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An outer membrane porin-lipoprotein complex modulates elongasome movement to establish cell curvature in Rhodospirillum rubrum

Author

Listed:
  • Sebastian Pöhl

    (University of Marburg)

  • Giacomo Giacomelli

    (Kiel University)

  • Fabian M. Meyer

    (Kiel University)

  • Volker Kleeberg

    (University of Freiburg
    Pädagogische Forschungsstelle Kassel)

  • Eli J. Cohen

    (Imperial College London)

  • Jacob Biboy

    (Institute for Cell and Molecular Biosciences, Newcastle University)

  • Julia Rosum

    (University of Marburg)

  • Timo Glatter

    (Max Planck Institute for Terrestrial Microbiology)

  • Waldemar Vollmer

    (Institute for Cell and Molecular Biosciences, Newcastle University
    University of Queensland)

  • Muriel C. F. Teeseling

    (University of Marburg
    Friedrich-Schiller-Universität)

  • Johann Heider

    (University of Marburg
    Center for Synthetic Microbiology (SYNMIKRO))

  • Marc Bramkamp

    (Kiel University)

  • Martin Thanbichler

    (University of Marburg
    Center for Synthetic Microbiology (SYNMIKRO)
    Max Planck Institute for Terrestrial Microbiology)

Abstract

Curved cell shapes are widespread among bacteria and important for cellular motility, virulence and fitness. However, the underlying morphogenetic mechanisms are still incompletely understood. Here, we identify an outer-membrane protein complex that promotes cell curvature in the photosynthetic species Rhodospirillum rubrum. We show that the R. rubrum porins Por39 and Por41 form a helical ribbon-like structure at the outer curve of the cell that recruits the peptidoglycan-binding lipoprotein PapS, with PapS inactivation, porin delocalization or disruption of the porin-PapS interface resulting in cell straightening. We further demonstrate that porin-PapS assemblies act as molecular cages that entrap the cell elongation machinery, thus biasing cell growth towards the outer curve. These findings reveal a mechanistically distinct morphogenetic module mediating bacterial cell shape. Moreover, they uncover an unprecedented role of outer-membrane protein patterning in the spatial control of intracellular processes, adding an important facet to the repertoire of regulatory mechanisms in bacterial cell biology.

Suggested Citation

  • Sebastian Pöhl & Giacomo Giacomelli & Fabian M. Meyer & Volker Kleeberg & Eli J. Cohen & Jacob Biboy & Julia Rosum & Timo Glatter & Waldemar Vollmer & Muriel C. F. Teeseling & Johann Heider & Marc Bra, 2024. "An outer membrane porin-lipoprotein complex modulates elongasome movement to establish cell curvature in Rhodospirillum rubrum," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51790-z
    DOI: 10.1038/s41467-024-51790-z
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    References listed on IDEAS

    as
    1. Alexandre Persat & Howard A. Stone & Zemer Gitai, 2014. "The curved shape of Caulobacter crescentus enhances surface colonization in flow," Nature Communications, Nature, vol. 5(1), pages 1-9, September.
    2. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    3. Nikolai Peschek & Roman Herzog & Praveen K. Singh & Marcel Sprenger & Fabian Meyer & Kathrin S. Fröhlich & Luise Schröger & Marc Bramkamp & Knut Drescher & Kai Papenfort, 2020. "RNA-mediated control of cell shape modulates antibiotic resistance in Vibrio cholerae," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    4. Emma J. Banks & Mauricio Valdivia-Delgado & Jacob Biboy & Amber Wilson & Ian T. Cadby & Waldemar Vollmer & Carey Lambert & Andrew L. Lovering & R. Elizabeth Sockett, 2022. "Asymmetric peptidoglycan editing generates cell curvature in Bdellovibrio predatory bacteria," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Gideon Mamou & Federico Corona & Ruth Cohen-Khait & Nicholas G. Housden & Vivian Yeung & Dawei Sun & Pooja Sridhar & Manuel Pazos & Timothy J. Knowles & Colin Kleanthous & Waldemar Vollmer, 2022. "Peptidoglycan maturation controls outer membrane protein assembly," Nature, Nature, vol. 606(7916), pages 953-959, June.
    6. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
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