Bifidobacterium bifidum extracellular sialidase enhances adhesion to the mucosal surface and supports carbohydrate assimilation

Keita Nishiyama, Yuji Yamamoto, Makoto Sugiyama, Takashi Takaki, Tadasu Urashima, Satoru Fukiya, Atsushi Yokota, Nobuhiko Okada, Takao Mukai

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

Bifidobacterium is a natural inhabitant of the human gastrointestinal (GI) tract. We studied the role of the extracellular sialidase (SiaBb2, 835 amino acids [aa]) from Bifidobacterium bifidum ATCC 15696 in mucosal surface adhesion and carbohydrate catabolism. Human milk oligosaccharides (HMOs) or porcine mucin oligosaccharides as the sole carbon source enhanced B. bifidum growth. This was impaired in a B. bifidum ATCC 15696 strain harboring a mutation in the siabb2 gene. Mutant cells in early to late exponential growth phase also showed decreased adhesion to human epithelial cells and porcine mucin relative to the wild-type strain. These results indicate that SiaBb2 removes sialic acid from HMOs and mucin for metabolic purposes and may promote bifidobacterial adhesion to the mucosal surface. To further characterize SiaBb2-mediated bacterial adhesion, we examined the binding of His-tagged recombinant SiaBb2 peptide to colonic mucins and found that His-SiaBb2 as well as a conserved sialidase domain peptide (aa 187 to 553, His-Sia) bound to porcine mucin and murine colonic sections. A glycoarray assay revealed that His-Sia bound to the α2,6-linked but not to the α2,3-linked sialic acid on sialyloligosaccharide and blood type A antigen [GalNAcα1-3(Fucα1-2)Galβ] at the nonreducing termini of sugar chains. These results suggest that the sialidase domain of SiaBb2 is responsible for this interaction and that the protein recognizes two distinct carbohydrate structures. Thus, SiaBb2 may be involved in Bifidobacterium-mucosal surface interactions as well as in the assimilation of a variety of sialylated carbohydrates. IMPORTANCE Adhesion to the host mucosal surface and carbohydrate assimilation are important for bifidobacterium colonization and survival in the host gastrointestinal tract. In this study, we investigated the mechanistic basis for B. bifidum extracellular sialidase (SiaBb2)-mediated adhesion. SiaBb2 cleaved sialyl-human milk oligosaccharides and mucin glycans to produce oligosaccharides that supported B. bifidum growth. Moreover, SiaBb2 enhanced B. bifidum adhesion to mucosal surfaces via specific interactions with the α2,6 linkage of sialyloligosaccharide and blood type A antigen on mucin carbohydrates. These findings provide insight into the bifunctional role of SiaBb2 and the adhesion properties of B. bifidum strains.

Original languageEnglish
Article numbere00928-17
JournalmBio
Volume8
Issue number5
DOIs
Publication statusPublished - 2017 Sep 1
Externally publishedYes

Fingerprint

Neuraminidase
Mucins
Carbohydrates
Oligosaccharides
Bifidobacterium
Human Milk
Swine
N-Acetylneuraminic Acid
Gastrointestinal Tract
Growth
Bacterial Adhesion
Antigens
Amino Acids
Bifidobacterium bifidum
Polysaccharides
Carbon
Epithelial Cells
Peptides
Mutation
Survival

Keywords

  • Adhesion molecules
  • Bacterial adhesion
  • Bifidobacteria
  • Carbohydrate metabolism
  • Sialidase

ASJC Scopus subject areas

  • Microbiology
  • Virology

Cite this

Bifidobacterium bifidum extracellular sialidase enhances adhesion to the mucosal surface and supports carbohydrate assimilation. / Nishiyama, Keita; Yamamoto, Yuji; Sugiyama, Makoto; Takaki, Takashi; Urashima, Tadasu; Fukiya, Satoru; Yokota, Atsushi; Okada, Nobuhiko; Mukai, Takao.

In: mBio, Vol. 8, No. 5, e00928-17, 01.09.2017.

Research output: Contribution to journalArticle

Nishiyama, K, Yamamoto, Y, Sugiyama, M, Takaki, T, Urashima, T, Fukiya, S, Yokota, A, Okada, N & Mukai, T 2017, 'Bifidobacterium bifidum extracellular sialidase enhances adhesion to the mucosal surface and supports carbohydrate assimilation', mBio, vol. 8, no. 5, e00928-17. https://doi.org/10.1128/mBio.00928-17
Nishiyama, Keita ; Yamamoto, Yuji ; Sugiyama, Makoto ; Takaki, Takashi ; Urashima, Tadasu ; Fukiya, Satoru ; Yokota, Atsushi ; Okada, Nobuhiko ; Mukai, Takao. / Bifidobacterium bifidum extracellular sialidase enhances adhesion to the mucosal surface and supports carbohydrate assimilation. In: mBio. 2017 ; Vol. 8, No. 5.
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AU - Urashima, Tadasu

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