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Specificity of Polysaccharide Use in Intestinal Bacteroides Species

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Specificity of Polysaccharide Use in Intestinal Bacteroides Species CORE Metadata, citation and similar papers at core.ac.uk Provided by Elsevier - Publisher Connector Specificity of Polysaccharide Use in Intestinal Bacteroides Species Determines Diet-Induced Microbiota Alterations Erica D. Sonnenburg,1,3 Hongjun Zheng,2,3 Payal Joglekar,1 Steven K. Higginbottom,1 Susan J. Firbank,2 David N. Bolam,2,* and Justin L. Sonnenburg1,* 1Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305, USA 2Institute for Cell and Molecular Biosciences, Newcastle University, Medical School, Newcastle upon Tyne, NE2 4HH, UK 3These authors contributed equally to this work *Correspondence: [email protected] (D.N.B.), [email protected] (J.L.S.) DOI 10.1016/j.cell.2010.05.005 SUMMARY tracted loss of the typical composition has been associated with several disorders including inflammatory bowel diseases The intestinal microbiota impacts many facets of (Frank et al., 2007). In addition, changes in composition have human health and is associated with human diseases. been associated with obesity and weight loss; however, factors Diet impacts microbiota composition, yet mecha- that cause these changes are not well defined (Duncan nisms that link dietary changes to microbiota alter- et al., 2008; Ley et al., 2006). The alterations in community ations remain ill-defined. Here we elucidate the basis membership, whether chronic or short-term, are accompanied of Bacteroides proliferation in response to fructans, by changes in the microbiota’s collective genome, or micro- biome, and the patterns and metabolic capabilities it specifies a class of fructose-based dietary polysaccharides. (Turnbaugh et al., 2009). Therefore, the mechanisms that link Structural and genetic analysis disclosed a fructose- relevant variables, such as changes in diet, to changes in the mi- binding, hybrid two-component signaling sensor that crobiome, are integral to understanding how environmental controls the fructan utilization locus in Bacteroides factors and behavior influence human biology. thetaiotaomicron. Gene content of this locus differs Many complex plant polysaccharides in the human diet are among Bacteroides species and dictates the speci- resistant to host-mediated degradation due to either insolubility ficity and breadth of utilizable fructans. BT1760, or lack of human-encoded hydrolytic enzymes (Flint et al., 2008; an extracellular b2-6 endo-fructanase, distinguishes Louis et al., 2007; Sonnenburg et al., 2005). These carbohy- B. thetaiotaomicron genetically and functionally, and drates are not absorbed in the upper gastrointestinal tract and enables the use of the b2-6-linked fructan levan. The serve as a major source of carbon and energy for the distal gut genetic and functional differences between Bacter- microbial community. Polysaccharide degradation is one of the core functions encoded in the microbiome (Lozupone et al., oides species are predictive of in vivo competitiveness 2008; Turnbaugh et al., 2007). Broad expansion of the genes in the presence of dietary fructans. Gene sequences and operons dedicated to degrading and consuming polysac- that distinguish species’ metabolic capacity serve as charides has occurred within the genomes of microbiota- potential biomarkers in microbiomic datasets to resident species (Xu et al., 2003, 2007), a logical outcome of enable rational manipulation of the microbiota via diet. the intense competition for these resources. It is, therefore, expected that alterations in the type and quantity of polysaccha- INTRODUCTION rides consumed can result in changes in the microbiota commu- nity composition and function. The trillions of microbial cells that reside within the intestine Inulin- and levan-type fructans (homopolymers of b2-1 or b2-6 shape aspects of host metabolism and immune function and fructose units, respectively) are common dietary plant polysac- extend the physiological definition of humans (Backhed et al., charides that feed the intestinal microbiota (Roberfroid et al., 2005; Hooper, 2009; Louis et al., 2007). While the general compo- 1993). Multiple bacterial taxa in the gut utilize fructans, including sition of the intestinal microbiota is similar in most healthy people, members of Firmicutes, Bacteroides, and Bifidobacterium, with greater than 90% of the cells belonging to the Firmicutes or (Duncan et al., 2003; Rossi et al., 2005; Van der Meulen et al., Bacteroidetes phyla (Dethlefsen et al., 2008), the species compo- 2006), and dietary fructan can result in expansion of Actinobac- sition is highly personalized (Turnbaugh et al., 2009). teria, Firmicutes, or Bacteroides (Kolida et al., 2007; Menne et al., Community membership and function of the microbiota