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Glycan complexity dictates microbial resource allocation in the large intestine.

Rogowski A, Briggs JA, Mortimer JC, Tryfona T, Terrapon N, Lowe EC, Baslé A, Morland C, Day AM, Zheng H, Rogers TE, Thompson P, Hawkins AR, Yadav MP, Henrissat B, Martens EC, Dupree P, Gilbert HJ, Bolam DN - Nat Commun (2015)

Bottom Line: We show here, using xylan as a model, that sharing the breakdown products of complex carbohydrates by key members of the microbiota, such as Bacteroides ovatus, is dependent on the complexity of the target glycan.Characterization of the extensive xylan degrading apparatus expressed by B. ovatus reveals that the breakdown of the polysaccharide by the human gut microbiota is significantly more complex than previous models suggested, which were based on the deconstruction of xylans containing limited monosaccharide side chains.Our report presents a highly complex and dynamic xylan degrading apparatus that is fine-tuned to recognize the different forms of the polysaccharide presented to the human gut microbiota.

View Article: PubMed Central - PubMed

Affiliation: Institute for Cell and Molecular Biosciences, The Medical School, Newcastle University, Newcastle upon Tyne NE2 4HH, UK.

ABSTRACT
The structure of the human gut microbiota is controlled primarily through the degradation of complex dietary carbohydrates, but the extent to which carbohydrate breakdown products are shared between members of the microbiota is unclear. We show here, using xylan as a model, that sharing the breakdown products of complex carbohydrates by key members of the microbiota, such as Bacteroides ovatus, is dependent on the complexity of the target glycan. Characterization of the extensive xylan degrading apparatus expressed by B. ovatus reveals that the breakdown of the polysaccharide by the human gut microbiota is significantly more complex than previous models suggested, which were based on the deconstruction of xylans containing limited monosaccharide side chains. Our report presents a highly complex and dynamic xylan degrading apparatus that is fine-tuned to recognize the different forms of the polysaccharide presented to the human gut microbiota.

No MeSH data available.


Related in: MedlinePlus

Growth profile of wild type and mutants of B. ovatus on xylans.WT and PUL deletion mutants were cultured in minimal media containing different xylans at 0.5% (w/v) as the sole carbon source. Birchwood glucuronoxylan (BGX; (a)) and wheat arabinoxylan (WAX; (b)) are relatively simple, sparsely decorated structures, while corn (c), sorghum (d) and rice (e) xylans are more complex heavily decorated glucuronoarabinoxylans (GAXs). The high starting OD for BGX is due to the background turbidity of the polysaccharide. A total of 6 replicate cultures were monitored at 20 min intervals for each substrate and used to generate the average growth curves shown.
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f6: Growth profile of wild type and mutants of B. ovatus on xylans.WT and PUL deletion mutants were cultured in minimal media containing different xylans at 0.5% (w/v) as the sole carbon source. Birchwood glucuronoxylan (BGX; (a)) and wheat arabinoxylan (WAX; (b)) are relatively simple, sparsely decorated structures, while corn (c), sorghum (d) and rice (e) xylans are more complex heavily decorated glucuronoarabinoxylans (GAXs). The high starting OD for BGX is due to the background turbidity of the polysaccharide. A total of 6 replicate cultures were monitored at 20 min intervals for each substrate and used to generate the average growth curves shown.

Mentions: The role of PUL-XylS and PUL-XylL in xylan degradation is illustrated by the growth profiles of mutant strains. Deletion of PUL-XylS (ΔPUL-XylS) did not influence the growth of B. ovatus on complex xylans (GAXs) from corn, rice and sorghum, but prevented growth on simpler xylans (BGX or WAX) (Fig. 6). By contrast, inactivation of PUL-XylL (ΔPUL-XylL) prevented growth on the three complex GAXs but did not significantly affect the utilization of simpler BGX or WAX (Fig. 6). The somewhat higher final density observed for the wild-type bacterium on WAX vs ΔPUL-XylL is likely due to the inability of this mutant to remove the arabinose decorations from this substrate. The growth profile of the mutants are consistent with the biochemical data presented above showing that PUL-XylL encodes the only endo-acting enzyme (GH98) able to cleave the backbone of CX (and likely other complex GAXs), a prerequisite for the utilization of these polysaccharides (see below). Similarly, the inability of the PUL-XylS mutant to utilize simple xylans such as GXs and AXs, where the xylan backbone is the major component, is consistent with the locus encoding the key endo-acting surface GH10 (BACOVA_04390) that hydrolyses the backbone of sparsely decorated xylans. It is somewhat surprising, however, that ΔPUL-XylS is able to efficiently utilize GAX even though the mutant is unable to fully depolymerize the xylan backbone. This likely reflects the extensive side chains present in CX and other complex GAXs, where the xylose backbone constitutes only a relatively minor component of the total monosaccharide units in these polysaccharides.


