Biophysical and functional characterization of the Escherichia coli Dr fimbrial envelope reveals its importance for pathogenesis and lithogenesis
13 affiliations
- 1Department of Biotechnology and Microbiology, Faculty of Chemistry, Gdańsk University of Technology, Gdańsk, Poland
- 2Division of Molecular Bacteriology, Intercollegiate Faculty of Biotechnology UG&MUG, Medical University of Gdańsk, Gdańsk, Poland
- 3Division of Biopharmacy and Pharmacokinetics, Faculty of Pharmacy, Medical University of Gdańsk, Gdańsk, Poland
- 4Department of Physics and Biophysics, Institute of Biology, Warsaw University of Life Sciences, Warsaw, Poland
- 5Centre for Advanced Materials and Technologies, Warsaw University of Technology, Warsaw, Poland
- 6Department of Physical Chemistry, Faculty of Chemistry, Gdańsk University of Technology, Gdańsk, Poland
- 7Molecular Modeling and Bioinformatics, IRB Barcelona, Barcelona, Spain
- 8University Paris-Saclay, INSERM, UMR-S 996 Inflammation, Microbiome and Immunosurveillance, Orsay, France
- 9Paris Center for Microbiome Medicine (PaCeMM) FHU, Paris, France
- 10Department of Polymer Technology, Faculty of Chemistry, Gdańsk University of Technology, Gdańsk, Poland
- 11Department of Electronics, Telecommunications and Informatics, Gdańsk University of Technology, Gdańsk, Poland
- 12Faculty of Applied Physics and Mathematics, Institute of Nanotechnology and Materials Engineering, Gdańsk University of Technology, Gdańsk, Poland
- 13Bioimaging Laboratory, Faculty of Biology, University of Gdańsk, Gdańsk, Poland
Abstract
Uropathogenic Escherichia coli strains rely on specialized surface appendages to colonize the urinary tract, including Dr fimbriae, which are strongly associated with recurrent infection and long-term persistence. Although traditionally described as receptor-binding fibers, their broader contribution to bacterial surface architecture and physicochemical behavior has remained unclear. Here, combining quantitative proteomics, computational modeling, rheology, surface physicochemistry, and flow-based adhesion assays, we show that Dr fimbriae collectively form a dense, highly hydrated amphipathic envelope surrounding the bacterial cell. Rather than functioning as isolated filaments, they generate a dynamic supramolecular layer approximately 200–300 nm thick that markedly alters whole-cell properties. Mechanistic analyses performed in a simplified laboratory model were validated in the clinical UPEC strain IH11128, demonstrating that the principal physicochemical and adhesive properties of the Dr envelope are preserved despite phase-variable fimbrial expression. The Dr envelope strongly enhanced adhesion to abiotic surfaces, particularly hydrophilic glass, where Dr-positive bacteria resisted nanonewton-range capillary detachment forces, indicating stable multipoint anchoring. The envelope also promoted selective binding to calcium oxalate (CaOx), the principal mineral component of kidney stones, under urinary conditions. In the clinical isolate, CaOx binding occurred almost exclusively within the Dr-positive subpopulation and was largely abolished by anti-Dr antibodies, demonstrating that mineral recognition depends specifically on Dr fimbriae. Beyond adhesion, the fimbrial mesh functioned as a size-selective molecular filter. Dr-positive bacteria showed markedly reduced susceptibility to large bacteriophages, whereas infection by smaller phages and susceptibility to low-molecular-weight antibiotics remained unchanged, indicating steric exclusion of large biological particles without restricting diffusion of small solutes. Together, these findings establish the Dr envelope as a multifunctional supramolecular surface architecture that governs bacterial surface physicochemistry, promotes stable urinary tract colonization, mediates CaOx recognition, and expands the adaptive capabilities of UPEC within the urinary tract. Author summary: Urinary tract infections, primarily caused by Escherichia coli, are among the most common bacterial infections, and recurrent disease is frequently associated with kidney stone formation. Some uropathogenic strains produce Dr fimbriae, surface fibers previously viewed mainly as specialized structures that help bacteria attach to host cells. Here we show that their role is much broader. We found that Dr fimbriae collectively assemble into a dense, hydrated envelope surrounding the bacterial cell, fundamentally changing the physical and chemical properties of its surface. Using a simplified laboratory model and validating the key findings in a clinical UPEC strain, we demonstrate that this envelope strengthens bacterial attachment to surfaces exposed to mechanical stress, promotes selective binding to CaOx crystals, the principal component of most kidney stones, and acts as a molecular filter that limits access of large bacteriophages while remaining permeable to small molecules. These findings identify the Dr envelope as a previously unrecognized surface architecture that may enhance bacterial persistence in the urinary tract and contribute to kidney stone-associated infections.
