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An atp binding cassette transporter mediates the uptake of α-(1,6)-linked dietary oligosaccharides in bifidobacterium and correlates with competitive growth on these substrates

Ejby, Morten; Fredslund, Folmer LU ; Andersen, Joakim Mark; Žagar¶, Andreja Vujičić; Henriksen, Jonas Rosager; Andersen, Thomas Lars; Svensson, Birte; Slotboom, Dirk Jan and Hachem, Maher Abou LU (2016) In Journal of Biological Chemistry 291(38). p.20220-20231
Abstract

The molecular details and impact of oligosaccharide uptake by distinct human gut microbiota (HGM) are currently not well understood. Non-digestible dietary galacto- and gluco-α-(1,6)-oligosaccharides from legumes and starch, respectively, are preferentially fermented by mainly bifidobacteria and lactobacilli in the human gut. Here we show that the solute binding protein (BlG16BP) associated with an ATP binding cassette (ABC) transporter from the probiotic Bifidobacterium animalis subsp. lactis Bl-04 binds α-(1,6)-linked glucosides and galactosides of varying size, linkage, and monosaccharide composition with preference for the trisaccharides raffinose and panose. This preference is also reflected in the α-(1,6)-galactoside uptake... (More)

The molecular details and impact of oligosaccharide uptake by distinct human gut microbiota (HGM) are currently not well understood. Non-digestible dietary galacto- and gluco-α-(1,6)-oligosaccharides from legumes and starch, respectively, are preferentially fermented by mainly bifidobacteria and lactobacilli in the human gut. Here we show that the solute binding protein (BlG16BP) associated with an ATP binding cassette (ABC) transporter from the probiotic Bifidobacterium animalis subsp. lactis Bl-04 binds α-(1,6)-linked glucosides and galactosides of varying size, linkage, and monosaccharide composition with preference for the trisaccharides raffinose and panose. This preference is also reflected in the α-(1,6)-galactoside uptake profile of the bacterium. Structures of BlG16BP in complex with raffinose and panose revealed the basis for the remarkable ligand binding plasticity of BlG16BP, which recognizes the nonreducing α-(1,6)-diglycoside in its ligands. BlG16BP homologues occur predominantly in bifidobacteria and a few Firmicutes but lack in other HGMs. Among seven bifidobacterial taxa, only those possessing this transporter displayed growth on α-(1,6)-glycosides. Competition assays revealed that the dominant HGM commensal Bacteroides ovatus was out-competed by B. animalis subsp. lactis Bl-04 in mixed cultures growing on raffinose, the preferred ligand for the BlG16BP. By comparison, B. ovatus mono-cultures grew very efficiently on this trisaccharide These findings suggest that the ABC-mediated uptake of raffinose provides an important competitive advantage, particularly against dominant Bacteroides that lack glycan-specific ABC-transporters. This novel insight highlights the role of glycan transport in defining the metabolic specialization of gut bacteria.

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author
organization
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type
Contribution to journal
publication status
published
subject
in
Journal of Biological Chemistry
volume
291
issue
38
pages
12 pages
publisher
ASBMB
external identifiers
  • scopus:84987849585
  • wos:000383243100041
ISSN
0021-9258
DOI
10.1074/jbc.M116.746529
language
English
LU publication?
yes
id
547e7d68-ac77-426b-8842-b58c813fe8f4
date added to LUP
2016-10-11 10:57:56
date last changed
2017-01-01 08:36:22
@article{547e7d68-ac77-426b-8842-b58c813fe8f4,
  abstract     = {<p>The molecular details and impact of oligosaccharide uptake by distinct human gut microbiota (HGM) are currently not well understood. Non-digestible dietary galacto- and gluco-α-(1,6)-oligosaccharides from legumes and starch, respectively, are preferentially fermented by mainly bifidobacteria and lactobacilli in the human gut. Here we show that the solute binding protein (BlG16BP) associated with an ATP binding cassette (ABC) transporter from the probiotic Bifidobacterium animalis subsp. lactis Bl-04 binds α-(1,6)-linked glucosides and galactosides of varying size, linkage, and monosaccharide composition with preference for the trisaccharides raffinose and panose. This preference is also reflected in the α-(1,6)-galactoside uptake profile of the bacterium. Structures of BlG16BP in complex with raffinose and panose revealed the basis for the remarkable ligand binding plasticity of BlG16BP, which recognizes the nonreducing α-(1,6)-diglycoside in its ligands. BlG16BP homologues occur predominantly in bifidobacteria and a few Firmicutes but lack in other HGMs. Among seven bifidobacterial taxa, only those possessing this transporter displayed growth on α-(1,6)-glycosides. Competition assays revealed that the dominant HGM commensal Bacteroides ovatus was out-competed by B. animalis subsp. lactis Bl-04 in mixed cultures growing on raffinose, the preferred ligand for the BlG16BP. By comparison, B. ovatus mono-cultures grew very efficiently on this trisaccharide These findings suggest that the ABC-mediated uptake of raffinose provides an important competitive advantage, particularly against dominant Bacteroides that lack glycan-specific ABC-transporters. This novel insight highlights the role of glycan transport in defining the metabolic specialization of gut bacteria.</p>},
  author       = {Ejby, Morten and Fredslund, Folmer and Andersen, Joakim Mark and Žagar¶, Andreja Vujičić and Henriksen, Jonas Rosager and Andersen, Thomas Lars and Svensson, Birte and Slotboom, Dirk Jan and Hachem, Maher Abou},
  issn         = {0021-9258},
  language     = {eng},
  month        = {09},
  number       = {38},
  pages        = {20220--20231},
  publisher    = {ASBMB},
  series       = {Journal of Biological Chemistry},
  title        = {An atp binding cassette transporter mediates the uptake of α-(1,6)-linked dietary oligosaccharides in bifidobacterium and correlates with competitive growth on these substrates},
  url          = {http://dx.doi.org/10.1074/jbc.M116.746529},
  volume       = {291},
  year         = {2016},
}