Specificity of Polysaccharide Use in Intestinal Bacteroides Species Determines Diet-Induced Microbiota Alterations

Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305, USA.
Cell (Impact Factor: 32.24). 06/2010; 141(7):1241-52. DOI: 10.1016/j.cell.2010.05.005
Source: PubMed


The intestinal microbiota impacts many facets of human health and is associated with human diseases. Diet impacts microbiota composition, yet mechanisms that link dietary changes to microbiota alterations remain ill-defined. Here we elucidate the basis of Bacteroides proliferation in response to fructans, a class of fructose-based dietary polysaccharides. Structural and genetic analysis disclosed a fructose-binding, hybrid two-component signaling sensor that controls the fructan utilization locus in Bacteroides thetaiotaomicron. Gene content of this locus differs among Bacteroides species and dictates the specificity and breadth of utilizable fructans. BT1760, an extracellular beta2-6 endo-fructanase, distinguishes B. thetaiotaomicron genetically and functionally, and enables the use of the beta2-6-linked fructan levan. The genetic and functional differences between Bacteroides species are predictive of in vivo competitiveness in the presence of dietary fructans. Gene sequences that distinguish species' metabolic capacity serve as potential biomarkers in microbiomic datasets to enable rational manipulation of the microbiota via diet.

Download full-text


Available from: Susan Firbank, Sep 29, 2015
92 Reads
  • Source
    • "As such, undigested polysaccharides reach the colon and serve as a major energy source for the GM. Not surprisingly, the enzymatic capacity of any singular bacterial taxon is a major determinant of fitness within its environment (Sonnenburg et al. 2010). While this has been elegantly demonstrated on the level of individual species, diet clearly places selective pressures on the GM at higher phylogenetic levels as well. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Eukaryotic organisms are colonized by rich and dynamic communities of microbes, both internally (e.g., in the gastrointestinal and respiratory tracts) and externally (e.g., on skin and external mucosal surfaces). The vast majority of bacterial microbes reside in the lower gastrointestinal (GI) tract, and it is estimated that the gut of a healthy human is home to some 100 trillion bacteria, roughly an order of magnitude greater than the number of host somatic cells. The development of culture-independent methods to characterize the gut microbiota (GM) has spurred a renewed interest in its role in host health and disease. Indeed, associations have been identified between various changes in the composition of the GM and an extensive list of diseases, both enteric and systemic. Animal models provide a means whereby causal relationships between characteristic differences in the GM and diseases or conditions can be formally tested using genetically identical animals in highly controlled environments. Clearly, the GM and its interactions with the host and myriad environmental factors are exceedingly complex, and it is rare that a single microbial taxon associates with, much less causes, a phenotype with perfect sensitivity and specificity. Moreover, while the exact numbers are the subject of debate, it is well recognized that only a minority of gut bacteria can be successfully cultured ex vivo. Thus, to perform studies investigating causal roles of the GM in animal model phenotypes, researchers need clever techniques to experimentally manipulate the GM of animals, and several ingenious methods of doing so have been developed, each providing its own type of information and with its own set of advantages and drawbacks. The current review will focus on the various means of experimentally manipulating the GM of research animals, drawing attention to the factors that would aid a researcher in selecting an experimental approach, and with an emphasis on mice and rats, the primary model species used to evaluate the contribution of the GM to a disease phenotype. © The Author 2015. Published by Oxford University Press on behalf of the Institute for Laboratory Animal Research. All rights reserved. For permissions, please email:
    ILAR journal / National Research Council, Institute of Laboratory Animal Resources 08/2015; 56(2). DOI:10.1093/ilar/ilv021 · 2.39 Impact Factor
    • "No significant differences in GH abundances were detected between Polaribacter and other Flavobacteriaceae members (Supplementary Figure S3). Polysaccharide degradation and uptake genes in Bacteroidetes are often co-located in operon-like PULs (Sonnenburg et al., 2010). PULs comprise a characteristic gene tandem coding for a SusD-like substrate-binding protein and a TonB-dependent receptor (TBDR) together with CAZyme genes and often contain genes for transport, transcriptional regulation, peptidases and sulfatases. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Members of the flavobacterial genus Polaribacter thrive in response to North Sea spring phytoplankton blooms. We analyzed two respective Polaribacter species by whole genome sequencing, comparative genomics, substrate tests and proteomics. Both can degrade algal polysaccharides but occupy distinct niches. The liquid culture isolate Polaribacter sp. strain Hel1_33_49 has a 3.0-Mbp genome with an overall peptidase:CAZyme ratio of 1.37, four putative polysaccharide utilization loci (PULs) and features proteorhodopsin, whereas the agar plate isolate Polaribacter sp. strain Hel1_85 has a 3.9-Mbp genome with an even peptidase:CAZyme ratio, eight PULs, a mannitol dehydrogenase for decomposing algal mannitol-capped polysaccharides but no proteorhodopsin. Unlike other sequenced Polaribacter species, both isolates have larger sulfatase-rich PULs, supporting earlier assumptions that Polaribacter take part in the decomposition of sulfated polysaccharides. Both strains grow on algal laminarin and the sulfated polysaccharide chondroitin sulfate. For strain Hel1_33_49, we identified by proteomics (i) a laminarin-induced PUL, (ii) chondroitin sulfate-induced CAZymes and (iii) a chondroitin-induced operon that likely enables chondroitin sulfate recognition. These and other data suggest that strain Hel1_33_49 is a planktonic flavobacterium feeding on proteins and a small subset of algal polysaccharides, while the more versatile strain Hel1_85 can decompose a broader spectrum of polysaccharides and likely associates with algae.The ISME Journal advance online publication, 5 December 2014; doi:10.1038/ismej.2014.225.
    The ISME Journal 12/2014; 9(6). DOI:10.1038/ismej.2014.225 · 9.30 Impact Factor
  • Source
    • "The fructose-based carbohydrates are well-known to influence the intestinal microbiota, and the basis of Bacteroides spp. proliferation in response to fructose-based carbohydrates is known (Sonnenburg et al., 2010). In addition, the fructose-based carbohydrates derived from plants such as Chinese yam and Chinese bitter melon as well as JBO VS have attracted attention as prebiotic foods, and were reported to promote the growth of helpful intestinal microbiota such as Bacteroides spp. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The aim of this work was to develop a simple and rapid in vitro evaluation method for screening and discovery of uncharacterised and untapped prebiotic foods. Using a NMR-based metabolomic approach coupled with multivariate statistical analysis, the metabolic profiles generated by intestinal microbiota after in vitro incubation with feces were examined. The viscous substances of Japanese bunching onion (JBOVS) were identified as one of the candidate prebiotic foods by this in vitro screening method. The JBOVS were primarily composed of sugar components, especially fructose-based carbohydrates. Our results suggested that ingestion of JBOVS contributed to lactate and acetate production by the intestinal microbiota, and were accompanied by an increase in the Lactobacillus murinus and Bacteroidetes sp. populations in the intestine and fluctuation of the host-microbial co-metabolic process. Therefore, our approach should be useful as a rapid and simple screening tool for potential prebiotic foods.
    Food Chemistry 06/2014; 152:251–260. DOI:10.1016/j.foodchem.2013.11.126 · 3.39 Impact Factor
Show more