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Assembly mechanism of a Tad secretion system secretin-pilotin complex

Author

Listed:
  • Matteo Tassinari

    (Imperial College
    Human Technopole)

  • Marta Rudzite

    (Imperial College)

  • Alain Filloux

    (Imperial College
    Nanyang Technological University)

  • Harry H. Low

    (Imperial College)

Abstract

The bacterial Tight adherence Secretion System (TadSS) assembles surface pili that drive cell adherence, biofilm formation and bacterial predation. The structure and mechanism of the TadSS is mostly unknown. This includes characterisation of the outer membrane secretin through which the pilus is channelled and recruitment of its pilotin. Here we investigate RcpA and TadD lipoprotein from Pseudomonas aeruginosa. Light microscopy reveals RcpA colocalising with TadD in P. aeruginosa and when heterologously expressed in Escherichia coli. We use cryogenic electron microscopy to determine how RcpA and TadD assemble a secretin channel with C13 and C14 symmetries. Despite low sequence homology, we show that TadD shares a similar fold to the type 4 pilus system pilotin PilF. We establish that the C-terminal four residues of RcpA bind TadD - an interaction essential for secretin formation. The binding mechanism between RcpA and TadD appears distinct from known secretin-pilotin pairings in other secretion systems.

Suggested Citation

  • Matteo Tassinari & Marta Rudzite & Alain Filloux & Harry H. Low, 2023. "Assembly mechanism of a Tad secretion system secretin-pilotin complex," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41200-1
    DOI: 10.1038/s41467-023-41200-1
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    1. 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.
    2. Yangqi Gu & Vishok Srikanth & Aldo I. Salazar-Morales & Ruchi Jain & J. Patrick O’Brien & Sophia M. Yi & Rajesh Kumar Soni & Fadel A. Samatey & Sibel Ebru Yalcin & Nikhil S. Malvankar, 2021. "Structure of Geobacter pili reveals secretory rather than nanowire behaviour," Nature, Nature, vol. 597(7876), pages 430-434, September.
    3. Rebecca Conners & Mathew McLaren & Urszula Łapińska & Kelly Sanders & M. Rhia L. Stone & Mark A. T. Blaskovich & Stefano Pagliara & Bertram Daum & Jasna Rakonjac & Vicki A. M. Gold, 2021. "CryoEM structure of the outer membrane secretin channel pIV from the f1 filamentous bacteriophage," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    4. Sara J. Weaver & Davi R. Ortega & Matthew H. Sazinsky & Triana N. Dalia & Ankur B. Dalia & Grant J. Jensen, 2020. "Publisher Correction: CryoEM structure of the type IVa pilus secretin required for natural competence in Vibrio cholera," Nature Communications, Nature, vol. 11(1), pages 1-1, December.
    5. David Tomasek & Shaun Rawson & James Lee & Joseph S. Wzorek & Stephen C. Harrison & Zongli Li & Daniel Kahne, 2020. "Structure of a nascent membrane protein as it folds on the BAM complex," Nature, Nature, vol. 583(7816), pages 473-478, July.
    6. J. Hu & L. J. Worrall & C. Hong & M. Vuckovic & C. E. Atkinson & N. Caveney & Z. Yu & N. C. J. Strynadka, 2018. "Cryo-EM analysis of the T3S injectisome reveals the structure of the needle and open secretin," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    7. Sara J. Weaver & Davi R. Ortega & Matthew H. Sazinsky & Triana N. Dalia & Ankur B. Dalia & Grant J. Jensen, 2020. "CryoEM structure of the type IVa pilus secretin required for natural competence in Vibrio cholerae," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    8. 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.
    9. Anastasia A. Chernyatina & Harry H. Low, 2019. "Core architecture of a bacterial type II secretion system," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    10. L. J. Worrall & C. Hong & M. Vuckovic & W. Deng & J. R. C. Bergeron & D. D Majewski & R. K. Huang & T. Spreter & B. B. Finlay & Z. Yu & N. C. J. Strynadka, 2016. "Near-atomic-resolution cryo-EM analysis of the Salmonella T3S injectisome basal body," Nature, Nature, vol. 540(7634), pages 597-601, December.
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    1. Michael Hohl & Emma J. Banks & Max P. Manley & Tung B. K. Le & Harry H. Low, 2024. "Bidirectional pilus processing in the Tad pilus system motor CpaF," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Shuaiqi Guo & Yunjie Chang & Yves V. Brun & P. Lynne Howell & Lori L. Burrows & Jun Liu, 2024. "PilY1 regulates the dynamic architecture of the type IV pilus machine in Pseudomonas aeruginosa," Nature Communications, Nature, vol. 15(1), pages 1-12, December.

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