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Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis

Key Points

  • Plant polysaccharides of dietary origin are a major energy source for the dense anaerobic microbial communities that inhabit the mammalian large intestine and rumen. Microbial fermentation products, in turn, provide energy and nutrients to the host that would otherwise be unavailable.

  • Only a few species of gut microorganism have the ability to act as primary degraders of insoluble substrates, such as plant cell walls, but many others benefit from cross-feeding interactions.

  • The organization and spectrum of enzymes, substrate-binding modules and transport systems largely defines the types of substrate that can be exploited by a given gut bacterium, but only two gut anaerobes have so far been the subject of detailed functional studies.

  • In the rumen cellulolytic bacterium Ruminococcus flavefaciens (phylum Firmicutes) enzymes that are involved in the degradation of insoluble plant cell walls are organized into a cellulosome complex that is bound to the cell surface.

  • By contrast, the sequestration and breakdown of soluble starch molecules is achieved mainly in the periplasm of the Gram-negative human colonic species Bacteroides thetaiotaomicron.

  • More information from microbial genomics is needed to reveal the diversity of the systems that are involved in polysaccharide utilization, and thus the extent of the variation in these two paradigms among gut bacteria.

  • Gut bacteria are largely untapped sources of enzymes and binding domains that have potential for biotechnological application.

Abstract

The microbiota of the mammalian intestine depend largely on dietary polysaccharides as energy sources. Most of these polymers are not degradable by the host, but herbivores can derive 70% of their energy intake from microbial breakdown — a classic example of mutualism. Moreover, dietary polysaccharides that reach the human large intestine have a major impact on gut microbial ecology and health. Insight into the molecular mechanisms by which different gut bacteria use polysaccharides is, therefore, of fundamental importance. Genomic analyses of the gut microbiota could revolutionize our understanding of these mechanisms and provide new biotechnological tools for the conversion of polysaccharides, including lignocellulosic biomass, into monosaccharides.

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Figure 1: Polysaccharide-degrading bacteria in the ruminant and human gastrointestinal tracts.
Figure 2: A simplified schematic illustrating the relationships between primary degraders of insoluble plant fibre and other members of gut microbial communities.
Figure 3: The cellulosome system of Ruminococcus flavefaciens for plant cell-wall degradation.
Figure 4: The sequestration system for soluble starch in Bacteroides thetaiotaomicron.
Figure 5: The distribution in four species of anaerobic gut bacteria of selected glycoside hydrolase domains that are associated with activity against plant-derived polysaccharides and oligosaccharides.

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Acknowledgements

The Rowett Research Institute receives support from the Scottish Government Rural and Environment Research and Analysis Directorate. M.T.R. is grateful for support from the European Union FP5 project GEMINI.

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Correspondence to Harry J. Flint.

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DATABASES

Entrez Gene

susA

susB

susC

susD

susG

Entrez Genome Project

Bacteroides fragilis

Bacteroides ovatus

Bacteroides thetaiotaomicron

Clostridium leptum

Ruminococcus albus 8

FURTHER INFORMATION

Bryan A. White's homepage

Edward A. Bayer's homepage

Harry J. Flint's homepage

Raphael Lamed's homepage

CAZY (carbohydrate-active enzymes)

Glossary

Lignocellulose

A complex mixture of structural polysaccharides, mainly cellulose and hemicellulose, that has varying amounts of polyphenolic lignins, and is the main constituent of plant cell-wall material.

Inulin

A storage polysaccharide that is found in some plants and consists mainly of β-(1,2)-linked D-fructose residues. Inulin, and the shorter fructo-oligosaccharides that are derived from it, is not hydrolysed by mammalian digestive enzymes, but can be used by bacteria in the large intestine.

Resistant starch

The fraction of dietary starch that evades digestion in the upper gut of monogastric animals, notably humans, and thus becomes available for fermentation by the microbial community in the large intestine.

Hemicellulose

A cross-linking glycan that constitutes up to 30% of plant cell walls; the two major hemicelluloses are xyloglucan and glucuronoarabinoxylan.

Dockerin

A calcium-binding, modular component of cellulosomal enzymes (and other components) that is characterized by a duplicated sequence that binds to a complementary cohesin.

Cohesin

A module in the scaffoldin to which cellulosomal dockerin-containing enzymes (and/or other components) are bound. The cohesin–dockerin pairs are grouped according to sequence similarity into phylogenetically different types.

Cellulosome

An extracellular enzyme complex that consists of a scaffoldin (or scaffoldins) and cellulosomal enzymes that are dedicated to the efficient degradation of plant cell walls.

Sortase

A transpeptidase that links peptide units on separate chains of peptidoglycan. Specifically, sortases link the threonine (T) residue of the LPXTG motif (where X denotes any amino acid) to the bacterial cell wall by a transpeptidation reaction.

Scaffoldin

A structural cellulosomal subunit that comprises cohesin modules and binds dockerin-bearing enzymes (and/or other components).

Neopullulanase

An amylase that has the ability to cleave the α-(1,4) linkages in amylose (a linear α-(1,4)-linked glucose polymer), amylopectin (amylose chains joined in a branching structure by α-(1,6) linkages) and pullulan (a linear polymer of α-(1,4)- and α-(1,6)- linked glucose residues).

Extracytoplasmic function-type sigma factor

A class of sigma factor that stimulates the transcription of specific genes by RNA polymerase in response to environmental signals. Each extracytoplasmic function-type sigma factor is typically complexed with a specific membrane-bound anti-sigma factor, and becomes active only when released in response to the environmental stimulus.

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Flint, H., Bayer, E., Rincon, M. et al. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol 6, 121–131 (2008). https://doi.org/10.1038/nrmicro1817

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