can 2000; Ramirez-Farias et al., 2008). Lack of predictability in how change due to numerous variables including antibiotic treat- the microbiota responds to such dietary interventions reflects ment, inflammation, or changes in diet (Dethlefsen et al., 2008; our limited understanding of nutrient sensing and utilization by Frank et al., 2007; Jernberg et al., 2007; Ley et al., 2006). Pro- members of the intestinal microbiota. Cell 141, 1241–1252, June 25, 2010 ª2010 Elsevier Inc. 1241 A SusG SusF SusE SusD SusC SusB SusA SusR Figure 1. Bt’s Use of Fructose-Containing Carbohydrates Corresponds to Induction of the Polysaccharide Utilization Locus BT1757-1763 and BT1765 Bt1754 Bt1757 Bt1758 Bt1759 Bt1760 Bt1761 Bt1762 Bt1763 Bt1765 (A) Genomic organization of Bt’s Sus locus (top) and putative fructan utilization locus (bottom). HTCS SusD-like SusC-like GH32 GH32 glycoside Genes of similar function are coded by color; inter- sensor/ fructokinase Outer membrane glycoside regulator hydrolases SusE vening unrelated genes are white; genes without Inner membrane polysaccharide hydrolase positioned corresponding homologs are gray. monosaccharide binding and gene (B) Gene expression patterns of differentially regu- import import proteins lated susC and susD homologs from Bt grown in rich medium (TYG) at five time points from early C B Time (hours) log (3.5 hr) to stationary phase (8.8 hr) in duplicate. 3.5 4.5 5.5 6.5 8.8 Colors indicate standard deviations above (red) BT0317-BT0319 and below (green) a gene’s mean expression (black). BT0483/BT0484 1.5 (C) Growth curves of Bt in minimal medium con- BT1042/BT1043 Fructose BT1280/BT1281 Sucrose taining indicated carbon source at 0.5% w/v. BT1619/BT1620 1 FOS, fructo-oligosaccharide. BT1762/BT1763 FOS BT2460/BT2461 Levan (D) RNA abundance for genes relevant to fructan BT2559/BT2560 0.5 Inulin use in cells grown in different carbon sources, rela- BT2625/BT2626 tive to growth in minimal medium plus glucose. BT2805/BT2806 BT3310/BT3311 0 Standard errors of expression levels from three BT3788/BT3789 Absorbance (OD 600) 0 24 48 biological replicate cultures are shown. BT3854/BT3855 BT3958/BT3959 Time (hours) -2 -1 0 1 2 HTCS, which may mediate the rapid and D specific responses required in the 100000 dynamic nutrient environment of the intes- 10000 tine. Here, we dissect a Bt PUL required for utilization of fructans to better under- 1000 stand how Bacteroides species acquire Fructose and process this common class of dietary Sucrose Fold induction 100 FOS carbohydrates. In addition, we provide Levan evidence that the associated HTCS con- 10 Inulin trols the expression of the fructan PUL and that monomeric fructose is the acti- 1 BT1754BT1757 BT1763 BT1765 BT3082 vating signal that binds directly to the periplasmic sensor domain of the regula- tory protein. These data provide an Bacteroides, a major genera in the human microbiota, have example of a well-defined ligand for a member of this class of a widely expanded capacity to use diverse types of dietary poly- sensor regulators. saccharides (Xu et al., 2007). Much of the glycan degrading and The fructan PUL is conserved to varying extents among Bacter- import machinery within Bacteroides genomes are encoded oides species, corresponding to a range of fructan utilization within clusters of coregulated genes known as polysaccharide capability across the genus. Using model intestinal microbiotas utilization loci (PULs). B. thetaiotaomicron (Bt), a prototypic living within gnotobiotic mice, we demonstrate that dietary fructan member of the Bacteroides, possesses 88 PULs, which differ can have disparate effects on community composition, depend- in polysaccharide specificity (Martens et al., 2008). The defining ing upon the fructan degrading capacity of members of the micro- characteristic of a PUL is the presence of a pair of genes homol- biota. These studies suggest that within personal microbiomic ogous to Bt susD and susC, which encode outer membrane datasets, we will be able to identify genetic biomarkers of discrete proteins that bind and import starch oligosaccharides, respec- functions. Inference of function from these biomarkers should tively (Figure 1A) (Martens et al., 2009; Shipman et al., 2000). provide predictive power in determining how an individual’s mi- The pair of susC and susD homologs is usually associated with crobiota will respond to changes in diet and other interventions. genes that encode the machinery necessary to convert extracel- lular polysaccharides into intracellular monosaccharides, such RESULTS as glycoside hydrolases (susA, susB, and susG in Figure 1A). In addition to machinery for polysaccharide acquisition, most BT1757-BT1763 and BT1765 Form a Putative PULs contain, or are closely linked to, a gene or genes encod- Polysaccharide Utilization Locus that Is Transcribed ing an
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