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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.


Models for the degradation of different forms of xylan by B. ovatus.In the upper part of each panel the monosaccharides and linkages in the main classes of xylan are shown and are represented in their Consortium for Functional Glycomics format69. The lower parts of each panel show the model for degradation of complex GAXs like CX (a) AXs like WAX (b) and GXs like BGX (c) The red asterisk next to BACOVA_03425 GH43 indicates that the single specific arabinofuranosidase acts after BACOVA_03417 (α1,3 double-specific arabinofuranosidase) to remove the remaining α1,2 linked L-arabinose. The black arrows indicate examples of the linkages cleaved by the enzymes, shown in green ovals and identified by their glycoside hydrolase family and locus tag. In panel a, the dotted arrows from the GH98 enzyme identify possibly linkages hydrolysed by the xylanase. Although not shown on the CX model, the PUL-XylS apparatus will be present, albeit at low levels (see Fig. 2c). A schematic of the crystal structures, colour-ramped from blue (N-terminus) to red (C-terminus), of two of the xylan degrading enzymes, determined in this study (BACOVA_03438 GH95; PDB accession code 4UFC) and in a recent report37 (BACOVA_03449 GH115; PDB accession code 4C91) are shown. The red arrow heads indicate glycan transport between cellular locations, while the yellow arrow heads show the ligand (or potential ligand in case of the question mark) that binds and activates the hybrid two component system (HTCS) encoded by PUL-XylS (BACOVA_04394, light blue HTCS; activating ligand xylotetraose4) or PUL-XylL (BACOVA_03437, dark blue HTCS; activating ligand likely an arabino-xylooligosaccharide). MFS is a member of the Major Facilitator Superfamily of transport proteins, and SGBP signifies the two surface xylan binding proteins encoded by the xylan PULs, BACOVA_03431 (inactive GH10, PUL-XylL) and BACOVA_04391 (PUL-XylS). A schematic of the crystal structure of BACOVA_04391 (PDB accession code 3ORJ), colour-ramped from blue (N-terminus) to red (C-terminus), is shown. Note only one of the two SusC/D pairs from PUL-XylL is shown for clarity.
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f7: Models for the degradation of different forms of xylan by B. ovatus.In the upper part of each panel the monosaccharides and linkages in the main classes of xylan are shown and are represented in their Consortium for Functional Glycomics format69. The lower parts of each panel show the model for degradation of complex GAXs like CX (a) AXs like WAX (b) and GXs like BGX (c) The red asterisk next to BACOVA_03425 GH43 indicates that the single specific arabinofuranosidase acts after BACOVA_03417 (α1,3 double-specific arabinofuranosidase) to remove the remaining α1,2 linked L-arabinose. The black arrows indicate examples of the linkages cleaved by the enzymes, shown in green ovals and identified by their glycoside hydrolase family and locus tag. In panel a, the dotted arrows from the GH98 enzyme identify possibly linkages hydrolysed by the xylanase. Although not shown on the CX model, the PUL-XylS apparatus will be present, albeit at low levels (see Fig. 2c). A schematic of the crystal structures, colour-ramped from blue (N-terminus) to red (C-terminus), of two of the xylan degrading enzymes, determined in this study (BACOVA_03438 GH95; PDB accession code 4UFC) and in a recent report37 (BACOVA_03449 GH115; PDB accession code 4C91) are shown. The red arrow heads indicate glycan transport between cellular locations, while the yellow arrow heads show the ligand (or potential ligand in case of the question mark) that binds and activates the hybrid two component system (HTCS) encoded by PUL-XylS (BACOVA_04394, light blue HTCS; activating ligand xylotetraose4) or PUL-XylL (BACOVA_03437, dark blue HTCS; activating ligand likely an arabino-xylooligosaccharide). MFS is a member of the Major Facilitator Superfamily of transport proteins, and SGBP signifies the two surface xylan binding proteins encoded by the xylan PULs, BACOVA_03431 (inactive GH10, PUL-XylL) and BACOVA_04391 (PUL-XylS). A schematic of the crystal structure of BACOVA_04391 (PDB accession code 3ORJ), colour-ramped from blue (N-terminus) to red (C-terminus), is shown. Note only one of the two SusC/D pairs from PUL-XylL is shown for clarity.

Mentions: To summarize, using the expression, localization and biochemical data presented above Fig. 7 shows the proposed models for the acquisition and breakdown by B. ovatus of the different classes of xylan presented to the colonic microbiota.


