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Stochastic chain termination in bacterial pilus assembly

Author

Listed:
  • Christoph Giese

    (ETH Zurich)

  • Chasper Puorger

    (ETH Zurich
    University of Applied Sciences and Arts Northwestern Switzerland)

  • Oleksandr Ignatov

    (ETH Zurich
    V.I. Grishchenko Clinic of Reproductive Medicine)

  • Zuzana Bečárová

    (ETH Zurich)

  • Marco E. Weber

    (ETH Zurich
    ETH Zurich)

  • Martin A. Schärer

    (ETH Zurich
    Paul Scherrer Institute)

  • Guido Capitani

    (Paul Scherrer Institute)

  • Rudi Glockshuber

    (ETH Zurich)

Abstract

Adhesive type 1 pili from uropathogenic Escherichia coli strains are filamentous, supramolecular protein complexes consisting of a short tip fibrillum and a long, helical rod formed by up to several thousand copies of the major pilus subunit FimA. Here, we reconstituted the entire type 1 pilus rod assembly reaction in vitro, using all constituent protein subunits in the presence of the assembly platform FimD, and identified the so-far uncharacterized subunit FimI as an irreversible assembly terminator. We provide a complete, quantitative model of pilus rod assembly kinetics based on the measured rate constants of FimD-catalyzed subunit incorporation. The model reliably predicts the length distribution of assembled pilus rods as a function of the ratio between FimI and the main pilus subunit FimA and is fully consistent with the length distribution of membrane-anchored pili assembled in vivo. The results show that the natural length distribution of adhesive pili formed via the chaperone-usher pathway results from a stochastic chain termination reaction. In addition, we demonstrate that FimI contributes to anchoring the pilus to the outer membrane and report the crystal structures of (i) FimI in complex with the assembly chaperone FimC, (ii) the FimI-FimC complex bound to the N-terminal domain of FimD, and (iii) a ternary complex between FimI, FimA and FimC that provides structural insights on pilus assembly termination and pilus anchoring by FimI.

Suggested Citation

  • Christoph Giese & Chasper Puorger & Oleksandr Ignatov & Zuzana Bečárová & Marco E. Weber & Martin A. Schärer & Guido Capitani & Rudi Glockshuber, 2023. "Stochastic chain termination in bacterial pilus assembly," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43449-y
    DOI: 10.1038/s41467-023-43449-y
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    References listed on IDEAS

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    1. Natalia Pakharukova & Henri Malmi & Minna Tuittila & Tobias Dahlberg & Debnath Ghosal & Yi-Wei Chang & Si Lhyam Myint & Sari Paavilainen & Stefan David Knight & Urpo Lamminmäki & Bernt Eric Uhlin & Ma, 2022. "Archaic chaperone–usher pili self-secrete into superelastic zigzag springs," Nature, Nature, vol. 609(7926), pages 335-340, September.
    2. Minge Du & Zuanning Yuan & Hongjun Yu & Nadine Henderson & Samema Sarowar & Gongpu Zhao & Glenn T. Werneburg & David G. Thanassi & Huilin Li, 2018. "Handover mechanism of the growing pilus by the bacterial outer-membrane usher FimD," Nature, Nature, vol. 562(7727), pages 444-447, October.
    3. Michael Vetsch & Chasper Puorger & Thomas Spirig & Ulla Grauschopf & Eilika U. Weber-Ban & Rudi Glockshuber, 2004. "Pilus chaperones represent a new type of protein-folding catalyst," Nature, Nature, vol. 431(7006), pages 329-333, September.
    4. Sebastian Geibel & Erik Procko & Scott J. Hultgren & David Baker & Gabriel Waksman, 2013. "Structural and energetic basis of folded-protein transport by the FimD usher," Nature, Nature, vol. 496(7444), pages 243-246, April.
    5. Gilles Phan & Han Remaut & Tao Wang & William J. Allen & Katharina F. Pirker & Andrey Lebedev & Nadine S. Henderson & Sebastian Geibel & Ender Volkan & Jun Yan & Micha B. A. Kunze & Jerome S. Pinkner , 2011. "Crystal structure of the FimD usher bound to its cognate FimC–FimH substrate," Nature, Nature, vol. 474(7349), pages 49-53, June.
    6. Minge Du & Zuanning Yuan & Glenn T. Werneburg & Nadine S. Henderson & Hemil Chauhan & Amanda Kovach & Gongpu Zhao & Jessica Johl & Huilin Li & David G. Thanassi, 2021. "Processive dynamics of the usher assembly platform during uropathogenic Escherichia coli P pilus biogenesis," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
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    1. Dawid S. Zyla & Thomas Wiegand & Paul Bachmann & Rafal Zdanowicz & Christoph Giese & Beat H. Meier & Gabriel Waksman & Manuela K. Hospenthal & Rudi Glockshuber, 2024. "The assembly platform FimD is required to obtain the most stable quaternary structure of type 1 pili," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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