4zs9 Citations

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.

J. Biol. Chem. 291 20220-31 (2016)
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Cited: 7 times
EuropePMC logo PMID: 27502277

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 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 non-reducing 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.

Reviews citing this publication (3)

  1. Beneficial Effect of Intestinal Fermentation of Natural Polysaccharides. Zhang T, Yang Y, Liang Y, Jiao X, Zhao C. Nutrients 10 (2018)
  2. Diet and microbiota linked in health and disease. Requena T, Martínez-Cuesta MC, Peláez C. Food Funct 9 688-704 (2018)
  3. The Critical Roles of Polysaccharides in Gut Microbial Ecology and Physiology. Porter NT, Martens EC. Annu. Rev. Microbiol. 71 349-369 (2017)

Articles citing this publication (4)

  1. Differential bacterial capture and transport preferences facilitate co-growth on dietary xylan in the human gut. Leth ML, Ejby M, Workman C, Ewald DA, Pedersen SS, Sternberg C, Bahl MI, Licht TR, Aachmann FL, Westereng B, Abou Hachem M. Nat Microbiol 3 570-580 (2018)
  2. Structural and thermodynamic insights into β-1,2-glucooligosaccharide capture by a solute-binding protein in Listeria innocua. Abe K, Sunagawa N, Terada T, Takahashi Y, Arakawa T, Igarashi K, Samejima M, Nakai H, Taguchi H, Nakajima M, Fushinobu S. J. Biol. Chem. 293 8812-8828 (2018)
  3. Molecular analysis of an enigmatic Streptococcus pneumoniae virulence factor: The raffinose-family oligosaccharide utilization system. Hobbs JK, Meier EPW, Pluvinage B, Mey MA, Boraston AB. J. Biol. Chem. 294 17197-17208 (2019)
  4. Substrate preference of an ABC importer corresponds to selective growth on β-(1,6)-galactosides in Bifidobacterium animalis subsp. lactis. Theilmann MC, Fredslund F, Svensson B, Lo Leggio L, Abou Hachem M. J. Biol. Chem. 294 11701-11711 (2019)