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Cited by 3Gut microbiota and healthBiochemical and Structural CharacterizationBacterial Genetics and Biotechnology

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Segmented filamentous bacteria undergo a structural transition at their adhesive tip during unicellular to filament development

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Cruz, Ana Raquel, Wimmer, Benedikt H., Teo, Teck Hui, Pehau-Arnaudet, Gérard, Winter, Jean-Marie, Gazi, Anastasia D., Lafaye, Pierre, Brier, Sébastien, Legrand, Agnès, Dubrovsky-Gaupp, Anna, Bérard, Marion, Aymé, Gabriel, Sartori-Rupp, Anna, Medalia, Ohad, Schnupf, Pamela·2025·Nature Communications
DOI 10.1038/s41467-025-66892-5PMC PMC12780176

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Abstract

Segmented filamentous bacteria (SFB) are intestinal commensals that promote immune system development and pathogen protection through intimate attachment to the ileal epithelium. Attachment occurs via the tip of unicellular teardrop-shaped SFB, called intracellular offsprings (IOs), before outgrowth into filaments. To characterize this critical stage of the SFB life cycle, we imaged SFB using cryo-electron microscopy and tomography. IOs were surrounded by a repetitive surface (S)-layer that became replaced by disordered hair-like structures specifically at the IO tip. During outgrowth into filaments, the S-layer was exchanged for a morphologically distinct repetitive hair-like layer. The bacterial structures and morphological transition were conserved across SFB from mouse and rat origin, while growth of mouse-SFB under non-attachment conditions in a heterologous host affected the SFB tip length and relative proportion of the tip stages. Moreover, a major Th17 and B cell antigen, while being a ubiquitous cell wall-associated protein, was immunologically accessible only at the filament tip, underscoring the unique properties of the tip structure. This study identifies an IO-specific S-layer and reveals a conserved developmental transition of the SFB tip surface including the transient appearance of structures consistent in location and timing with being involved in host cell attachment.

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Metadata

Authors
Cruz, A. R., Wimmer, B. H., Teo, T. H., Pehau-Arnaudet, G., Winter, J.-M., Gazi, A. D., Lafaye, P., Brier, S., Legrand, A., Dubrovsky-Gaupp, A., Bérard, M., Aymé, G., Sartori-Rupp, A., Medalia, O., & Schnupf, P.
Affiliations
  • University of Zurich (CH)
  • Agency for Science, Technology and Research (SG)
  • Institut Pasteur (FR)
  • Centre National de la Recherche Scientifique (FR)
Corresponding author
Schnupf, Pamela
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2025-12-17
Volume
17
Issue
1
Pages
222-222
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/s41467-025-66892-5
PMC
PMC12780176
OpenAlex
W4417424135
Cited by
3
References
3
Citations by year
2026: 3
FWCI
0.90
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, other-oa)
  • PubMed (publishedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • HAL (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Zurich Open Repository and Archive (University of Zurich) (submittedVersion, cc-by)
  • Zurich Open Repository and Archive (University of Zurich)
Funders
  • Bill and Melinda Gates Foundation (OPP1141322)
  • Infrastructures en Biologie Santé et Agronomie
  • Equipex (ANR-11-EQPX-0008)
  • Agence Nationale de la Recherche (ANR-10–INSB–04, 10-LABX-62-IBEID, ANR-10–INSB–04-01, 10-INSB-04-01, ANR‐10‐LABX‐62‐IBEID, LABX-62-IBEID, ANR-10, ANR-10-LABX, ANR-10-LABX-0062, ANR-10-INBS-0004, ANR-10-LABX-62, ANR-11-EQPX-0008)
  • Institut National de la Santé et de la Recherche Médicale (ANR-10-INSB-04-01, ANR-10-LABX-62-IBEID)
  • Centre National de la Recherche Scientifique (ANR-10-LABX-62-IBEID, 10-LABX-62-IBEID, ANR-10-LABX-62)
  • Universität Zürich
  • Fondation Bettencourt Schueller (R19214KK)
  • Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Structural Characterization
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords
segmented filamentous bacteria, surface layer, host cell attachment, ileal epithelium, bacterial life cycle, B-cell antigens, commensal bacteria, cryo-electron tomography
MeSH terms
Animals, Bacteria, Bacterial Adhesion, Ileum, Intestinal Mucosa, Mice, Inbred C57BL, Cryoelectron Microscopy, Mice, Rats

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