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BibTeX
@article{nagorka2026biophysical,
title = {{Biophysical and functional characterization of the Escherichia coli Dr fimbrial envelope reveals its importance for pathogenesis and lithogenesis}},
author = {Michalina Nagórka and Beata Zalewska-Piątek and Adam Iwanicki and Paweł Wityk and Slawomir Jakiela and Weronika Switlik and Piotr Bruździak and Miłosz Wieczór and Vanessa Liévin-Le Moal and Joanna Raczak-Gutknecht and Przemysław Gnatowski and Mateusz Ficek and Angelika Łepek and Magdalena Narajczyk and Rafał Piątek},
journal = {PLOS Pathogens},
year = {2026},
month = sep,
doi = {10.1371/journal.ppat.1014588},
url = {https://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1014588},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Biophysical and functional characterization of the Escherichia coli Dr fimbrial envelope reveals its importance for pathogenesis and lithogenesis
AU - Michalina Nagórka
AU - Beata Zalewska-Piątek
AU - Adam Iwanicki
AU - Paweł Wityk
AU - Slawomir Jakiela
AU - Weronika Switlik
AU - Piotr Bruździak
AU - Miłosz Wieczór
AU - Vanessa Liévin-Le Moal
AU - Joanna Raczak-Gutknecht
AU - Przemysław Gnatowski
AU - Mateusz Ficek
AU - Angelika Łepek
AU - Magdalena Narajczyk
AU - Rafał Piątek
PY - 2026
DA - 2026/09/16
JO - PLOS Pathogens
DO - 10.1371/journal.ppat.1014588
UR - https://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1014588
AB - Uropathogenic Escherichia coli strains rely on specialized surface appendages to colonize the urinary tract, including Dr fimbriae, which are strongly associated with recurrent infection and long-term persistence. Although traditionally described as receptor-binding fibers, their broader contribution to bacterial surface architecture and physicochemical behavior has remained unclear. Here, combining quantitative proteomics, computational modeling, rheology, surface physicochemistry, and flow-based adhesion assays, we show that Dr fimbriae collectively form a dense, highly hydrated amphipathic envelope surrounding the bacterial cell. Rather than functioning as isolated filaments, they generate a dynamic supramolecular layer approximately 200–300 nm thick that markedly alters whole-cell properties. Mechanistic analyses performed in a simplified laboratory model were validated in the clinical UPEC strain IH11128, demonstrating that the principal physicochemical and adhesive properties of the Dr envelope are preserved despite phase-variable fimbrial expression. The Dr envelope strongly enhanced adhesion to abiotic surfaces, particularly hydrophilic glass, where Dr-positive bacteria resisted nanonewton-range capillary detachment forces, indicating stable multipoint anchoring. The envelope also promoted selective binding to calcium oxalate (CaOx), the principal mineral component of kidney stones, under urinary conditions. In the clinical isolate, CaOx binding occurred almost exclusively within the Dr-positive subpopulation and was largely abolished by anti-Dr antibodies, demonstrating that mineral recognition depends specifically on Dr fimbriae. Beyond adhesion, the fimbrial mesh functioned as a size-selective molecular filter. Dr-positive bacteria showed markedly reduced susceptibility to large bacteriophages, whereas infection by smaller phages and susceptibility to low-molecular-weight antibiotics remained unchanged, indicating steric exclusion of large biological particles without restricting diffusion of small solutes. Together, these findings establish the Dr envelope as a multifunctional supramolecular surface architecture that governs bacterial surface physicochemistry, promotes stable urinary tract colonization, mediates CaOx recognition, and expands the adaptive capabilities of UPEC within the urinary tract. Author summary: Urinary tract infections, primarily caused by Escherichia coli, are among the most common bacterial infections, and recurrent disease is frequently associated with kidney stone formation. Some uropathogenic strains produce Dr fimbriae, surface fibers previously viewed mainly as specialized structures that help bacteria attach to host cells. Here we show that their role is much broader. We found that Dr fimbriae collectively assemble into a dense, hydrated envelope surrounding the bacterial cell, fundamentally changing the physical and chemical properties of its surface. Using a simplified laboratory model and validating the key findings in a clinical UPEC strain, we demonstrate that this envelope strengthens bacterial attachment to surfaces exposed to mechanical stress, promotes selective binding to CaOx crystals, the principal component of most kidney stones, and acts as a molecular filter that limits access of large bacteriophages while remaining permeable to small molecules. These findings identify the Dr envelope as a previously unrecognized surface architecture that may enhance bacterial persistence in the urinary tract and contribute to kidney stone-associated infections.
SN - 1553-7374
ER -