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

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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; Andersen, Joakim Mark; Žagar¶, Andreja Vujičić; Henriksen, Jonas Rosager; Andersen, Thomas Lars; Svensson, Birte; Slotboom, Dirk Jan; Hachem, Maher Abou.

In: Journal of Biological Chemistry, Vol. 291, No. 38, 16.09.2016, p. 20220-20231.

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Ejby, M, Fredslund, F, Andersen, JM, Žagar¶, AV, Henriksen, JR, Andersen, TL, Svensson, B, Slotboom, DJ & Hachem, MA 2016, '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', Journal of Biological Chemistry, vol. 291, no. 38, pp. 20220-20231. https://doi.org/10.1074/jbc.M116.746529

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Ejby, Morten ; Fredslund, Folmer ; Andersen, Joakim Mark ; Žagar¶, Andreja Vujičić ; Henriksen, Jonas Rosager ; Andersen, Thomas Lars ; Svensson, Birte ; Slotboom, Dirk Jan ; Hachem, Maher Abou. / 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. In: Journal of Biological Chemistry. 2016 ; Vol. 291, No. 38. pp. 20220-20231.

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TY - JOUR

T1 - 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

AU - Ejby, Morten

AU - Fredslund, Folmer

AU - Andersen, Joakim Mark

AU - Žagar¶, Andreja Vujičić

AU - Henriksen, Jonas Rosager

AU - Andersen, Thomas Lars

AU - Svensson, Birte

AU - Slotboom, Dirk Jan

AU - Hachem, Maher Abou

PY - 2016/9/16

Y1 - 2016/9/16

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=84987849585&partnerID=8YFLogxK

U2 - 10.1074/jbc.M116.746529

DO - 10.1074/jbc.M116.746529

M3 - Article

VL - 291

SP - 20220

EP - 20231

JO - Journal of Biological Chemistry

JF - Journal of Biological Chemistry

SN - 1083-351X

IS - 38

ER -