186:2576–85 [Google Scholar]
  85. Rincon MT, McCrae SI, Kirby J, Scott KP, Flint HJ. 85.  2001. EndB, a multidomain family 44 cellulase from Ruminococcus flavefaciens 17, binds to cellulose via a novel cellulose-binding module and to another R. flavefaciens protein via a dockerin domain. Appl. Environ. Microbiol. 67:4426–31 [Google Scholar]
  86. Robert C, Bernalier-Donadille A. 86.  2003. The cellulolytic microflora of the human colon: evidence of microcrystalline cellulose-degrading bacteria in methane-excreting subjects. FEMS Microbiol. Ecol. 46:81–89 [Google Scholar]
  87. Robert C, Chassard C, Lawson PA, Bernalier-Donadille A. 87.  2007. Bacteroides cellulosilyticus sp. nov., a cellulolytic bacterium from the human gut microbial community. Int. J. Syst. Evol. Microbiol. 57:1516–20 [Google Scholar]
  88. Robinson IM, Allison MJ, Bucklin JA. 88.  1981. Characterization of the cecal bacteria of normal pigs. Appl. Environ. Microbiol. 41:950–55 [Google Scholar]
  89. Ryan SM, Fitzgerald GF, van Sinderen D. 89.  2006. Screening for and identification of starch-, amylopectin-, and pullulan-degrading activities in bifidobacterial strains. Appl. Environ. Microbiol. 72:5289–96 [Google Scholar]
  90. Salyers AA, Vercellotti JR, West SEH, Wilkins TD. 90.  1977. Fermentation of mucin and plant polysaccharides by strains of Bacteroides from human colon. Appl. Environ. Microbiol. 33:319–22 [Google Scholar]
  91. Schwarz WH. 91.  2001. The cellulosome and cellulose degradation by anaerobic bacteria. Appl. Microbiol. Biotechnol. 56:634–49 [Google Scholar]
  92. Scott KP, Martin JC, Chassard C, Clerget M, Potrykus J. 92.  et al. 2011. Substrate-driven gene expression in Roseburia inulinivorans: importance of inducible enzymes in the utilization of inulin and starch. Proc. Natl. Acad. Sci. USA 108:4672–79 [Google Scholar]
  93. Scott KP, Martin JC, Duncan SH, Flint HJ. 93.  2013. Prebiotic stimulation of human colonic butyrate-producing bacteria and bifidobacteria, in vitro. FEMS Microbiol. Ecol. 87:30–40 [Google Scholar]
  94. Shipman JA, Cho KH, Siegel HA, Salyers AA. 94.  1999. Physiological characterization of SusG, an outer membrane protein essential for starch utilization by Bacteroides thetaiotaomicron. J. Bacteriol. 181:7206–11 [Google Scholar]
  95. Slavin JL, Brauer PM, Marlett JA. 95.  1981. Neutral detergent fiber, hemicellulose and cellulose digestibility in human subjects. J. Nutr. 111:287–97 [Google Scholar]
  96. Sonnenburg ED, Sonnenburg JL, Manchester JK, Hansen EE, Chiang HC, Gordon JI. 96.  2006. A hybrid two-component system protein of a prominent human gut symbiont couples glycan sensing in vivo to carbohydrate metabolism. Proc. Natl. Acad. Sci. USA 103:8834–39 [Google Scholar]
  97. Sonnenburg JL, Xu J, Leip DD, Chen CH, Westover BP. 97.  et al. 2005. Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307:1955–59 [Google Scholar]
  98. Suen G, Stevenson DM, Bruce DC, Chertkov O, Copeland A. 98.  et al. 2011. Complete genome of the cellulolytic ruminal bacterium Ruminococcus albus 7. J. Bacteriol. 193:5574–75 [Google Scholar]
  99. Suen G, Weimer PJ, Stevenson DM, Aylward FO, Boyum J. 99.  et al. 2011. The complete genome sequence of Fibrobacter succinogenes S85 reveals a cellulolytic and metabolic specialist. PLoS ONE 6:e18814 [Google Scholar]
  100. Van Gylswyk NO. 100.  1990. Enumeration and presumptive identification of some functional groups of bacteria in the rumen of dairy cows fed grass silage-based diets. FEMS Microbiol. Lett. 73:243–53 [Google Scholar]
