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Expulsion mechanism of the substrate-translocating subunit in ECF transporters

Author

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  • Chancievan Thangaratnarajah

    (University of Groningen
    University of Groningen)

  • Mark Nijland

    (University of Groningen)

  • Luís Borges-Araújo

    (CNRS and University of Lyon)

  • Aike Jeucken

    (University of Groningen)

  • Jan Rheinberger

    (University of Groningen
    University of Groningen
    University of Heidelberg)

  • Siewert J. Marrink

    (University of Groningen)

  • Paulo C. T. Souza

    (CNRS and University of Lyon)

  • Cristina Paulino

    (University of Groningen
    University of Groningen
    University of Heidelberg)

  • Dirk J. Slotboom

    (University of Groningen)

Abstract

Energy-coupling factor (ECF)-type transporters mediate the uptake of micronutrients in many bacteria. They consist of a substrate-translocating subunit (S-component) and an ATP-hydrolysing motor (ECF module) Previous data indicate that the S-component topples within the membrane to alternately expose the binding site to either side of the membrane. In many ECF transporters, the substrate-free S-component can be expelled from the ECF module. Here we study this enigmatic expulsion step by cryogenic electron microscopy and reveal that ATP induces a concave-to-convex shape change of two long helices in the motor, thereby destroying the S-component’s docking site and allowing for its dissociation. We show that adaptation of the membrane morphology to the conformational state of the motor may favour expulsion of the substrate-free S-component when ATP is bound and docking of the substrate-loaded S-component after hydrolysis. Our work provides a picture of bilayer-assisted chemo-mechanical coupling in the transport cycle of ECF transporters.

Suggested Citation

  • Chancievan Thangaratnarajah & Mark Nijland & Luís Borges-Araújo & Aike Jeucken & Jan Rheinberger & Siewert J. Marrink & Paulo C. T. Souza & Cristina Paulino & Dirk J. Slotboom, 2023. "Expulsion mechanism of the substrate-translocating subunit in ECF transporters," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40266-1
    DOI: 10.1038/s41467-023-40266-1
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    References listed on IDEAS

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    1. Ke Xu & Minhua Zhang & Qin Zhao & Fang Yu & Hui Guo & Chengyuan Wang & Fangyuan He & Jianping Ding & Peng Zhang, 2013. "Crystal structure of a folate energy-coupling factor transporter from Lactobacillus brevis," Nature, Nature, vol. 497(7448), pages 268-271, May.
    2. Ignacio Faustino & Haleh Abdizadeh & Paulo C. T. Souza & Aike Jeucken & Weronika K. Stanek & Albert Guskov & Dirk J. Slotboom & Siewert J. Marrink, 2020. "Membrane mediated toppling mechanism of the folate energy coupling factor transporter," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    3. Ioannis Manolaridis & Scott M. Jackson & Nicholas M. I. Taylor & Julia Kowal & Henning Stahlberg & Kaspar P. Locher, 2018. "Cryo-EM structures of a human ABCG2 mutant trapped in ATP-bound and substrate-bound states," Nature, Nature, vol. 563(7731), pages 426-430, November.
    4. Zhou Chen & Abhisek Mondal & Fayal Abderemane-Ali & Seil Jang & Sangeeta Niranjan & José L. Montaño & Balyn W. Zaro & Daniel L. Minor, 2023. "EMC chaperone–CaV structure reveals an ion channel assembly intermediate," Nature, Nature, vol. 619(7969), pages 410-419, July.
    5. Lin Bai & Qinglong You & Xiang Feng & Amanda Kovach & Huilin Li, 2020. "Structure of the ER membrane complex, a transmembrane-domain insertase," Nature, Nature, vol. 584(7821), pages 475-478, August.
    6. Valentina Arkhipova & Albert Guskov & Dirk J. Slotboom, 2020. "Structural ensemble of a glutamate transporter homologue in lipid nanodisc environment," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    7. Lotteke J. Y. M. Swier & Albert Guskov & Dirk J. Slotboom, 2016. "Structural insight in the toppling mechanism of an energy-coupling factor transporter," Nature Communications, Nature, vol. 7(1), pages 1-11, April.
    8. Tingliang Wang & Guobin Fu & Xiaojing Pan & Jianping Wu & Xinqi Gong & Jiawei Wang & Yigong Shi, 2013. "Structure of a bacterial energy-coupling factor transporter," Nature, Nature, vol. 497(7448), pages 272-276, May.
    9. Peng Zhang & Jiawei Wang & Yigong Shi, 2010. "Structure and mechanism of the S component of a bacterial ECF transporter," Nature, Nature, vol. 468(7324), pages 717-720, December.
    10. Susanne Hofmann & Dovile Januliene & Ahmad R. Mehdipour & Christoph Thomas & Erich Stefan & Stefan Brüchert & Benedikt T. Kuhn & Eric R. Geertsma & Gerhard Hummer & Robert Tampé & Arne Moeller, 2019. "Conformation space of a heterodimeric ABC exporter under turnover conditions," Nature, Nature, vol. 571(7766), pages 580-583, July.
    11. Charles R. Harris & K. Jarrod Millman & Stéfan J. Walt & Ralf Gommers & Pauli Virtanen & David Cournapeau & Eric Wieser & Julian Taylor & Sebastian Berg & Nathaniel J. Smith & Robert Kern & Matti Picu, 2020. "Array programming with NumPy," Nature, Nature, vol. 585(7825), pages 357-362, September.
    12. Michael L. Oldham & Dheeraj Khare & Florante A. Quiocho & Amy L. Davidson & Jue Chen, 2007. "Crystal structure of a catalytic intermediate of the maltose transporter," Nature, Nature, vol. 450(7169), pages 515-521, November.
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    1. Solène N. Lefebvre & Mark Nijland & Ivan Maslov & Dirk J. Slotboom, 2025. "Single-molecule visualization of ATP-induced dynamics of the subunit composition of an ECF transporter complex under turnover conditions," Nature Communications, Nature, vol. 16(1), pages 1-12, December.

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