Biochemical characterization of the Escherichia coli surfaceome: a focus on type I fimbriae and flagella
The Escherichia coli surfaceome consists mainly of the large surface organelles expressed by the organism to navigate and interact with the surrounding environment. The current study focuses on type I fimbriae and flagella. These large polymeric surface organelles are composed of hundreds to thousan...
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Frontiers Media S.A.
2025-02-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2025.1507286/full |
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| author | Devon W. Kavanaugh Adeline Sivignon Yannick Rossez Zina Chouit Christophe Chambon Christophe Chambon Louane Béal Mathilde Bonnet Michel Hébraud Michel Hébraud Yann Guérardel Hang Thi Thu Nguyen Nicolas Barnich |
| author_facet | Devon W. Kavanaugh Adeline Sivignon Yannick Rossez Zina Chouit Christophe Chambon Christophe Chambon Louane Béal Mathilde Bonnet Michel Hébraud Michel Hébraud Yann Guérardel Hang Thi Thu Nguyen Nicolas Barnich |
| author_sort | Devon W. Kavanaugh |
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| description | The Escherichia coli surfaceome consists mainly of the large surface organelles expressed by the organism to navigate and interact with the surrounding environment. The current study focuses on type I fimbriae and flagella. These large polymeric surface organelles are composed of hundreds to thousands of subunits, with their large size often preventing them from being studied in their native form. Recent studies are accumulating which demonstrate the glycosylation of surface proteins or virulence factors in pathogens, including E. coli. Using biochemical and glycobiological techniques, including biotin-hydrazide labeling of glycans and chemical and glycosidase treatments, we demonstrate (i) the presence of a well-defined and chemically resistant FimA oligomer in several strains of pathogenic and non-pathogenic E. coli, (ii) the major subunit of type I fimbriae, FimA, in pathogenic and laboratory strains is recognized by concanavalin A, (iii) standard methods to remove N-glycans (PNGase F) or a broad-specificity mannosidase fail to remove the glycan structure, despite the treatments resulting in altered migration in SDS-PAGE, (iv) PNGase F treatment results in a novel 32 kDa band recognized by anti-FliC antiserum. While the exact identity of the glycan(s) and their site of attachment currently elude detection by conventional glycomics/glycoproteomics, the current findings highlight a potential additional layer of complexity of the surface (glyco) proteome of the commensal or adhesive and invasive E. coli strains studied. |
| format | Article |
| id | doaj-art-27677614f7ff4331bd069ac644113eb5 |
| institution | Kabale University |
| issn | 1664-302X |
| language | English |
| publishDate | 2025-02-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Microbiology |
| spelling | doaj-art-27677614f7ff4331bd069ac644113eb52025-02-05T23:05:22ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-02-011610.3389/fmicb.2025.15072861507286Biochemical characterization of the Escherichia coli surfaceome: a focus on type I fimbriae and flagellaDevon W. Kavanaugh0Adeline Sivignon1Yannick Rossez2Zina Chouit3Christophe Chambon4Christophe Chambon5Louane Béal6Mathilde Bonnet7Michel Hébraud8Michel Hébraud9Yann Guérardel10Hang Thi Thu Nguyen11Nicolas Barnich12Université Clermont Auvergne, Inserm, INRAE, M2iSH, Université Clermont Auvergne, Clermont–Ferrand, FranceUniversité Clermont Auvergne, Inserm, INRAE, M2iSH, Université Clermont Auvergne, Clermont–Ferrand, FranceUnité de Glycobiologie Structurale et Fonctionnelle (UGSF), Université de Lille, Lille, FranceUnité de Glycobiologie Structurale et Fonctionnelle (UGSF), Université de Lille, Lille, FrancePlateforme d’Exploration du Métabolisme, Composante Protéomique (PFEMcp), Theix, FranceUR 0370 Qualité des Produits Animaux (QuaPA), INRAE, Theix, FranceUniversité Clermont Auvergne, Inserm, INRAE, M2iSH, Université Clermont Auvergne, Clermont–Ferrand, FranceUniversité Clermont Auvergne, Inserm, INRAE, M2iSH, Université Clermont Auvergne, Clermont–Ferrand, FrancePlateforme d’Exploration du Métabolisme, Composante Protéomique (PFEMcp), Theix, FranceUniversité Clermont Auvergne, INRAE, Microbiologie Environnement Digestif Santé (MEDiS), Clermont–Ferrand, FranceUnité de Glycobiologie Structurale et Fonctionnelle (UGSF), Université de Lille, Lille, FranceUniversité Clermont Auvergne, Inserm, INRAE, M2iSH, Université Clermont Auvergne, Clermont–Ferrand, FranceUniversité Clermont Auvergne, Inserm, INRAE, M2iSH, Université Clermont Auvergne, Clermont–Ferrand, FranceThe Escherichia coli surfaceome consists mainly of the large surface organelles expressed by the organism to navigate and interact with the surrounding environment. The current study focuses on type I fimbriae and flagella. These large polymeric surface organelles are composed of hundreds to thousands of subunits, with their large size often preventing them from being studied in their native form. Recent studies are accumulating which demonstrate the glycosylation of surface proteins or virulence factors in pathogens, including E. coli. Using biochemical and glycobiological techniques, including biotin-hydrazide labeling of glycans and chemical and glycosidase treatments, we demonstrate (i) the presence of a well-defined and chemically resistant FimA oligomer in several strains of pathogenic and non-pathogenic E. coli, (ii) the major subunit of type I fimbriae, FimA, in pathogenic and laboratory strains is recognized by concanavalin A, (iii) standard methods to remove N-glycans (PNGase F) or a broad-specificity mannosidase fail to remove the glycan structure, despite the treatments resulting in altered migration in SDS-PAGE, (iv) PNGase F treatment results in a novel 32 kDa band recognized by anti-FliC antiserum. While the exact identity of the glycan(s) and their site of attachment currently elude detection by conventional glycomics/glycoproteomics, the current findings highlight a potential additional layer of complexity of the surface (glyco) proteome of the commensal or adhesive and invasive E. coli strains studied.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1507286/fulltype I fimbriaeflagellapost-translational modificationpathobiontglycobiologystructural characterization |
| spellingShingle | Devon W. Kavanaugh Adeline Sivignon Yannick Rossez Zina Chouit Christophe Chambon Christophe Chambon Louane Béal Mathilde Bonnet Michel Hébraud Michel Hébraud Yann Guérardel Hang Thi Thu Nguyen Nicolas Barnich Biochemical characterization of the Escherichia coli surfaceome: a focus on type I fimbriae and flagella Frontiers in Microbiology type I fimbriae flagella post-translational modification pathobiont glycobiology structural characterization |
| title | Biochemical characterization of the Escherichia coli surfaceome: a focus on type I fimbriae and flagella |
| title_full | Biochemical characterization of the Escherichia coli surfaceome: a focus on type I fimbriae and flagella |
| title_fullStr | Biochemical characterization of the Escherichia coli surfaceome: a focus on type I fimbriae and flagella |
| title_full_unstemmed | Biochemical characterization of the Escherichia coli surfaceome: a focus on type I fimbriae and flagella |
| title_short | Biochemical characterization of the Escherichia coli surfaceome: a focus on type I fimbriae and flagella |
| title_sort | biochemical characterization of the escherichia coli surfaceome a focus on type i fimbriae and flagella |
| topic | type I fimbriae flagella post-translational modification pathobiont glycobiology structural characterization |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2025.1507286/full |
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