Engineering and Dissecting the Glycosylation Pathway of a Streptococcal Serine-rich Repeat Adhesin

Zhu, Fan; Zhang, Hua; Yang, Tiandi; Haslam, Stuart M.; Dell, Anne; Wu, Hui

doi:10.1074/jbc.m116.752998

Cited by 36Glycosylation and Glycoproteins ResearchCarbohydrate Chemistry and SynthesisBiochemical and Structural Characterization

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Engineering and Dissecting the Glycosylation Pathway of a Streptococcal Serine-rich Repeat Adhesin

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Zhu, Fan, Zhang, Hua, Yang, Tiandi, Haslam, Stuart M., Dell, Anne, Wu, Hui·2016·Journal of Biological Chemistry

DOI 10.1074/jbc.m116.752998PMC PMC5207161

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Abstract

Serine-rich repeat glycoproteins (SRRPs) are conserved in Gram-positive bacteria. They are crucial for modulating biofilm formation and bacterial-host interactions. Glycosylation of SRRPs plays a pivotal role in the process; thus understanding the glycosyltransferases involved is key to identifying new therapeutic drug targets. The glycosylation of Fap1, an SRRP of Streptococcus parasanguinis, is mediated by a gene cluster consisting of six genes: gtf1, gtf2, gly, gtf3, dGT1, and galT2 Mature Fap1 glycan possesses the sequence of Rha1-3Glc1-(Glc1-3GlcNAc1)-2,6-Glc1-6GlcNAc. Gtf12, Gtf3, and dGT1 are responsible for the first four steps of the Fap1 glycosylation, catalyzing the transfer of GlcNAc, Glc, Glc, and GlcNAc residues to the protein backbone sequentially. The role of GalT2 and Gly in the Fap1 glycosylation is unknown. In the present study, we synthesized the fully modified Fap1 glycan in Escherichia coli by incorporating all six genes from the cluster. This study represents the first reconstitution of an exogenous stepwise O-glycosylation synthetic pathway in E. coli In addition, we have determined that GalT2 mediates the fifth step of the Fap1 glycosylation by adding a rhamnose residue, and Gly mediates the final glycosylation step by transferring glucosyl residues. Furthermore, inactivation of each glycosyltransferase gene resulted in differentially impaired biofilms of S. parasanguinis, demonstrating the importance of Fap1 glycosylation in the biofilm formation. The Fap1 glycosylation system offers an excellent model to engineer glycans using different permutations of glycosyltransferases and to investigate biosynthetic pathways of SRRPs because SRRP genetic loci are highly conserved.

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Loss of glycosylation of the Fap1 serine-rich repeat adhesin with GalNAc, GlcNAc, and rhamnose of the oral commensal Streptococcus parasanguinis influences biofilm-forming ability.
“For example, loss of glycosylation of the Fap1 serine-rich repeat adhesin with GalNAc, GlcNAc, and rhamnose of the oral commensal Streptococcus parasanguinis influences biofilm-forming ability.36–38”
From The dental plaque biofilm matrix (2021) · cites this paper as [38]
The Results report that disrupting Fap1 glycosyltransferases reduced biofilm formation in S. parasanguinis. But the paper describes the Fap1 glycan as containing rhamnose, glucose, and GlcNAc—not GalNAc—so the claim's inclusion of GalNAc is unsupported. The cited passages have section labels but no page numbers in our copy. (LLM, conf=0.90)
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Authors: Zhu, F., Zhang, H., Yang, T., Haslam, S. M., Dell, A., & Wu, H.
Affiliations: University of Alabama at Birmingham (US)
Imperial College London (GB)
Corresponding author: Haslam, Stuart M.
Wu, Hui
ORCID: Zhu, Fan
Zhang, Hua
Yang, Tiandi
Haslam, Stuart M.
Dell, Anne
Wu, Hui
Venue: Journal of Biological Chemistry
Publisher: Elsevier BV
Published: 2016-12
Volume: 291
Issue: 53
Pages: 27354-27363
ISSN: 0021-9258 (ISSN-L)
DOI: 10.1074/jbc.m116.752998
PMC: PMC5207161
OpenAlex: W2551887876
Cited by: 34
References: 68
Citations by year: 2026: 1 · 2025: 3 · 2024: 3 · 2023: 4 · 2022: 1 · 2021: 4 · 2020: 4 · 2019: 2 · 2018: 9 · 2017: 3
FWCI: 2.43
Type: journal article
Language: en
Update notices: erratum (2018-03-30)
Open access: hybrid
doi.org
Licence: cc-by
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
creativecommons.org/licenses/by/4.0/ (vor, 1366 d)
Locations: Journal of Biological Chemistry (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion, cc-by)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Spiral (Imperial College London) (submittedVersion)
Spiral (Imperial College London) (submittedVersion, cc-by)
Funders: Biotechnology and Biological Sciences Research Council
National Institutes of Health (R01DE017954)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Glycosylation and Glycoproteins Research
Physical Sciences › Chemistry › Organic Chemistry › Carbohydrate Chemistry and Synthesis
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Structural Characterization
Keywords: Streptococcus parasanguinis, O-glycosylation, glycosyltransferases, glycosylation pathway, rhamnosyltransferase, biofilm formation, glycan engineering, bacterial adhesins
MeSH terms: Bacterial Proteins, Escherichia coli, Genetic Complementation Test, Glycoproteins, Glycosylation, Serine, Streptococcus, Gene Expression Regulation, Bacterial, Biofilms, Adhesins, Bacterial

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Engineering and Dissecting the Glycosylation Pathway of a Streptococcal Serine-rich Repeat Adhesin

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