Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon
Xiaolei Ze, Sylvia H Duncan, Petra Louis, Harry J Flint, Xiaolei Ze, Sylvia H Duncan, Petra Louis, Harry J Flint
Abstract
The release of energy from particulate substrates such as dietary fiber and resistant starch (RS) in the human colon may depend on the presence of specialist primary degraders (or 'keystone species') within the microbial community. We have explored the roles of four dominant amylolytic bacteria found in the human colon in the degradation and utilization of resistant starches. Eubacterium rectale and Bacteroides thetaiotaomicron showed limited ability to utilize RS2- and RS3-resistant starches by comparison with Bifidobacterium adolescentis and Ruminococcus bromii. In co-culture, however, R. bromii proved unique in stimulating RS2 and RS3 utilization by the other three bacterial species, even in a medium that does not permit growth of R. bromii itself. Having previously demonstrated low RS3 fermentation in vivo in two individuals with undetectable populations of R. bromii-related bacteria, we show here that supplementation of mixed fecal bacteria from one of these volunteers with R. bromii, but not with the other three species, greatly enhanced the extent of RS3 fermentation in vitro. This argues strongly that R. bromii has a pivotal role in fermentation of RS3 in the human large intestine, and that variation in the occurrence of this species and its close relatives may be a primary cause of variable energy recovery from this important component of the diet. This work also indicates that R. bromii possesses an exceptional ability to colonize and degrade starch particles when compared with previously studied amylolytic bacteria from the human colon.
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References
- Abell GCJ, Cooke CM, Bennett CN, Conlon MA, McOrist AL. Phylotypes related to Ruminococcus bromii are abundant in the large bowel of humans and increase in response to a diet high in resistant starch. FEMS Microbiol Ecol. 2008;66:505–515.
- Aminov RI, Walker AW, Duncan SH, Harmsen HJM, Welling GW, Flint HJ. 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 Microbiol. 2006;72:6371–6376.
- Barcenilla A, Pryde SE, Martin J, Duncan SH, Stewart CS, Henderson C, et al. Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl Environ Microbiol. 2000;66:1654–1661.
- Belenguer A, Duncan SH, Calder G, Holtrop G, Louis P, Lobley GE, et al. Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Appl Environ Microbiol. 2006;72:3593–3599.
- Chassard C, Delmas E, Robert C, Lawson PA, Bernalier-Donadille A. Ruminococcus champanellensis sp.nov., a cellulose-degrading bacterium from the human gut microbiota. Int J Syst Evol Microbiol. 2011;62 (Pt 1:138–143.
- Dehority BA. Effects of microbial synergism on fibre digestion in the rumen. Proc Nutr Soc. 1991;50:149–159.
- D'Elia JN, Salyers AA. Contribution of a neopullulanase, a pullulanase, and an α-glucosidase to growth of Bacteroides thetaiotaomicron on starch. J Bacteriol. 1996;178:7173–7179.
- Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. Colorimetric method for determination of sugars and related substances. Anal Chem. 1956;28:350–356.
- Englyst HN, Kingman SM, Cummings JH. Classification and measurement of nutritionally important starch fractions. Eur J Clin Nutr. 1992;46:S33–S50.
- Ferguson LR, Tasman-Jones C, Englyst H, Harris PJ. Comparative effects of three resistant starch preparations on transit time and short-chain fatty acid production in rats. Nutr Cancer. 2000;36:230–237.
- Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nature Rev Microbiol. 2008;6:121–131.
- Herbeck JL, Bryant MP. Nutritional features of the intestinal anaerobe Ruminococcus bromii. J Appl Microbiol. 1974;28:1018–1022.
- Hsieh MK, Shyu CL, Liao JW, Franje CA, Huang YJ, Chang SK, et al. Correlation analysis of heat stability of veterinary antibiotics by structural degradation, changes in antimicrobial activity and genotoxicity. Veterinarni Medicina. 2011;56:274–285.
- Jacobasch G, Dongowski G, Schmiedl D, Müller-Schmehl K. Hydrothermal treatment of novelose 330 results in high yield of resistant starch type 3 with beneficial prebiotic properties and decreased secondary bile acid formation in rats. Br J Nutr. 2006;95:1063–1074.
- Kazimierczak KA, Rincon MT, Patterson AJ, Martin JC, Young P, Flint HJ, et al. A new tetracycline efflux gene, tet(40), is located in tandem with tet(O/32/O) in a human gut Firmicute bacterium and in metagenomic clone libraries. Antimicrob Agents Chemother. 2008;52:4001–4009.
- Kovatcheva-Datchary P, Egert M, Maathuis A, Rajilic-Stojanovic M, de Graaf AA, Smidt H, et al. Linking phylogenetic identities of bacteria to starch fermentation in an in vitro model of the large intestine by RNA-based stable isotope probing. Environ Microbiol. 2009;11:914–926.