  101. Van Soest PJ. 101.  1994. Nutritional Ecology of the Ruminant Ithaca, NY: Cornell Univ. Press
  102. Veira DM. 102.  1986. The role of ciliate protozoa in nutrition of the ruminant. J. Anim. Sci. 63:1547–60 [Google Scholar]
  103. Vodovnik M, Duncan SH, Reid MD, Cantlay L, Turner K. 103.  et al. 2013. Expression of cellulosome components and type IV pili within the extracellular proteome of Ruminococcus flavefaciens 007. PLoS ONE 8:e65333 [Google Scholar]
  104. Walker AW, Duncan SH, Harmsen HJ, Holtrop G, Welling GW, Flint HJ. 104.  2008. The species composition of the human intestinal microbiota differs between particle-associated and liquid phase communities. Environ. Microbiol. 10:3275–83 [Google Scholar]
  105. Walker AW, Ince J, Duncan SH, Webster LM, Holtrop G. 105.  et al. 2011. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 5:220–30 [Google Scholar]
  106. Weaver J, Whitehead TR, Cotta MA, Valentine PC, Salyers AA. 106.  1992. Genetic analysis of a locus on the Bacteroides ovatus chromosome which contains xylan utilization genes. Appl. Environ. Microbiol. 58:2764–70 [Google Scholar]
  107. Wegmann U, Louis P, Goesmann A, Henrissat B, Duncan SH, Flint HJ. 107.  2013. Complete genome of a new Firmicutes species belonging to the dominant human colonic microbiota (‘Ruminococcus bicirculans’) reveals two chromosomes and a selective capacity to utilize plant glucans. Environ. Microbiol. In press. doi: 10.1111/1462-2920.12217
  108. Williams AG. 108.  1986. Rumen holotrich ciliate protozoa. Microbiol. Rev. 50:25–49 [Google Scholar]
  109. Wilson DB, Kostylev M. 109.  2012. Cellulase processivity. Meth. Mol. Biol. 908:93–99 [Google Scholar]
  110. Woese CR, Goldenfeld N. 110.  2009. How the microbial world saved evolution from the scylla of molecular biology and the charybdis of the modern synthesis. Microbiol. Mol. Biol. Rev. 73:14–21 [Google Scholar]
  111. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY. 111.  et al. 2011. Linking long-term dietary patterns with gut microbial enterotypes. Science 334:105–8 [Google Scholar]
  112. Xu Q, Luo Y, Ding S-Y, Lamed R, Bayer EA, Himmel ME. 112.  2011. Multifunctional enzyme systems for plant cell wall degradation. Comprehensive Biotechnology M Moo-Young, M Butler, C Webb, A Moreira, F Bai 15–25 Amsterdam: Elsevier [Google Scholar]
  113. Xu Q, Morrison M, Nelson KE, Bayer EA, Atamna N, Lamed R. 113.  2004. A novel family of carbohydrate-binding modules identified with Ruminococcus albus proteins. FEBS Lett. 566:11–16 [Google Scholar]
  114. Yoshida S, Mackie RI, Cann IK. 114.  2010. Biochemical and domain analyses of FSUAxe6B, a modular acetyl xylan esterase, identify a unique carbohydrate binding module in Fibrobacter succinogenes S85. J. Bacteriol. 192:483–93 [Google Scholar]
  115. Ze X. 115.  2013. Degradation and utilization of resistant starch by microbiota in the human large intestine PhD thesis, University of Aberdeen, Aberdeen, Scotl.
  116. Ze X, Duncan SH, Louis P, Flint HJ. 116.  2012. Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon. ISME J. 6:1535–43 [Google Scholar]
  117. Ze X, Le Mougen F, Duncan SH, Louis P, Flint HJ. 117.  2013. Some are more equal than others: the role of “keystone” species in the degradation of recalcitrant substrates. Gut Microbes 4:236–40 [Google Scholar]
/content/journals/10.1146/annurev-micro-092412-155618
Loading
/content/journals/10.1146/annurev-micro-092412-155618
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error