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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 M, Fredslund F, Andersen JM, Vujičić Žagar A, Henriksen JR, Andersen TL, Svensson B, Slotboom DJ, Abou Hachem M
J Biol Chem 291 20220-31 (2016)
Related entries: 4zs9, 4zze

Cited: 24 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.

Articles - 4zza mentioned but not cited (1)

  1. 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 M, Fredslund F, Andersen JM, Vujičić Žagar A, Henriksen JR, Andersen TL, Svensson B, Slotboom DJ, Abou Hachem M. J Biol Chem 291 20220-20231 (2016)


Reviews citing this publication (7)

  1. Diet and microbiota linked in health and disease. Requena T, Martínez-Cuesta MC, Peláez C. Food Funct 9 688-704 (2018)
  2. The Critical Roles of Polysaccharides in Gut Microbial Ecology and Physiology. Porter NT, Martens EC. Annu. Rev. Microbiol. 71 349-369 (2017)
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  1. Multiple Transporters and Glycoside Hydrolases Are Involved in Arabinoxylan-Derived Oligosaccharide Utilization in Bifidobacterium pseudocatenulatum. Saito Y, Shigehisa A, Watanabe Y, Tsukuda N, Moriyama-Ohara K, Hara T, Matsumoto S, Tsuji H, Matsuki T. Appl Environ Microbiol 86 e01782-20 (2020)
  2. 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)
  3. α-Galactosidase and Sucrose-Kinase Relationships in a Bi-functional AgaSK Enzyme Produced by the Human Gut Symbiont Ruminococcus gnavus E1. Lafond M, Tauzin AS, Bruel L, Laville E, Lombard V, Esque J, André I, Vidal N, Pompeo F, Quinson N, Perrier J, Fons M, Potocki-Veronese G, Giardina T. Front Microbiol 11 579521 (2020)
  4. A Novel Two-Component System, XygS/XygR, Positively Regulates Xyloglucan Degradation, Import, and Catabolism in Ruminiclostridium cellulolyticum. Kampik C, Denis Y, Pagès S, Perret S, Tardif C, Fierobe HP, de Philip P. Appl Environ Microbiol 86 e01357-20 (2020)
  5. 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)
  6. Bifidobacterium response to lactulose ingestion in the gut relies on a solute-binding protein-dependent ABC transporter. Yoshida K, Hirano R, Sakai Y, Choi M, Sakanaka M, Kurihara S, Iino H, Xiao JZ, Katayama T, Odamaki T. Commun Biol 4 541 (2021)
  7. Characterization of a GH36 α-D-Galactosidase Associated with Assimilation of Gum Arabic in Bifidobacterium longum subsp. longum JCM7052. Sasaki Y, Uchimura Y, Kitahara K, Fujita K. J Appl Glycosci (1999) 68 47-52 (2021)
  8. EDESIA: Plants, Food and Health: A cross-disciplinary PhD programme from crop to clinic. Clark IM, Cassidy A, Heppleston A, Bal M, Morgan Y, Nicklin A, Yue Y, Zardkoohi A, Martin C. Nutr Bull 47 366-373 (2022)
  9. Analysis of Structural and Functional Differences of Glucans Produced by the Natively Released Dextransucrase of Liquorilactobacillus hordei TMW 1.1822. Schmid J, Wefers D, Vogel RF, Jakob F. Appl Biochem Biotechnol 193 96-110 (2021)
  10. Butyrate producing colonic Clostridiales metabolise human milk oligosaccharides and cross feed on mucin via conserved pathways. Pichler MJ, Yamada C, Shuoker B, Alvarez-Silva C, Gotoh A, Leth ML, Schoof E, Katoh T, Sakanaka M, Katayama T, Jin C, Karlsson NG, Arumugam M, Fushinobu S, Abou Hachem M. Nat Commun 11 3285 (2020)
  11. Functional host-specific adaptation of the intestinal microbiome in hominids. Rühlemann MC, Bang C, Gogarten JF, Hermes BM, Groussin M, Waschina S, Poyet M, Ulrich M, Akoua-Koffi C, Deschner T, Muyembe-Tamfum JJ, Robbins MM, Surbeck M, Wittig RM, Zuberbühler K, Baines JF, Leendertz FH, Franke A. Nat Commun 15 326 (2024)
  12. Identifying the essential nutritional requirements of the probiotic bacteria Bifidobacterium animalis and Bifidobacterium longum through genome-scale modeling. Schöpping M, Gaspar P, Neves AR, Franzén CJ, Zeidan AA. NPJ Syst Biol Appl 7 47 (2021)
  13. 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)
  14. Prebiotic Properties of Non-Fructosylated α-Galactooligosaccharides from PEA (Pisum sativum L.) Using Infant Fecal Slurries. Marín-Manzano MDC, Hernandez-Hernandez O, Diez-Municio M, Delgado-Andrade C, Moreno FJ, Clemente A. Foods 9 (2020)
  15. 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)
  16. Utilization of dietary mixed-linkage β-glucans by the Firmicute Blautia producta. Singh RP, Niharika J, Thakur R, Wagstaff BA, Kumar G, Kurata R, Patel D, Levy CW, Miyazaki T, Field RA. J Biol Chem 299 104806 (2023)


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