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)

Models for the degradation of different forms of xylan by B. ovatus.In the upper part of each panel the monosaccharides and linkages in the main classes of xylan are shown and are represented in their Consortium for Functional Glycomics format69. The lower parts of each panel show the model for degradation of complex GAXs like CX (a) AXs like WAX (b) and GXs like BGX (c) The red asterisk next to BACOVA_03425 GH43 indicates that the single specific arabinofuranosidase acts after BACOVA_03417 (α1,3 double-specific arabinofuranosidase) to remove the remaining α1,2 linked L-arabinose. The black arrows indicate examples of the linkages cleaved by the enzymes, shown in green ovals and identified by their glycoside hydrolase family and locus tag. In panel a, the dotted arrows from the GH98 enzyme identify possibly linkages hydrolysed by the xylanase. Although not shown on the CX model, the PUL-XylS apparatus will be present, albeit at low levels (see Fig. 2c). A schematic of the crystal structures, colour-ramped from blue (N-terminus) to red (C-terminus), of two of the xylan degrading enzymes, determined in this study (BACOVA_03438 GH95; PDB accession code 4UFC) and in a recent report37 (BACOVA_03449 GH115; PDB accession code 4C91) are shown. The red arrow heads indicate glycan transport between cellular locations, while the yellow arrow heads show the ligand (or potential ligand in case of the question mark) that binds and activates the hybrid two component system (HTCS) encoded by PUL-XylS (BACOVA_04394, light blue HTCS; activating ligand xylotetraose4) or PUL-XylL (BACOVA_03437, dark blue HTCS; activating ligand likely an arabino-xylooligosaccharide). MFS is a member of the Major Facilitator Superfamily of transport proteins, and SGBP signifies the two surface xylan binding proteins encoded by the xylan PULs, BACOVA_03431 (inactive GH10, PUL-XylL) and BACOVA_04391 (PUL-XylS). A schematic of the crystal structure of BACOVA_04391 (PDB accession code 3ORJ), colour-ramped from blue (N-terminus) to red (C-terminus), is shown. Note only one of the two SusC/D pairs from PUL-XylL is shown for clarity.
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f7: Models for the degradation of different forms of xylan by B. ovatus.In the upper part of each panel the monosaccharides and linkages in the main classes of xylan are shown and are represented in their Consortium for Functional Glycomics format69. The lower parts of each panel show the model for degradation of complex GAXs like CX (a) AXs like WAX (b) and GXs like BGX (c) The red asterisk next to BACOVA_03425 GH43 indicates that the single specific arabinofuranosidase acts after BACOVA_03417 (α1,3 double-specific arabinofuranosidase) to remove the remaining α1,2 linked L-arabinose. The black arrows indicate examples of the linkages cleaved by the enzymes, shown in green ovals and identified by their glycoside hydrolase family and locus tag. In panel a, the dotted arrows from the GH98 enzyme identify possibly linkages hydrolysed by the xylanase. Although not shown on the CX model, the PUL-XylS apparatus will be present, albeit at low levels (see Fig. 2c). A schematic of the crystal structures, colour-ramped from blue (N-terminus) to red (C-terminus), of two of the xylan degrading enzymes, determined in this study (BACOVA_03438 GH95; PDB accession code 4UFC) and in a recent report37 (BACOVA_03449 GH115; PDB accession code 4C91) are shown. The red arrow heads indicate glycan transport between cellular locations, while the yellow arrow heads show the ligand (or potential ligand in case of the question mark) that binds and activates the hybrid two component system (HTCS) encoded by PUL-XylS (BACOVA_04394, light blue HTCS; activating ligand xylotetraose4) or PUL-XylL (BACOVA_03437, dark blue HTCS; activating ligand likely an arabino-xylooligosaccharide). MFS is a member of the Major Facilitator Superfamily of transport proteins, and SGBP signifies the two surface xylan binding proteins encoded by the xylan PULs, BACOVA_03431 (inactive GH10, PUL-XylL) and BACOVA_04391 (PUL-XylS). A schematic of the crystal structure of BACOVA_04391 (PDB accession code 3ORJ), colour-ramped from blue (N-terminus) to red (C-terminus), is shown. Note only one of the two SusC/D pairs from PUL-XylL is shown for clarity.
Mentions: To summarize, using the expression, localization and biochemical data presented above Fig. 7 shows the proposed models for the acquisition and breakdown by B. ovatus of the different classes of xylan presented to the colonic microbiota.

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.