Glycan complexity dictates microbial resource allocation in the large intestine.

Rogowski A, Briggs JA, Mortimer JC, Tryfona T, Terrapon N, Lowe EC, Baslé A, Morland C, Day AM, Zheng H, Rogers TE, Thompson P, Hawkins AR, Yadav MP, Henrissat B, Martens EC, Dupree P, Gilbert HJ, Bolam DN - Nat Commun (2015)

Growth profile of wild type and mutants of B. ovatus on xylans.WT and PUL deletion mutants were cultured in minimal media containing different xylans at 0.5% (w/v) as the sole carbon source. Birchwood glucuronoxylan (BGX; (a)) and wheat arabinoxylan (WAX; (b)) are relatively simple, sparsely decorated structures, while corn (c), sorghum (d) and rice (e) xylans are more complex heavily decorated glucuronoarabinoxylans (GAXs). The high starting OD for BGX is due to the background turbidity of the polysaccharide. A total of 6 replicate cultures were monitored at 20 min intervals for each substrate and used to generate the average growth curves shown.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4491172&req=5

f6: Growth profile of wild type and mutants of B. ovatus on xylans.WT and PUL deletion mutants were cultured in minimal media containing different xylans at 0.5% (w/v) as the sole carbon source. Birchwood glucuronoxylan (BGX; (a)) and wheat arabinoxylan (WAX; (b)) are relatively simple, sparsely decorated structures, while corn (c), sorghum (d) and rice (e) xylans are more complex heavily decorated glucuronoarabinoxylans (GAXs). The high starting OD for BGX is due to the background turbidity of the polysaccharide. A total of 6 replicate cultures were monitored at 20 min intervals for each substrate and used to generate the average growth curves shown.
Mentions: The role of PUL-XylS and PUL-XylL in xylan degradation is illustrated by the growth profiles of mutant strains. Deletion of PUL-XylS (ΔPUL-XylS) did not influence the growth of B. ovatus on complex xylans (GAXs) from corn, rice and sorghum, but prevented growth on simpler xylans (BGX or WAX) (Fig. 6). By contrast, inactivation of PUL-XylL (ΔPUL-XylL) prevented growth on the three complex GAXs but did not significantly affect the utilization of simpler BGX or WAX (Fig. 6). The somewhat higher final density observed for the wild-type bacterium on WAX vs ΔPUL-XylL is likely due to the inability of this mutant to remove the arabinose decorations from this substrate. The growth profile of the mutants are consistent with the biochemical data presented above showing that PUL-XylL encodes the only endo-acting enzyme (GH98) able to cleave the backbone of CX (and likely other complex GAXs), a prerequisite for the utilization of these polysaccharides (see below). Similarly, the inability of the PUL-XylS mutant to utilize simple xylans such as GXs and AXs, where the xylan backbone is the major component, is consistent with the locus encoding the key endo-acting surface GH10 (BACOVA_04390) that hydrolyses the backbone of sparsely decorated xylans. It is somewhat surprising, however, that ΔPUL-XylS is able to efficiently utilize GAX even though the mutant is unable to fully depolymerize the xylan backbone. This likely reflects the extensive side chains present in CX and other complex GAXs, where the xylose backbone constitutes only a relatively minor component of the total monosaccharide units in these polysaccharides.

Bottom Line: We show here, using xylan as a model, that sharing the breakdown products of complex carbohydrates by key members of the microbiota, such as Bacteroides ovatus, is dependent on the complexity of the target glycan.Characterization of the extensive xylan degrading apparatus expressed by B. ovatus reveals that the breakdown of the polysaccharide by the human gut microbiota is significantly more complex than previous models suggested, which were based on the deconstruction of xylans containing limited monosaccharide side chains.Our report presents a highly complex and dynamic xylan degrading apparatus that is fine-tuned to recognize the different forms of the polysaccharide presented to the human gut microbiota.

View Article: PubMed Central - PubMed

Affiliation: Institute for Cell and Molecular Biosciences, The Medical School, Newcastle University, Newcastle upon Tyne NE2 4HH, UK.

ABSTRACT
The structure of the human gut microbiota is controlled primarily through the degradation of complex dietary carbohydrates, but the extent to which carbohydrate breakdown products are shared between members of the microbiota is unclear. We show here, using xylan as a model, that sharing the breakdown products of complex carbohydrates by key members of the microbiota, such as Bacteroides ovatus, is dependent on the complexity of the target glycan. Characterization of the extensive xylan degrading apparatus expressed by B. ovatus reveals that the breakdown of the polysaccharide by the human gut microbiota is significantly more complex than previous models suggested, which were based on the deconstruction of xylans containing limited monosaccharide side chains. Our report presents a highly complex and dynamic xylan degrading apparatus that is fine-tuned to recognize the different forms of the polysaccharide presented to the human gut microbiota.

No MeSH data available.


Related in: MedlinePlus