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Review
, 426 (23), 3851-65

The Devil Lies in the Details: How Variations in Polysaccharide Fine-Structure Impact the Physiology and Evolution of Gut Microbes

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Review

The Devil Lies in the Details: How Variations in Polysaccharide Fine-Structure Impact the Physiology and Evolution of Gut Microbes

Eric C Martens et al. J Mol Biol.

Abstract

The critical importance of gastrointestinal microbes to digestion of dietary fiber in humans and other mammals has been appreciated for decades. Symbiotic microorganisms expand mammalian digestive physiology by providing an armament of diverse polysaccharide-degrading enzymes, which are largely absent in mammalian genomes. By out-sourcing this aspect of digestive physiology to our gut microbes, we maximize our ability to adapt to different carbohydrate nutrients on timescales as short as several hours due to the ability of the gut microbial community to rapidly alter its physiology from meal to meal. Because of their ability to pick up new traits by lateral gene transfer, our gut microbes also enable adaption over time periods as long as centuries and millennia by adjusting their gene content to reflect cultural dietary trends. Despite a vast amount of sequence-based insight into the metabolic potential of gut microbes, the specific mechanisms by which symbiotic gut microorganisms recognize and attack complex carbohydrates remain largely undefined. Here, we review the recent literature on this topic and posit that numerous, subtle variations in polysaccharides diversify the spectrum of available nutrient niches, each of which may be best filled by a subset of microorganisms that possess the corresponding proteins to recognize and degrade different carbohydrates. Understanding these relationships at precise mechanistic levels will be essential to obtain a complete understanding of the forces shaping gut microbial ecology and genomic evolution, as well as devising strategies to intentionally manipulate the composition and physiology of the gut microbial community to improve health.

Keywords: Bacteroides; lateral gene transfer; microbiome; microbiota; polysaccharide.

Figures

Figure 1
Figure 1. Polysaccharide Utilization Loci (PULs) and their substrates
(A.) The Starch Utilization System of Bacteroides thetaiotaomicron is the archetypal PUL.; (B. & C.) The B. thetaiotaomicron Fructan Utilization Locus (B.) and the B. ovatus Xyloglucan Utilization Locus (XyGUL, C.) represent two other PULs for which all of the glycoside hydrolases (GH) and several substrate-binding proteins have been biochemically characterized. (D.) A partially homologous and syntenic B. uniformis XyGUL is predicted to degrade both (arabinogalacto)xyloglucan and (fucogalacto)xyloglucan due to an “upgrade” with a predicted fucosidase from GH95. (E. & F.) The B. plebeius Porphyran Utilization Locus (E.) and the B. intestinalis Xylan Utilization Locus (F.) represent complex loci with only partially characterized enzyme complements; for some gene products, function may be broadly predicted by family membership, but exact specificities are currently unknown. Notably, the B. plebeius Porphyran Utilization Locus encodes individual enzymes with specificity for either porphyran or agarose, but is only induced by the former. (G. & H.) The Capnocytophaga canimorsus N-glycan Degradation Locus (G.) and one of several B. thetaiotaomicron mucin O-linked glycan utilization loci; (H.) represent PULs in which the GH complement does not reflect the full complexity of the substrate; complete saccharification necessarily requires the input of other loci. Gene color-coding by putative or confirmed function is as follows: Blue, GHs; Purple, SusC-like; Orange, SusD-like; Yellow, SusE-positioned (but lacking sequence similarity); Salmon, Sensor/transcriptional regulator; Red, mobile elements; Cyan, non-catalytic carbohydrate-binding; Green, other proteins with characterized homologs; Grey, unknown function. Abbreviations: glycoside hydrolase (GH), carbohydrate binding protein (CBP), carbohydrate esterase (CE), fructokinase (FruK), hexose transporter (HXT), integrase (INT), mucin protease (PRO), sulfatase (Sul). Sugars are represented by Consortium for Functional Glycomics standard symbols.
Figure 2
Figure 2. Generic models for polysaccharide acquisition by gut bacteria
(A.) Gram-negative model based on Bacteroidetes Sus-like systems showing the transition from a surveillance state to active degradation. Monosaccharides are illustrated, alone or in chains, as red circles. Key sequential steps, beginning with the first encounter with soluble or accessible polysaccharides and ending with increased expression of degradative and assimilatory machinery are noted in blue. Insets at the bottom of panel A. shows B. thetaiotaomicron cells stained with an antibody against SusD, involved in starch degradation (see text for details). (B.) Gram-positive model based on ABC transporter-based systems present in Firmicutes and Actinobacteria. Opening and closing of the cytoplasmic-membrane spanning permease allows mono- and oligosaccharide substrates that are bound by solute-binding proteins (SBPs) to be transported as ATP is hydrolyzed to ADP and inorganic phosphate. Abbreviations: glycoside hydrolase (GH), polysaccharide lyase (PL).
Figure 3
Figure 3. Sampling of Bacteroidetes conjugative transposon (cTn) diversity in sequenced genomes
(A.). A cladogram based on alignment of 501 Bacteroidetes amino acid sequences for TraJ, a conserved protein involved in bacterial conjugation. Terminal branches are color-coded based on the habitat from which the sequenced bacterial isolate was taken. Two branches in the lower left quadrant that contain tRNAlys and tRNAphe targeting cTns related to the characterized elements, which confer porphyran and fungal mannan degrading abilities to B. plebeius and B. thetaiotaomicron, are highlighted in light green and pink, respectively. Survey was from the publicly available sequence database up to May 2012 and the cladogram was constructed using clustalW. (B.) A more detailed view of the cTn sequences and their putative functions associated with tRNAlys and tRNAphe insertion sites. The precise insertion sequences corresponding to the 3′ end of each tRNA are listed; examples where a direct copy of this repeat could was located at the adjacent (right) flank of the element are indicated with an asterisk. Variable cargo gene regions are connected between different elements with gray shading to highlight the conserved location of cargo, but the different size and functions of transferred genes. The previously characterized elements from B. plebeius and B. thetaiotaomicron are highlighted with red boxes. Five other elements contain putative polysaccharide utilization loci (PULs) and are indicated by blue cargo genes. Breaks in incomplete elements (a result of gaps in draft genome assemblies) are indicated as vertical black line

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