A bacterial sulfoglycosidase highlights mucin O-glycan breakdown in the gut ecosystem

Toshihiko Katoh; Chihaya Yamada; Michael D. Wallace; Ayako Yoshida; Aina Gotoh; Moe Arai; Takako Maeshibu; Toma Kashima; Arno Hagenbeek; Miriam N. Ojima; Hiromi Takada; Mikiyasu Sakanaka; Hidenori Shimizu; Keita Nishiyama; Hisashi Ashida; Junko Hirose; Maria Suarez-Diez; Makoto Nishiyama; Ikuo Kimura; Keith A. Stubbs; Shinya Fushinobu; Takane Katayama

doi:10.1038/s41589-023-01272-y

A bacterial sulfoglycosidase highlights mucin O-glycan breakdown in the gut ecosystem

Toshihiko Katoh, Chihaya Yamada, Michael D. Wallace, Ayako Yoshida, Aina Gotoh, Moe Arai, Takako Maeshibu, Toma Kashima, Arno Hagenbeek, Miriam N. Ojima, Hiromi Takada, Mikiyasu Sakanaka, Hidenori Shimizu, Keita Nishiyama, Hisashi Ashida, Junko Hirose, Maria Suarez-Diez, Makoto Nishiyama, Ikuo Kimura, Keith A. StubbsShinya Fushinobu^*, Takane Katayama^*

^*Corresponding author for this work

Systems and Synthetic Biology

Research output: Contribution to journal › Article › Academic › peer-review

31 Citations (Scopus)

Abstract

Mucinolytic bacteria modulate host–microbiota symbiosis and dysbiosis through their ability to degrade mucin O-glycans. However, how and to what extent bacterial enzymes are involved in the breakdown process remains poorly understood. Here we focus on a glycoside hydrolase family 20 sulfoglycosidase (BbhII) from Bifidobacterium bifidum, which releases N-acetylglucosamine-6-sulfate from sulfated mucins. Glycomic analysis showed that, in addition to sulfatases, sulfoglycosidases are involved in mucin O-glycan breakdown in vivo and that the released N-acetylglucosamine-6-sulfate potentially affects gut microbial metabolism, both of which were also supported by a metagenomic data mining analysis. Enzymatic and structural analysis of BbhII reveals the architecture underlying its specificity and the presence of a GlcNAc-6S-specific carbohydrate-binding module (CBM) 32 with a distinct sugar recognition mode that B. bifidum takes advantage of to degrade mucin O-glycans. Comparative analysis of the genomes of prominent mucinolytic bacteria also highlights a CBM-dependent O-glycan breakdown strategy used by B. bifidum. [Figure not available: see fulltext.].

Original language	English
Pages (from-to)	778-789
Number of pages	12
Journal	Nature Chemical Biology
Volume	19
DOIs	https://doi.org/10.1038/s41589-023-01272-y
Publication status	Published - 2 Mar 2023

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Katoh, T., Yamada, C., Wallace, M. D., Yoshida, A., Gotoh, A., Arai, M., Maeshibu, T., Kashima, T., Hagenbeek, A., Ojima, M. N., Takada, H., Sakanaka, M., Shimizu, H., Nishiyama, K., Ashida, H., Hirose, J., Suarez-Diez, M., Nishiyama, M., Kimura, I., ... Katayama, T. (2023). A bacterial sulfoglycosidase highlights mucin O-glycan breakdown in the gut ecosystem. Nature Chemical Biology, 19, 778-789. https://doi.org/10.1038/s41589-023-01272-y

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title = "A bacterial sulfoglycosidase highlights mucin O-glycan breakdown in the gut ecosystem",

abstract = "Mucinolytic bacteria modulate host–microbiota symbiosis and dysbiosis through their ability to degrade mucin O-glycans. However, how and to what extent bacterial enzymes are involved in the breakdown process remains poorly understood. Here we focus on a glycoside hydrolase family 20 sulfoglycosidase (BbhII) from Bifidobacterium bifidum, which releases N-acetylglucosamine-6-sulfate from sulfated mucins. Glycomic analysis showed that, in addition to sulfatases, sulfoglycosidases are involved in mucin O-glycan breakdown in vivo and that the released N-acetylglucosamine-6-sulfate potentially affects gut microbial metabolism, both of which were also supported by a metagenomic data mining analysis. Enzymatic and structural analysis of BbhII reveals the architecture underlying its specificity and the presence of a GlcNAc-6S-specific carbohydrate-binding module (CBM) 32 with a distinct sugar recognition mode that B. bifidum takes advantage of to degrade mucin O-glycans. Comparative analysis of the genomes of prominent mucinolytic bacteria also highlights a CBM-dependent O-glycan breakdown strategy used by B. bifidum. [Figure not available: see fulltext.].",

