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PreprintCited by 13Glycosylation and Glycoproteins ResearchEnzyme Production and CharacterizationCarbohydrate Chemistry and Synthesis

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Genetic and functional diversity of β- N -acetylgalactosamine residue-targeting glycosidases expanded by deep-sea metagenome

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Sumida, Tomomi, Hiraoka, Satoshi, Usui, Keiko, Ishiwata, Akihiro, Sengoku, Toru, Stubbs, Keith A, Tanaka, Katsunori, Deguchi, Shigeru, Fushinobu, Shinya, Nunoura, Takuro·2023·Nature Communications
DOI 10.1101/2023.07.28.550916PMC PMC11087588

Preprint — published as 10.1038/s41467-024-47653-2 · Paper page

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Abstract

β- N -Acetylgalactosamine-containing glycans play essential roles in several biological processes, including cell adhesion, signal transduction, and immune responses. β- N -Acetylgalactosaminidases hydrolyze β- N -acetylgalactosamine linkages of various glycoconjugates. However, their biological significance remains ambiguous, primarily because only one type of enzyme, exo-β- N -acetylgalactosaminidases that specifically act on β- N -acetylgalactosamine residues, has been documented so far. In this study, we identified three novel glycoside hydrolase families distributed among all three domains of life and characterized eight novel β- N -acetylgalactosaminidases and β- N -acetylhexosaminidase through sequence-based screening of deep-sea metagenomes and subsequent searching of public protein databases. Despite low sequence similarity, the crystal structures of these enzymes demonstrate that all enzymes share a prototype structure and diversify their substrate specificities (endo-, dual-endo/exo-, and exo-) through the accumulation of mutations and insertional amino acid sequences. The diverse β- N -acetylgalactosaminidases reported in this study could facilitate the comprehension of their structures and functions and present novel evolutionary pathways for expanding their substrate specificity.

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Metadata

Authors
Sumida, T., Hiraoka, S., Usui, K., Ishiwata, A., Sengoku, T., Stubbs, K. A., Tanaka, K., Deguchi, S., Fushinobu, S., & Nunoura, T.
Affiliations
  • Japan Agency for Marine-Earth Science and Technology (JP)
  • RIKEN (JP)
  • Yokohama City University (JP)
  • The University of Western Australia (AU)
  • Tokyo Institute of Technology (JP)
  • The University of Tokyo (JP)
Corresponding author
  • Sumida, Tomomi
  • Fushinobu, Shinya
ORCID
Venue
Nature Communications
Publisher
openRxiv
Published
2023-07-28
Volume
15
Issue
1
Pages
3543-3543
ISSN
2041-1723 (ISSN-L)
DOI
10.1101/2023.07.28.550916
PMC
PMC11087588
OpenAlex
W4396803025
Cited by
13
References
1
Citations by year
2026: 6 · 2025: 4 · 2024: 2 · 2023: 1
FWCI
1.63
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Nature Communications (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • UWA Profiles and Research Repository (UWA) (submittedVersion, cc-by)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Mizutani Foundation for Glycoscience
  • Japan Agency for Medical Research and Development (JP22ama-( 121001)
  • Australian Research Council (FT100100291)
  • Japan Society for the Promotion of Science (24H02269, 22K05398, 20K15444)
  • Japan Agency for Marine-Earth Science and Technology
  • Institute of Genetics
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Glycosylation and Glycoproteins Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Enzyme Production and Characterization
  • Physical Sciences › Chemistry › Organic Chemistry › Carbohydrate Chemistry and Synthesis
Keywords
beta-N-acetylhexosaminidase, glycoside hydrolases, substrate specificity, enzyme evolution, crystal structure, glycoconjugates
MeSH terms
Acetylgalactosamine, Amino Acid Sequence, Animals, beta-N-Acetylhexosaminidases, Glycoside Hydrolases, Phylogeny, Substrate Specificity, Crystallography, X-Ray, Metagenome

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