- Lay C, Sutren M, Violaine Rochet V, Saunier K, Doré J, Rigottier-Gois L, et al. Design and validation of 16S rRNA probes to enumerate members of the Clostridium leptum subgroup in human faecal microbiota. Environ Microbiol. 2005;7:933–946.
- Leitch ECM, Walker AW, Duncan SH, Holtrop G, Flint HJ. Selective colonization of insoluble substrates by human faecal bacteria. Environ Microbiol. 2007;9:667–679.
- Le Leu RK, Brown IL, Hu Y, Bird AR, Jackson M, Esterman A, et al. A synbiotic combination of resistant starch and Bifidobacterium lactis facilitates apoptotic deletion of carcinogen-damaged dells in rat colon. J Nutr. 2005;135:996–1001.
- Le Leu RK, Hu Y, Brown IL, Young GP.2009Effect of high amylose maize starches on colonic fermentation and apoptotic response to DNA-damage in the colon of rats Nutr Metab 611doi: 10.1186/1743-7075-6-11
- Lever M. Carbohydrate determination with 4 hydroxybenzoic acid hydrazide (PAHBAH): effect of bismuth on the reaction. Anal Biochem. 1977;81:21–27.
- Macfarlane GT, Englyst HN. Starch utilization by the human large intestinal microflora. J Appl Bacteriol. 1986;60:195–201.
- MacFarlane GT, Hay S, Gibson GR. Influence of mucin on glycosidase, protease and arylamidase activities of human gut bacteria grown in a 3-stage continuous culture system. J Appl Bacteriol. 1989;66:407–417.
- Martínez I, Kim J, Duffy PR, Schlegel VL, Walter J. Resistant starches types 2 and 4 have differential effects on the composition of the fecal microbiota in human subjects. PLoS ONE. 2010;5:e15046.
- Miyazaki K, Martin JC, Marinsek-Logar R, Flint HJ. Degradation and utilization of xylans by the rumen anaerobe Prevotella bryantii (formerly P. ruminicola subsp. brevis) B14. Anaerobe. 1997;3:373–381.
- Moore WEC, Cato EP, Holdeman LV. Ruminococcus bromii sp. n and emendation of the description of Ruminococcus Sijpestein. Int J Syst Bacteriol. 1972;22:78–80.
- Moore WEC, Moore LH. Intestinal floras of populations that have a high risk of colon cancer. Appl Environ Microbiol. 1995;61:3202–3207.
- Motherway MO, Fitzgerald GF, Neirynck S, Ryan S, Steidler L, van Sinderen D, et al. Characterization of ApuB, an extracellular type II amylopullulanase from Bifidobacterium breve UCC2003. Appl Environ Microbiol. 2008;74:6271–6279.
- Niderman-Meyer O, Zeidman T, Shimoni E, Kashi Y. Mechanisms involved in governing adherence of Vibrio cholerae to granular starch. Appl Environ Microbiol. 2010;76:1034–1043.
- Ramakrishna BS, Venkataraman S, Srinivasan P, Dash P, Young GP, Binder HJ, et al. Amylase-resistant starch plus oral rehydration solution for cholera. N Engl J Med. 2000;342:308–313.
- Ramsay AG, Scott KP, Martin JC, Rincon MT, Flint HJ. Cell-associated α-amylases of butyrate-producing firmicute bacteria from the human colon. Microbiology. 2006;152:3281–3290.
- Robertson MD, Bickerton AS, Dennis AL, Vidal H, Frayn KN. Insulin-sensitizing effects of dietary resistant starch and effects on skeletal muscle and adipose tissue metabolism. Am J Clin Nutr. 2005;82:559–567.
- 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;72:5289–5296.
- Salyers AA, West SEH, Vercellotti JR, Wilkins TD. Fermentation of mucins and plant polysaccharides by anaerobic bacteria from the human colon. Appl Environ Microbiol. 1977;34:529–533.
- Stewart CS, Flint HJ, Bryant MP.1997The rumen bacteriaIn: Hobson PN, Stewart CS (eds).The Rumen Microbial Ecosystem2nd edn.Blackie Academic & Professional: London, UK; 10–72.
- Tap J, Mondot S, Levenez F, Pelletier E, Caron C, Furet JP, et al. Towards the human intestinal microbiota phylogenetic core. Environ Microbiol. 2009;11:2574–2584.
- Walker AW, Duncan SH, Harmsen HJM, Holtrop G, Welling GW, Flint HJ. The species composition of the human intestinal microbiota differs between particle-associated and liquid phase communities. Environ Microbiol. 2008;10:3275–3283.
- Walker AW, Ince J, Duncan SH, Webster LM, Holtrop G, Ze X, et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISMEJ. 2011;5:220–230.
- Young GP, Hu Y, Le Leu RK, Nyskohus L. Dietary fibre and colorectal cancer: a model for environment - gene interactions. Mol Nutr Food Res. 2005;49:571–584.
Source: PubMed