author = "Toshihiko Katoh and Chihaya Yamada and Wallace, {Michael D.} and Ayako Yoshida and Aina Gotoh and Moe Arai and Takako Maeshibu and Toma Kashima and Arno Hagenbeek and Ojima, {Miriam N.} and Hiromi Takada and Mikiyasu Sakanaka and Hidenori Shimizu and Keita Nishiyama and Hisashi Ashida and Junko Hirose and Maria Suarez-Diez and Makoto Nishiyama and Ikuo Kimura and Stubbs, {Keith A.} and Shinya Fushinobu and Takane Katayama",

year = "2023",

month = mar,

day = "2",

doi = "10.1038/s41589-023-01272-y",

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Katoh, T, Yamada, C, Wallace, MD, Yoshida, A, Gotoh, A, Arai, M, Maeshibu, T, Kashima, T, Hagenbeek, A, Ojima, MN, Takada, H, Sakanaka, M, Shimizu, H, Nishiyama, K, Ashida, H, Hirose, J, Suarez-Diez, M, Nishiyama, M, Kimura, I, Stubbs, KA, Fushinobu, S & Katayama, T 2023, 'A bacterial sulfoglycosidase highlights mucin O-glycan breakdown in the gut ecosystem', Nature Chemical Biology, vol. 19, pp. 778-789. https://doi.org/10.1038/s41589-023-01272-y

TY - JOUR

T1 - A bacterial sulfoglycosidase highlights mucin O-glycan breakdown in the gut ecosystem

AU - Katoh, Toshihiko

AU - Yamada, Chihaya

AU - Wallace, Michael D.

AU - Yoshida, Ayako

AU - Gotoh, Aina

AU - Arai, Moe

AU - Maeshibu, Takako

AU - Kashima, Toma

AU - Hagenbeek, Arno

AU - Ojima, Miriam N.

AU - Takada, Hiromi

AU - Sakanaka, Mikiyasu

AU - Shimizu, Hidenori

AU - Nishiyama, Keita

AU - Ashida, Hisashi

AU - Hirose, Junko

AU - Suarez-Diez, Maria

AU - Nishiyama, Makoto

AU - Kimura, Ikuo

AU - Stubbs, Keith A.

AU - Fushinobu, Shinya

AU - Katayama, Takane

PY - 2023/3/2

Y1 - 2023/3/2

N2 - Mucinolytic bacteria modulate host–microbiota symbiosis and dysbiosis through their ability to degrade mucin O-glycans. However, how and to what extent bacterial enzymes are involved in the breakdown process remains poorly understood. Here we focus on a glycoside hydrolase family 20 sulfoglycosidase (BbhII) from Bifidobacterium bifidum, which releases N-acetylglucosamine-6-sulfate from sulfated mucins. Glycomic analysis showed that, in addition to sulfatases, sulfoglycosidases are involved in mucin O-glycan breakdown in vivo and that the released N-acetylglucosamine-6-sulfate potentially affects gut microbial metabolism, both of which were also supported by a metagenomic data mining analysis. Enzymatic and structural analysis of BbhII reveals the architecture underlying its specificity and the presence of a GlcNAc-6S-specific carbohydrate-binding module (CBM) 32 with a distinct sugar recognition mode that B. bifidum takes advantage of to degrade mucin O-glycans. Comparative analysis of the genomes of prominent mucinolytic bacteria also highlights a CBM-dependent O-glycan breakdown strategy used by B. bifidum. [Figure not available: see fulltext.].

AB - Mucinolytic bacteria modulate host–microbiota symbiosis and dysbiosis through their ability to degrade mucin O-glycans. However, how and to what extent bacterial enzymes are involved in the breakdown process remains poorly understood. Here we focus on a glycoside hydrolase family 20 sulfoglycosidase (BbhII) from Bifidobacterium bifidum, which releases N-acetylglucosamine-6-sulfate from sulfated mucins. Glycomic analysis showed that, in addition to sulfatases, sulfoglycosidases are involved in mucin O-glycan breakdown in vivo and that the released N-acetylglucosamine-6-sulfate potentially affects gut microbial metabolism, both of which were also supported by a metagenomic data mining analysis. Enzymatic and structural analysis of BbhII reveals the architecture underlying its specificity and the presence of a GlcNAc-6S-specific carbohydrate-binding module (CBM) 32 with a distinct sugar recognition mode that B. bifidum takes advantage of to degrade mucin O-glycans. Comparative analysis of the genomes of prominent mucinolytic bacteria also highlights a CBM-dependent O-glycan breakdown strategy used by B. bifidum. [Figure not available: see fulltext.].

U2 - 10.1038/s41589-023-01272-y

DO - 10.1038/s41589-023-01272-y

M3 - Article

AN - SCOPUS:85149065656

SN - 1552-4450

VL - 19

SP - 778

EP - 789

JO - Nature Chemical Biology

JF - Nature Chemical Biology

ER -

A bacterial sulfoglycosidase highlights mucin O-glycan breakdown in the gut ecosystem

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