Expulsion mechanism of the substrate-translocating subunit in ECF transporters

Chancievan Thangaratnarajah; Mark Nijland; Luís Borges-Araújo; Aike Jeucken; Jan Rheinberger; Siewert J Marrink; Paulo C T Souza; Cristina Paulino; Dirk J Slotboom

doi:10.1038/s41467-023-40266-1

Expulsion mechanism of the substrate-translocating subunit in ECF transporters

Chancievan Thangaratnarajah, Mark Nijland, Luís Borges-Araújo, Aike Jeucken, Jan Rheinberger, Siewert J Marrink, Paulo C T Souza, Cristina Paulino^*, Dirk J Slotboom^*

^*Corresponding author voor dit werk

Onderzoeksoutput › Academic › peer review

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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.

Originele taal-2	English
Artikelnummer	4484
Aantal pagina's	14
Tijdschrift	Nature Communications
Volume	14
Nummer van het tijdschrift	1
DOI's	https://doi.org/10.1038/s41467-023-40266-1
Status	Published - 25-jul.-2023

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10.1038/s41467-023-40266-1Licentie: CC BY

Expulsion mechanism of the substrate-translocating subunit in ECF transportersFinal publisher's version, 4,06 MBLicentie: CC BY

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Expulsion mechanism of the substrate-translocating subunit in ECF transporters
Thangaratnarajah, C. (Creator), Nijland, M. (Creator), Borges-Araújo, L. (Creator), Jeucken, A. (Creator), Rheinberger, J. (Creator), Marrink, S. J. (Creator), Souza, P. C. T. (Creator), Paulino, C. (Creator) & Slotboom, D. J. (Creator), ZENODO, 27-jul.-2023
DOI: 10.5281/zenodo.8116403
Dataset

oLife Fellowship Programme
Roos, W. (Hoofdonderzoeker), van der Tak, F. (Hoofdonderzoeker), Zijlstra, W. (Hoofdonderzoeker), Dobos, V. (Postdoc), Heinen, L. (Postdoc), Thangaratnarajah, C. (Postdoc), Hoekzema, M. (Postdoc), Blokhuis, A. (Postdoc), Mascotti, L. (Postdoc), Padin Santos, D. (Postdoc), Chopra, A. (Postdoc), Obermaier, S. (Postdoc), Driver, M. (Postdoc), Moreira Goulart, M. (Postdoc), Sasidharan, S. (Postdoc), Samar Mahapatra, S. (Postdoc), Zylstra, A. (Postdoc), Geiger, Y. (Postdoc), Llopis Lorente, A. (Postdoc), Aschmann, D. (Postdoc) & Kulala Vittala, S. (Postdoc)
01/04/2019 → 31/03/2024
Project: Research

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title = "Expulsion mechanism of the substrate-translocating subunit in ECF transporters",

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.",

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AU - Thangaratnarajah, Chancievan

AU - Nijland, Mark

AU - Borges-Araújo, Luís

AU - Jeucken, Aike

AU - Rheinberger, Jan

AU - Marrink, Siewert J

AU - Souza, Paulo C T

AU - Paulino, Cristina

AU - Slotboom, Dirk J

PY - 2023/7/25

Y1 - 2023/7/25

N2 - 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.

AB - 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.

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DO - 10.1038/s41467-023-40266-1

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SN - 2041-1723

VL - 14

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 4484

ER -

Expulsion mechanism of the substrate-translocating subunit in ECF transporters

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Expulsion mechanism of the substrate-translocating subunit in ECF transporters

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